Cuadernos de herpetología vol. 34 n° 2 - 2020 by Cuadernos de Herpetología

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HERPETOLOGÍA VOLUMEN 34 - NUMERO 2 - SEPTIEMBRE 2020 ppct.caicyt.gov.ar/index.php/cuadherpetol/

Revista de la Asociación Herpetológica Argentina

Volumen 34 - Número 2 - Septiembre 2020

C UADERNOS de HERPETOLOGÍA

Revista de la Asociación Herpetológica Argentina

Cuad. herpetol. 34 (2): 135-143 (2020)

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Bushmaster bites in Brazil: ecological niche modeling and spatial analysis to improve human health measures Nathalie Citeli1,2,3, Mariana de-Carvalho4, Bruno Moreira de Carvalho5, Mônica de Avelar Figueiredo Mafra Magalhães6, Rosany Bochner1 Sistema Nacional de Informações Tóxico-Farmacológicas (SINITOX), Fundação Oswaldo Cruz, Instituto de Informação e Comunicação Científica e Tecnológica em Saúde, Fundação Oswaldo Cruz, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ 21040-900, Brasil. 2 Laboratório de Fauna e Unidades de Conservação, Universidade de Brasília, Brasília, Distrito Federal, DF 70910-900, Brasil. 3 Laboratório de Anatomia Comparada dos Vertebrados, Universidade de Brasília, Distrito Federal, DF 70910900, Brasil. 4 Laboratório de Comportamento Animal, Universidade de Brasília, Distrito Federal, DF 70910-900, Brasil. 5 Laboratório de Vigilância Entomológica em Diptera e Hemiptera, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ 21040-900, Brasil. 6 Núcleo de Geoprocessamento, Laboratório de Informação em Saúde, Instituto de Informação e Comunicação Científica e Tecnológica em Saúde, Fundação Oswaldo Cruz, Av. Brasil 4365, Manguinhos, Rio de Janeiro, RJ 21040-900, Brasil. 1

Recibido: 20 S eptiembre 2019 Revisado: 17 Marzo 2020 Aceptado: 03 Junio 2020 Editor Asociado:

P. Pa s s o s

doi: 10.31017/CdH.2020.(2019-033)

ABSTRACT In 2017, the World Health Organization has included snakebites in category A on the list of neglected tropical diseases, i.e., with a high impact on world health, not receiving the necessary attention. It is fundamental to prevent this health issue through the cooperation among different areas of knowledge. Our goals here were to identify the potential geographical distribution of the largest venomous American snake Lachesis muta (the Bushmaster), to support the planning of antivenom distribution in Brazil and mitigate this disease, once this species may cause serious accidents with a high risk of death. Occurrence records of the species were obtained from scientific collections. Data on antivenom distribution were obtained from the Ministry of Health and State Secretaries of Health. Our results showed climatic suitability for L. muta in 60% of the Brazilian territory, including the Amazon and the Atlantic Forest. The highest incidence rates and suitability values were recorded for the northern region, which is a priority for the mitigation of this disease. Our results may help planning efficient antivenom distribution. We also encourage mapping the distribution of other venomous species to identify areas of occurrence and improve human health measures. Key words: Anti-botropic-laquetic serum, Maximum entropy modeling of species, Ophidian accidents, Prevalence, Venomous snake.

Introduction Venomous snakes occur in most parts of the world, consequently there are snakebites, which can lead to serious public health problems, with high morbidity and mortality (Gutiérrez et al. 2006; 2010; Uetz et al., 2018). Annually, about 2 million people are affected by snakebites, mostly in poor communities and in developing countries in tropical regions (Kasturiratne et al., 2008; Harrison et al., 2009). More than a

half of the victims need specific medical treatment, such as the administration of antivenom (WHO, 2018), often monospecific antivenom (e.g., Habib and Warrel, 2013). Antivenom is safe and effective to minimize mortality and morbidity caused by snakebites (WHO, 2018). The crisis in the production, deployment, and accessibility of this product is a concern

Author for correspondence: citeli@outlook.com

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N. Citeli et al. - Bushmaster bites and antivenom distribution in Brazil in many parts of the world (e.g., Theakston and Warrell, 2000). Antivenoms are costly, often scarce and poorly distributed in areas where they are most needed (Gutiérrez et al., 2006; Michael et al., 2018; Schioldann et al., 2018). Building an operating system by organizing local epidemiological data and anticipating the occurrence of accidents can be the first step to decrease public health problems (Chippaux, 2017). This operating system is relevant for the appropriate distribution of antivenoms since the distribution of these products should be guided by the species’ distribution ranges and epidemiological data (Gutiérrez et al., 2009). Currently, the distribution of antivenom to Brazilian States of the federation is done by the Ministry of Health just based on epidemiological data (Gutiérrez et al., 2009). Ecological niche modeling can be useful to predict regions of epidemiological importance, as it highlights regions of high suitability for a given species (i.e., venomous snakes), providing information on areas that are potentially occupied by such species but were not previously investigated (Needleman et al., 2018). Consequently, these models can guide and support the distribution of antivenom, which is expensive and scarce (Gutiérrez et al., 2009; Chippaux et al., 2015). However, most studies about snakebites and their epidemiological importance have only focused on the description of the clinical aspects of the envenomation (Kasturiratne et al., 2008). Given the importance of the effective distribution of antivenom, our goal was to determine the potential distribution of a large venomous snake, Lachesis muta (Linnaeus, 1766) (Bushmaster) and its relation with the location of healthcare service for snakebite assistance in Brazil and the snakebite events caused by this species. Considering the areas of high suitability for this species, we also propose priority regions that should receive the Lachesis antivenom, the anti-botropic-laquetic serum (SABL). Despite the frequency of bushmaster’s bites is lower than the others venomous snakes’ (e.g., Bothrops spp.), from a clinical point of view, it is still an important snakebite, configuring a public health problem in Brazil. However, the available literature about the detailed distribution of this species and envenomation is scarce. The present study is the first to propose actions to reduce the burden of Lachesis muta snakebites in Brazil through ecological niche modeling. It may also be a model for similar studies with other venomous species in other countries and regions worldwide. 136

Materials and methods To identify if the regions with suitability for Lachesis muta have available healthcare services and if they correspond to the areas with snakebite records, we surveyed the occurrence of L. muta in South America, and used these dataset to select the least correlated bioclimatic variables. We used these variables to build a potential distribution model for L. muta using the Maxent algorithm, and then we identify and mapped the municipalities that counted on healthcare services. We also surveyed the number of snakebites and calculated their incidence rates by municipality between 2006 and 2017. Study species The genus Lachesis (Bushmaster) comprises the largest venomous snakes in the Americas, reaching up to 3.5 m of total length (Campbell and Lamar, 2004). All bushmaster’s snakebites are considered critical, posing a high risk of death (Haad, 1981; Jorge et al., 1997; Souza et al., 2007) or causing irreversible sequelae, such as necrosis (e.g., Rosenthal et al., 2002). In Brazil, there is only one species of the genus, Lachesis muta (see Fernandes et al., 2004). It has been recorded from Panama to southeastern Brazil, in tropical rainforests such as the Amazonia and the Atlantic Forest (Campbell and Lamar, 2004; Fernandes et al., 2004; Almeida et al., 2007). It inhabits well-preserved forests, with high humidity levels and temperature usually ranging from 24-28° C (Melgarejo, 2002). Lachesis muta is sensitive to handling, because it has little resistance to injuries and rarely tolerates the stress caused by capture and transportation (Melgarejo, 2002). Due to these sensitivity, captive breeding is quite complex, and consequently, the production of its antivenom is expensive and scarce. Therefore, there is a need to send medication serum to strategic locations to avoid wastes. Since the clinical symptomatology of the bushmaster’s snakebites can be mistaken with the ones caused by another snake of the same family, Bothrops, a pentavalent antivenom is used in Brazil (Ministry of Health, personal communication) to cope with accidents caused by either of these two snakes: the anti-botropic-laquetic serum (SABL). Lachesis muta occurrences The identification and mapping of museum specimens can be used to produce ecological niche mo-

Cuad. herpetol. 34 (2): 135-143 (2020) deling maps to indicate potential areas of occurrence in Brazil. We obtained data on Lachesis muta occurrence records from the following herpetological collections: Museu Nacional, Universidade Federal do Rio de Janeiro (MNRJ), Coleção Científica do Instituto Vital Brazil (CCIVB) and Museu de Zoologia da Universidade de São Paulo (MUZUSP). In addition, we included available records from the online databases: Specieslink (splink.org.br) and GBIF (https://www.gbif.org/): Brazil: Amazonas: Coleção Herpetológica do Instituto Nacional de Pesquisas Amazônicas (INPA-HERPETO); Bahia: Coleção de Serpentes do Museu de História Natural da Bahia (CRMZUFBA); Mato Grosso: Herpetologia-Répteis Coleção Científica de Serpentes da Universidade Federal do Mato Grosso (UFMT-R); Minas Gerais: Coleção Científica de Serpentes da Fundação Ezequiel Dias (FUNED-SERP); Coleção de Répteis do Centro de Taxonomia da Universidade Federal do Rio de Janeiro (UFMG-REP); Pará: Coleção Herpetológica do Museu Paraense Emílio Goeldi (MPEG.HOP); Rio Grande do Sul: Coleção de Répteis do Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul (MCT-PUCRS); São Paulo: Coleção de Répteis do Museu de Zoologia da Universidade de Campinas (ZUEC-REP); Coleção Herpetológica Alphonse Richard Hoge (Instituto Butantan - IBSP); Colombia: Bogota: Museo de La Salle – Universidad de La Salle (MLS-of); Fundación Puerto Rastrojo (FPR - Colombia) and United States of America: Washington: Smithsonian National Museum of Natural History (NMNH-Animalia_BR). To minimize possible misidentification of specimens, all occurrences referred as "observations", without a voucher specimen held by a scientific collection, were excluded. To build accurate maps, we only considered the specific geographical coordinates informed by the collectors, and excluded unspecified coordinates of municipal headquarters. Climate Variables We used nineteen bioclimatic variables from World -Clim – Global Climate Data (www.worldclim.org) version 2.0, restricted to the period between 19702000, with a resolution of 2.5 arc minutes (ca., 5 km) (Fick and Hijmans, 2017) for South America. We performed a principal component analysis (PCA) in the R environment (version 3.4.1; R Core Team, 2017) using vegan (Oksanen et al., 2017), dismo (Hijmans et al., 2017) and rgdal packages (Bivand et al., 2017) to identify a subset of available biocli-

matic variables that were not strongly correlated (R2 < 0.7). Variables were chosen according to Lachesis muta’s ecological characteristics (see Lachesis muta section; Cunha and Nascimento, 1978; Melgarejo, 2002; Campbell and Lamar, 2004). Thus, we selected seven variables for the model: mean temperature diurnal range, isothermality, maximum temperature of warmest month, minimum temperature of coldest month, precipitation of wettest month, precipitation of driest month, and precipitation of warmest quarter. Healthcare services The distribution process of the antivenom is decentralized and based on the needs of each region along the country. To determine which regions of suitability for Lachesis muta have medical assistance for snakebites, we identified municipalities with healthcare services by requesting this information to each federative unit (total = 26). We used online protocols related to the Brazilian Law of Access to Public Information (Law No. 12,527, November 18, 2011; Brasil, 2011). The geographic coordinates were obtained from the Brazilian Institute of Geography and Statistics (IBGE), datum Sirgas 2000. Ecological Niche Models We used the Maximum Entropy algorithm - MaxEnt (Phillips et al., 2006) for modeling the potential areas of occurrence of Lachesis muta, one of the most popular and high-performance algorithms for ecological niche modeling (Hijmans and Graham, 2006; Fourcade et al., 2014). This algorithm has a high performance and less sensitivity to possible geographical positioning errors (Hijmans and Graham, 2006; Fourcade et al., 2014). Occurrences were randomly separated into 70% for training and 30% for validating the model, with 1000 bootstrap pseudoreplicates. We used the area under the ROC curve (AUC) for accessing the model performance, where values closer to 1 indicate a better agreement between model outputs and the test occurrences. A less conservative threshold (minimum training presence) was applied to MaxEnt’s outputs to build the final binary map at Quantum GIS 2.18.1 (QGIS Development Team, 2016). To validate the final map, we considered the literature about Lachesis muta that suggests the Atlantic Forest of Rio de Janeiro state (Brazilian coast) and the Amazon region of Mato Grosso state (central-western Brazil) are the south and southwest limit regions for the species’ distribution, respectively (e.g., Cunha 137

N. Citeli et al. - Bushmaster bites and antivenom distribution in Brazil and Nascimento, 1978; Campbell and Lamar, 2004; Fernandes et al., 2004; Melgarejo, 2009). A recent biogeographic analysis showed L. muta does not occur in the southern Atlantic Forest (Moura et al., 2016). Therefore, these regions were removed from the analyses performed here. Snakebites by bushmaster To identify the incidence rate and evaluate the distribution of accidents caused by Lachesis in Brazil and its relation with suitability regions, we obtained epidemiological data from the DATASUS platform, from the Ministry of Health (www.datasus.com). We used all the available period for the analyses (between 2007-2016); and selected the type of snakebite by “Lachesis muta”. All Brazilian states were considered for the analyses. Analyses We identified the states with the largest area of potential occurrence of Lachesis muta and most suitable municipalities according to the ecological niche modeling. For this, we calculated the proportion

of suitable areas in each state. To identify the most suitable municipalities, we calculated the median values of suitability of each municipality. We selected priority areas for receiving the SABL according to the municipalities and states that showed the highest suitability rates. Both analyses were done at Quan�� tum GIS 2.18.4 (QGIS Development Team, 2016). To identify the current number of accidents caused by Lachesis muta, we calculated the incidence rates of accidents by municipality (number of new cases over a defined period in a population at risk of begin affected). This rate was calculated by dividing the sum of all accidents occurred between 2007 and 2016, by the estimated population in the same period. Finally, we identify if the regions with accident records correspond to the areas with potential occurrence of L. muta. Results Suitability for Lachesis muta and Snakebites We obtained 226 occurrences of Lachesis muta distributed in South and Central America, 56 of which

Figure 1. Potential distribution of Lachesis muta in South America. Yellow dots are the occurrences. There is high suitability for L. muta at the North region, which should be a priority for receive Anti-botropic-laquetic Serum – SABL.

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Cuad. herpetol. 34 (2): 135-143 (2020) were specific geographical coordinate occurrences. The model performance was high (AUC = 0.98). The final map showed two large regions of high climatic suitability, one in the Amazonia with enclaves in the Cerrado and another in the Atlantic Forest, distributed along the Brazilian coast (Fig. 1). After applying the threshold (0.130), the total territorial extent with suitability was 5.2 million km². In Brazil, the area with suitability occupy 60% of the country. The states that covered the greatest extensions of suitability were Amazonas with 30% of total suitability, Pará with 21.9%, and Mato Grosso with 18.43% (Table 1). One thousand three hundred and six municipalities (23% of the total Brazilian municipalities) showed suitability for L. Muta occurrence. The highest suitability values were in the Amazonia, for the municipalities of Mâncio Lima (0.97) in the state of Acre, and Eirunepé (0.97), Ipixuna (0.96), Envira (0.96) and Guajará (0.95) in the Amazonas State. In Brazil, approximately 41.5% (n = 788) of the Table 1. Brazilian states and the percentage of total suitability found for Lachesis muta after the threshold. There are high values for North region.

State

Percentage of Climatic Suitability

Amazonas

30,1

Pará

21,9

Mato Grosso

18,3

Rondônia

4,8

Tocantins

4,5

Roraima

3,9

Goiás

3,8

Bahia

3,2

Acre

3,0

Amapá

2.1

Maranhão

1,6

Espirito Santo

0,6

Piauí

0,5

Minas Gerais

0,4

Pernambuco

0,1

Alagoas

0,1

Sergipe

0,1

Paraíba

0,1

Rio de Janeiro

0,1

Rio Grande do Norte

0,01

Ceará

0,01

Distrito Federal

0,00

municipalities with hospital assistance for snakebites have climatic suitability for Lachesis muta. Among the 3,663 municipalities that do not have medical assistance for snakebites, 15.5% (n = 518) presented climatic suitability for the occurrence of L. muta. The highest values were found in Bujari (0.68) and Porto Acre (0.67), both in the states of Acre; Careiro da Várzea (0.66) in Amazonas State; Cujubim (0.65) in Rondônia State and Capixaba (0.64) also in Acre State. In Brazil, 8,500 accidents were reported as caused by Lachesis muta between 2007 and 2017. The highest incidence rates (in 100,000 inhabitants) were for the states of Acre (10.73), followed by Amazonas (10.09) and Roraima (6.34). The municipalities with the highest incidence rates were Uiramutã (166) in Roraima, Uarini (64.2), Nova Olinda do Norte (60.9) and Alvarães (57.4) in Amazonas state, as well as Rodrigues Alves (57.3) in Acre state (Fig. 2). The municipalities with the lowest incidence rates included Rio de Janeiro (0.005), in the state of Rio de Janeiro, Salvador (0.003) in Bahia State and São Paulo (0.001), in São Paulo State. About 69% (472) of the municipalities that reported accidents with L. muta presented suitability for the species’ occurrence, and 31% (n = 214) did not presented any suitability. We found low correlation with climatic suitability and incidence rate (Spearman Correlation: 0.36, p < 0.001). Discussion The present study is the first to suggest an effective distribution of Lachesis muta antivenom (Antibotropic-laquetic Serum - SABL) based on areas of high suitability for the species in Brazil. First, we discuss the regions that have more incidence rates of accidents and suitability for the occurrence of the species. We point the municipalities that should be prioritized to receive antivenom. We point out regions that have records of Lachesis bites, but do not have suitability for its occurrence. We also show the importance of studies that recognize areas of occurrence of venomous animals for supporting the efficient distribution of the antivenom. The highest values of suitability and incidence rates of snakebites were in northern Brazil showing the importance of distributing SABL to this region as a priority. This region also has shown the highest incidence of other snakebites (Rebouças Santos et al., 2019), and can be treated as a priority for health 139

N. Citeli et al. - Bushmaster bites and antivenom distribution in Brazil

Figure 2. Incidence rates of accidents by Lachesis muta in Brazilian municipalities. The highest incidence rates were at Amazon region.

surveillance and control. Although northern Brazil has low values of land use (high values is related to the most common epidemiological profile in snakebites; e.g., men at productive age working at agriculture), remotes communities are present in such places (Bochner and Struchiner, 2003; IBGE 2010). Fifty per cent of the Brazilian indigenous populations live in the northern region (IBGE, 2010; 2016). These populations already suffer from many other health problems and the available systematized information on the subject is scarce (Montenegro and Stephens, 2006; Leite et al., 2013). Most part of these health problems would be easy to control (e.g., Tuberculosis - Coimbra and Basta, 2007), but they still prevail due to the lack of investment and the difficulty of accessing adequate healthcare services (Stephens et al., 2006; Gracey and King, 2009). Our results also indicate the importance of hospitals with SABL closer to indigenous populations. The states with high suitability, such as Acre, Amazonas and Pará (northern Brazil) should always be prioritized for receiving SABL, especially the municipalities of Mâncio Lima, Eirunepé, Ipixuna, Envira, and 140

Guajará. All these municipalities must receive antivenom and hospital assistance to treat the bitten patients and reduce their chances of dying or having permanent sequelae. Even though the coastal Atlantic Forest presented lower values of climatic suitability, not being a priority when compared to the northern region (maximum of 0.66 and 0.97, respectively), it should not be neglected. Therefore, we recommend regular shipments of SABL to this region. However, we find no need to distribute antivenom for Lachesis snakebites to certain municipalities such as Salvador (Bahia State), Rio de Janeiro (Rio de Janeiro State) and São Paulo (São Paulo State). Lachesis muta is considered locally extinct in Salvador (Lira-da-Silva et al., 2011), its last record for Rio de Janeiro State was more than 30 years ago (IVB 01, in 1986), and do not have current or historical records in São Paulo State. Approximately 70% of the municipalities that have reported snakebites showed high suitability for Lachesis muta. However, the remaining municipalities with reported accidents (30%) do not show any suitability, supporting low correlation. For example,

Cuad. herpetol. 34 (2): 135-143 (2020) accidents reported for Distrito Federal, Paraná, Rio Grande do Sul, Santa Catarina and São Paulo were not congruent with our modeling results and neither with the results of other studies (see Moura et al., 2016), since these localities were not suitable areas for the species occurrence. Therefore, we suggest these accidents may have been caused by captive animals, such as Zoos and vivaria or even misidentified. Inaccurate completion of accident report sheets might also have caused this incongruence between the modeling results and the states with snakebite notifications. Lachesis muta can be mistaken by health professionals with species from a high diversity and abundant genus in Brazil, the genus Bothrops (Silva et al., 2019). Studies that prioritize environmental education about medically important animals, associated with professional training and the dissemination of correct information are indispensable (Gutiérrez et al., 2009; Chippaux, 2017). We recommend all municipalities with reported accidents must invest in environmental education for population and training health agents. Since it is not easy to distinguish between Bothrops and Lachesis envenomation, another strategy for treatment is the administration of polyspecific antivenom (e.g., Madrigal et al., 2017). Thus, the current use of SABL by the Ministry of Health, which is a conjugated antivenom made from the venoms of Bothrops and Lachesis is the most appropriate. In the period from 2007 to 2017 alone, 260,000 snakebites were reported in Brazil, 100,000 of which were considered as moderate and severe. There are regions in Brazil where the access to antivenom is still limited and where patients have to travel long distances to receive antivenom treatment (Gutiérrez et al., 2009). Adequately guiding the distribution of antivenom is crucial, because it would not only improve the treatment of snakebites, but it would also improve the logistics of antivenom production, and even the policies of snakebite prevention. We also encourage mapping the medically important species, because such technique can reveal subsampled areas of occurrence and guide the efficient distribution of antivenom. Ecological modeling can complement and even point out problems on snakebite mapping. It can also be applied to any region of the world, showing results that can help to create policies to minimize public health issues. Acknowledgments This study is dedicated to the memory of Dr. Anibal

Melgarejo. We thank Breno Hamdan, Hussam Zaher and Paulo Passos for providing access to specimens under their care; Breno Almeida, Rejane Lira-daSilva, Rodrigo Souza and Aníbal Melgarejo (in memoriam) who helped us with crucial information about Lachesis biology; Rodrigo C. Gonzalez, Regina Macedo and Reuber Brandão who helped us with manuscript review. Financial support was provided by PROGRAMA CAPES DEMANDA SOCIAL (PROCESS 1602200) (grant to NC). Literature cited

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© 2020 por los autores, licencia otorgada a la Asociación Herpetológica Argentina. Este artículo es de acceso abierto y distribuido bajo los términos y condiciones de una licencia Atribución-No Comercial 2.5 Argentina de Creative Commons. Para ver una copia de esta licencia, visite http://creativecommons.org/licenses/by-nc/2.5/ar/

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Cuad. herpetol. 34 (2): 145-162 (2020)

Trabajo

Serra do Navio, Guiana Shield lowland area, Brazil: a region with high diversity of Squamata Ana Lúcia da Costa Prudente1, João Fabrício de Melo Sarmento1, Karla Kaliana Camara Costa1, Ângelo Cortez Moreira Dourado1, Marina Meireles dos Santos1, Janaina Reis Ferreira Lima2, Jucivaldo Dias Lima2, Ulisses Galatti1 Museu Paraense Emílio Goeldi (MPEG), Laboratório de Herpetologia, Coordenação de Zoologia, Avenida Perimetral, 1901, Caixa Postal 399, Terra Firme, Belém, 66017-970, Pará, Brazil. 2 Instituto de Pesquisas Cientificas e Tecnológicas do Amapá (IEPA), Núcleo de Biodiversidade (NUBIO), Laboratório de Herpetologia. Rodovia Juscelino Kubitschek, s/n, Distrito da Fazendinha, Macapá, Amapá, Brazil. 1

Recibido: 17 S eptiembre 2019 Revisado: 30 Enero 2020 Aceptado: 23 Abril 2020 Editor Asociado:

D. B a l d o

doi: 10.31017/CdH.2020.(2019-039)

ABSTRACT The Guiana Region is the area bordered by the Orinoco and Negro rivers to the west, by the Amazonas River to the south and by the Atlantic Ocean to the north and east. This area is a biogeographic unit known as the Guiana Shield, with a variety of landscapes. Located in the extreme north of Brazil, in the Guiana Shield lowlands, the state of Amapá presents great diversity of habitats. In this study we provide composition and diversity data of the Squamata from Serra do Navio (SN) region, in the northeastern part of the state of Amapá, Brazil, a lowland area of the Guiana Shield. The species list was based on data obtained from herpetological collections and collection expeditions carried out at 10 sites in the municipalities of Pedra Branca do Amapari and Serra do Navio. We consider literature data from 14 sites and SN data to compare the composition of herpetofauna between the lowland and highland areas in the Brazilian Amazon.We recorded 95 species, including 57 snakes, 36 lizards, and two species of amphisbaenians. Atractus aboiporu, A. trefauti, and Erythrolamprus rochai were described from the data collected in this study. The Squamata community of SN consists mainly of diurnal lizards and nocturnal snakes, with terrestrial and cryptozoic habits, present in pristine and altered environments. The most abundant species of lizard and snake were Loxopholis guianense and Atractus latifrons, respectively. The SN region has 17 exclusive Squamata species, with a fauna similar to the Tumucumaque Mountains and northern Pará sites, geographically closer regions with similar altitudes. Key words: Lizards, Snakes, Amphisbaenians, Amazonian, community. RESUMEN La región de Guayana es el área bordeada por los ríos Orinoco y Negro al oeste, por el río Amazonas al sur y por el océano Atlántico al norte y al este. Esta área es una unidad biogeográfica conocida como Escudo Guayanés, con una variedad de paisajes. Ubicado en el extremo norte de Brasil, en las tierras bajas del Escudo Guayanés, el estado de Amapá presenta una gran diversidad de hábitats. En este estudio, proporcionamos datos sobre la composición y diversidad de Squamata de la región de Serra do Navio (SN), en la parte noreste del estado de Amapá, Brasil, un área de tierras bajas del Escudo de Guyana. La lista de especies se basó en datos obtenidos de colecciones herpetológicas y expediciones de recolección realizadas en 10 sitios en los municipios de Pedra Branca do Amapari y Serra do Navio. Consideramos datos de literatura de 14 sitios y datos de SN para comparar la composición de herpetofauna entre las áreas de tierras bajas y tierras altas en la Amazonía brasileña. Registramos 95 especies, incluyendo 57 serpientes, 36 lagartos y dos especies de anfisbaenias. Atractus aboiporu, A. trefauti y Erythrolamprus rochai se describieron a partir de los datos recopilados en este estudio. La comunidad Squamata de SN consiste principalmente en lagartos diurnos y serpientes nocturnas, con hábitos terrestres y criptozoicos, presentes en ambientes prístinos y alterados. Las especies más abundantes de lagarto y serpiente fueron Loxopholis guianense y Atractus latifrons, respectivamente. La región SN tiene 17 especies exclusivas de Squamata, y tiene una fauna similar a las montañas Tumucumaque y los sitios del norte de Pará, regiones geográficamente más cercanas y con altitudes similares. Palabras clave: Lagartos, Serpientes, Anfibaenias, Amazónicos, Comunidad.

Author for correspondence: prudente@museu-goeldi.br

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A. L. C. Prudente et al. - Squamata diversity of Serra do Navio, Brazil Introduction Evidence of high diversity of snake and lizard species in the Amazon region come mostly from studies of communities (e.g. Duellman, 1978; Martins and Oliveira, 1999; Bernarde and Abe, 2006; Maschio et al., 2009) and herpetofaunistic inventories (e.g. Prudente and Santos-Costa, 2005; Prudente et al., 2010; Santos-Costa et al., 2015). It is estimated that there are about 229 species of snakes, 148 of lizards and 25 of amphisbaenians in the brazilian Amazon, representing 56% of the 405 species of snakes, 54% of the 276 species of lizards and 35% of the 72 species of amphisbaenians recorded for Brazil (Costa and Bérnils, 2018). These numbers are growing every year due to regular descriptions of new species (e.g. Ascenso et al., 2019; Melo-Sampaio et al., 2019). On the other hand, some species will never be revealed to science, as the loss or fragmentation of habitats caused by human activities can lead to extinction on a local and global scale (Prudente et al., 2018). The Guiana Region is bounded by the Orinoco and Negro rivers to the west, the Amazonas River to the south and the Atlantic Ocean to the north and east (Hoogmoed, 1979). It includes Guyana, Suriname, French Guiana, southeastern of Venezuela, and northern Brazil (states of Amapá, Roraima, part of the states of Pará and Amazonas situated north of the Amazonas River) (Hoogmoed, 1979; Avila-Pires et al., 2010). This area is considered as a unit known as the Guiana Shield (Gansser, 1954), with a wide variety of landscapes including sandstone tepuis, granite inselbergs, white sands forests, seasonally flooded tropical savannas, lowlands with numerous rivers, isolated mountain ranges, and coastal swamps (Huber et al., 1995; Huber, 1995). The Guiana Shield highlands region, with elevations above 1,500 m is considered a distinct biogeographic region, known as Pantepui, with large number of endemic species (82% of amphibians and 62% of reptiles) (McDiarmid and Donnelly, 2005; Avila-Pires et al., 2007; Moraes et al., 2017); in contrast, the Guiana lowlands have a number of species in common with other areas of Amazonian and lower number of endemic species (52% of amphibians and 26% of reptiles) (Hoogmoed, 1979; Avila-Pires et al., 2010). Located in the extreme north of Brazil, within the Guiana Shield lowlands, the state of Amapá presents a great diversity of habitats, including Terra Firme forests, flooded floodplain and igapó forests, lakes, extensive mangrove areas, plant formations 146

associated with rocky outcrops and a significant portion of Amazonian cerrado in its central area (IBGE, 2014). Avila-Pires (2005) recorded 84 species of snakes, 41 of lizards and two of amphisbaenians for the state of Amapá, whereas Lima (2008) and Campos et al. (2015) recorded a lower diversity (45 species snakes, 33 lizards and two of amphisbaenians, and 22 species of lizards and one of amphisbaenia, respectively). Recently, in the list of reptiles of Brazil, Costa and Bérnils (2018) registered 88 species of snakes, 46 lizards, and three amphisbaenians for the state of Amapá, while Nogueira et al. (2019), in extensive data compilation about Brazilian snakes, indicated a total 90 species of snakes for the state. This study represents a contribution to the understanding of the herpetofauna of the eastern Amazonian lowlands, north of the Amazon River. Here we provide the composition and diversity of Squamata species of the Serra do Navio region, in the municipalities of Pedra Branca do Amapari and Serra do Navio, state of Amapá, Brazil. We compared our results with literature data of 14 sites of the lowlands and hightlands in the Brazilian Amazon, considering the altitudinal differences and distances between the areas. Materials and methods The present study was carried out with data obtained from herpetological collections of the Museu Paraense Emílio Goeldi (MPEG) and Instituto de Pesquisas Científicas e Tecnológicas do Amapá (IEPA), collected in two nearby municipalities, Serra do Navio and Pedra Branca do Amapari, areas with the same altitude range and geomorphological characteristics (Fig. 1). In addition, we included samples collected from seven locations in the Pedra Branca do Amapari, two of these affected by artisanal-scale mining (garimpo), and three in the Serra do Navio (Table 1), both located in the midwest region of Amapá State, Brazil (Fig. 1). Samplings at Pedra Branca do Amapari were conducted during three expeditions in 2000 (April-December), two in the rainy season and one in the dry season, lasting between seven and ten days each (Table 1). In Serra do Navio sampling occurred during one expedition lasting ten days in November 2007. Due to the proximity between the municipalities of Serra do Navio and Pedra Branca do Amapari, we consider here as an area defined as Serra do Navio region. This region can be characterized by

Cuad. herpetol. 34 (2): 145-162 (2020) Table 1. Location and description of the herpetofauna sampling sites in Serra do Navio and Pedra Branca do Amapari, state of Amapá, Brazil. Municipality

Geographic coordinates

Serra do Navio

00°59’28” N, 52°01’33” W

Encompasses flooded, primary and secondary growth forests

Site description

Serra do Navio

01°00’41” N, 52°03’29” W

Flooded and secondary growth forests

Serra do Navio

01°00’43” N, 52°05’45” W

Flooded and primary forests

Pedra Branca do Amapari

00°52’23” N, 51°52’28” W

Primary forest and understorey with uneven terrain, with William stream drainage

Pedra Branca do Amapari

00°51’47” N, 51°52’43” W

Primary forest and rust lagoon, formed by collapse of porous lateritic soil

Pedra Branca do Amapari

00°53’45” N, 51°52’55” W

Steep terrain with presence of some very robust and close trees

Pedra Branca do Amapari

00°51’34” N, 51°52’34” W

Primary forest with a more closed canopy, with drainage of the Arrependido stream, much affected by the activity of garimpo

Pedra Branca do Amapari

00°50’54” N, 51°53’12” W

Secondary growth forests on flat ground

Pedra Branca do Amapari

00°50’58” N, 51°53’17” W

Stretch of forest altered by the garimpo dominated by herbaceous and shrub vegetation

Pedra Branca do Amapari

00°51’29” N, 51°53’27” W

Slightly uneven terrain with primary forest of hill top and thin trees, between the drainages of Taperebá and Mata-Fome streams, where the terrain is stony and the water is turbid

having Equatorial (Am) climate according to the Köppen-Geiger classification, with annual rainfall above 3,300 mm in the north-central Amapá, with monsoon period between February and May, when the monthly rainfall is around 400 mm, and dry period between August to November (Alvares et al., 2013). Annual mean temperature is 27°C, with daily flutuactions between 25 and 35°C and temperatures at night between 20 and 25°C (Hoogmoed and AvilaPires, 1989). It is characterized by tropical florest with areas of Terra Firme containing submontane dense ombrophylous forest formations with emergent docel as well as altered areas (Hoogmoed and Avila-Pires, 1989). All Squamata were captured using two capture methods: Time Constrained Search (Campbell and Christman, 1982; Scott et al., 1989; Martins and Oliveira, 1999) and Pitfall Traps with Drift Fences (Greenberg et al., 1994; Cechin and Martins, 2000). We also obtained specimens captured by third parties and found occasionally throughout the sites described. All specimens collected in this study were deposited at the Herpetological Collection of MPEG and IEPA. We compared the composition of the herpetofauna of the Serra do Navio region with 14 other lowland and highland areas in northern Brazilian Amazon. Considering the distances and altitudes between the analyzed areas we defined: seven sites in northern Pará State (Avila-Pires et al., 2010); five sites in Tumucumaque Mountains National Park, state of Amapá (Lima, 2008); one site in Almeireim,

state of Pará (Ribeiro Junior et al., 2008); one site in Serra da Mocidade, state of Roraima (Moraes et al., 2017) (Fig. 1); and one site in Serra do Navio region (this study). Cluster dendrogram based on dissimilarity matrix by Jaccard index were performed in R package version 2.1.0. (Maechler et al., 2019). To describe the Squamata community we use categories of daily activity and the use of microhabitat (e.g., day or night, arboreal, terrestrial, aquatic, etc.), considering that many Amazonian snakes and lizards use more than one substrate for their activities and are active both day and night (Hoogmoed, 1973; Dixon and Soini, 1975, 1986; Cunha and Nascimento, 1978, 1993; Gasc et al., 1983; Cunha et al., 1985; Magnusson and Lima, 1984; Hoogmoed and Avila-Pires, 1989, 1991; Martins, 1991; AvilaPires, 1995; Martins and Oliveira, 1999; Maciel et al., 2003; Bailey et al., 2005; Maschio, 2008; Vitt et al., 2008; Avila-Pires et al., 2010; Fraga et al., 2013; Santos-Costa et al., 2015; Ascenso et al., 2019; Melo-Sampaio et al., 2019). Here we used general information of the species found under the following conditions: active, resting, foraging, on the substrate, on the vegetation, in the water, near the water, and other. The abundance of species was considering only for the Serra do navio region, which was defined according to Maschio (2008), where dominant species vary between 9 and 15%, intermediate between 0.53 and 4.76%, and rare when present in 0.26% of the total sampled specimens. The taxonomic nomenclature and species identification followed: Avila-Pires (2005), Lima 147

A. L. C. Prudente et al. - Squamata diversity of Serra do Navio, Brazil

Figure 1. Map of the areas where the herpetofaunistic inventories were made in Amazonian Brazil. Legend: White triangles – Serra da Mocidade, Roraima State; black triangles – northern Pará State (Avila-Pires et al., 2010); white pentagon - Almeirim, Pará State (Ribeiro Junior et al., 2008); black squares – Tumucumaque Mountains National Park (Lima, 2008); white diamond - Fazendinha Environmental Protection Area, Amapá State (Campos et al., 2015); white stars – Serra do Navio region, Amapá State (this work).

(2008), Campos et al. (2005); Costa and Bérnils (2018); Avila-Pires et al. (2007); Melo-Sampaio et al. (2019); Vitt et al. (2008); Fraga et al. (2013); Ascenso et al. (2019); and Nogueira et al. (2019). The species conservation status was based on the IUCN (2019) classification, being divided into nine categories: Not Evaluated (NE), Data Deficient (DD), Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN), Critically Endangered (CR), Extinct in the Wild (EW) and Extinct (EX). Results We recorded 95 species for the Serra do Navio region, consisting of 57 snakes, 36 lizards, and two species of amphisbaenians (Table 2). Among the lizards, 94% of the species are exclusively diurnal and only 6% nocturnal. Most of the registered species (67%) occur in both primary and secondary environments, while 24% were exclusively from primary forest (Table 3). Most species were 148

primarily cryptozoic (44%), followed by arboreal (30%) and terrestrial species (28%). Two species of amphisbaenians were exclusively fossorial. The family Gymnophthalmidae had the highest number of species (n= 13; 36.1%), Loxopholis guianense being the most abundant species (n= 111; 21.5%), followed by Norops chrysolepis (8.1%), Chatogekko amazonicus (8.1%), Kentropyx calcarata (7.3%), and Iphisa elegans (6.0%) (Table 3). We registered 43% of the species of snakes as exclusively nocturnal and 38% as diurnal. Most of the registered species (61%) can occur in both primary and secondary forest environments, and 35% are species that occur exclusively in primary forest (Table 4). Species of snakes that are exclusively terrestrial and exclusively cryptozoic corresponded to 21% of the total species registered. Species that are predominantly arboreal and those that are predominantly fossorial correspond to 15 and 12%, respectively. The fossorial species accounted for approximately 5% of the total number of species

Cuad. herpetol. 34 (2): 145-162 (2020) Table 2. List of Squamata of the Serra do Navio region, recorded in this study, and other regions of the state of Amapá, Brazil, according to Avila-Pires (2005), Lima (2008), Campos et al. (2015), and Costa and Bérnils (2018). The "x" followed by a ‘‘? ’’ if a listing is uncertain. Family / specie

Avila-Pires (2005)

Campos et al. (2015)

Costa and Bérnils (2018)

Lima (2008)

This study- This studyfieldwork collection (n) data (n)

Amphisbaenians Amphisbaenidae Amphisbaena alba (Linnaeus, 1758)

Amphisbaena fuliginosa Linnaeus, 1758

Amphisbaena vanzolinii Gans, 1963

Lizards Dactyloidae Dactyloa punctata (Daudin, 1802)

Norops auratus (Daudin, 1802)

Norops chrysolepis (Duméril and Bibron, 1837)

Norops fuscoauratus (D’Orbigny, 1837 in Duméril and Bibron, 1837)

Norops ortonii (Cope, 1868)

Iguanidae Iguana iguana (Linnaeus, 1758)

Gekkonidae Hemidactylus mabouia (Moreau de Jonnes, 1818)

Gymnophthalmidae Alopoglossus angulatus (Linnaeus, 1758)

Amapasaurus tetradactylus Cunha, 1970

Arthrosaura kockii (Lidth de Jeude, 1904)

Arthrosaura reticulata (O’Shaughnessy, 1881)

Bachia flavescens (Bonnaterre, 1789)

Bachia gr. heteropa (Wiegmann, 1856)

x x

Bachia remota Ribeiro-Júnior, da Silva and Lima, 2016

Cercosaura argulus Peters, 1862 Cercosaura ocellata Wagler, 1830

3 x

Cercosaura oshaughnessyi (Boulenger, 1885) Colobosaura modesta (Reinhardt and Lütken, 1862)

Iphisa elegans Gray, 1851

Loxopholis guianense (Ruibal, 1952)

Loxopholis percarinatum (Muller, 1923)

Neusticurus bicarinatus (Linnaeus, 1758)

Neusticurus surinamensis (Boulenger, 1900)

Ptychoglossus brevifrontalis Boulenger, 1912 Tretioscincus agilis (Ruthven, 1916)

x x

Tretioscincus oriximinensis Avila-Pires, 1995

Phyllodactylidae Thecadactylus rapicauda (Houttuyn, 1782)

Polychrotidae

149

A. L. C. Prudente et al. - Squamata diversity of Serra do Navio, Brazil Polychrus marmoratus (Linnaeus, 1758)

Scincidae Copeoglossum nigropunctatum (Spix, 1825)

Varzea bistriata (Spix, 1825)

Sphaerodactylidae Chatogekko amazonicus (Andersson, 1918)

Gonatodes annularis Boulenger, 1887

Gonatodes humeralis (Guichenot, 1855)

Lepidoblepharis heyerorum Vanzolini, 1978

Pseudogonatodes guianensis Parker, 1935

x x

Teiidae Ameiva ameiva (Linnaeus, 1758)

Cnemidophorus cryptus Cole and Dessauer, 1993

Cnemidophorus lemniscatus (Linnaeus, 1758)

Crocodilurus amazonicus (Spix, 1825)

Dracaena guianensis Daudin, 1802

Kentropyx calcarata Spix, 1825

Kentropyx striata (Daudin, 1802)

Tupinambis teguixin (Linnaeus, 1758)

Plica umbra (Linnaeus, 1758)

Tropidurus hispidus Spix, 1825

Tropiduridae Plica plica (Linnaeus, 1758)

Tropidurus oreadicus Rodrigues 1987

x x

Uracentron azureum (Linnaeus, 1758)

Uranoscodon superciliosus (Linnaeus, 1758)

Boa constrictor Linnaeus, 1758

Corallus caninus (Linnaeus, 1758)

Corallus hortulanus (Linnaeus, 1758)

Epicrates cenchria (Linnaeus, 1758)

x x

Snakes Aniliidae Anilius scytale (Linnaeus, 1758) Anomalepididae Typhlophis squamosus (Schlegel, 1839) Boidae

Epicrates maurus Gray, 1849

Eunectes deschauenseei Dunn and Conant, 1936

Eunectes murinus (Linnaeus, 1758)

Colubridae Chironius carinatus (Linnaeus, 1758)

Chironius exoletus (Linnaeus, 1758)

Chironius flavolineatus (Jan, 1863)

x x x

Chironius fuscus (Linnaeus, 1758)

Chironius multiventris Schmidt and Walker

Chironius scurrulus (Wagler, 1824)

150

Cuad. herpetol. 34 (2): 145-162 (2020) Dendrophidion dendrophis (Schlegel, 1837)

Drymarchon corais Boie, 1827

Drymoluber dichrous (Peters, 1863)

Leptophis ahaetulla (Linnaeus, 1758)

Mastigodryas boddaerti (Sentzen, 1796)

Mastigodryas bifossatus (Raddi, 1820)

Oxybelis aeneus (Wagler, 1824)

Oxybelis fulgidus (Daudin, 1803)

Phrynonax poecilonotus (Günther, 1858)

Phrynonax polylepis (Peters, 1867)

x 1

Rhinobothryum lentiginosum (Scopoli, 1785)

Spilotes pullatus (Linnaeus, 1758)

Spilotes sulphureus (Wagler, 1824)

Tantilla melanocephala (Linnaeus, 1758)

Dipsadidae Apostolepis quinquelineata Boulenger, 1896

Atractus aboiporu Melo-Sampaio, Passos, Fouquet, Prudente and Torres-Carvajal, 2019 Atractus latifrons (Günther, 1868)

4 3

Atractus torquatus (Duméril, Bibron and Duméril, 1854)

Atractus trefauti Melo-Sampaio, Passos, Fouquet, Prudente and Torres-Carvajal, 2019 Atractus zidoki Gasc and Rodrigues, 1979

Cercophis auratus (Schlegel, 1837)

Clelia clelia (Daudin, 1803)

Dipsas catesbyi (Sentzen, 1796)

Dipsas indica Laurenti, 1768

Dipsas pavonina Schlegel, 1837

Dipsas variegata (Duméril, Bibron and Duméril, 1854)

Drepanoides anomalus (Jan, 1863)

Erythrolamprus aesculapii (Linnaeus, 1766)

Erythrolamprus breviceps (Cope, 1860)

Erythrolamprus cobella (Linnaeus, 1766)

Erythrolamprus miliaris (Linnaeus, 1758)

Erythrolamprus poecilogyrus (Wied, 1824)

Erythrolamprus reginae (Linnaeus, 1758)

1 1

1 x

2 1 2

x x

Erythrolamprus rochai Ascenso, Costa and Prudente, 2019

1 2 2

Erythrolamprus taeniogaster (Jan, 1863)

Erythrolamprus typhlus (Linnaeus, 1758)

Helicops angulatus (Linnaeus, 1758)

Helicops hagmanni Roux, 1910 Helicops leopardinus (Schlegel, 1837)

x x

Helicops polylepis Günther, 1861

Helicops trivittatus (Gray, 1849)

151

A. L. C. Prudente et al. - Squamata diversity of Serra do Navio, Brazil Hydrodynastes bicinctus (Herrmann, 1804)

Hydrodynastes gigas (Duméril, Bibron and Duméril, 1854)

Hydrops triangulares (Wagler, 1824)

Imantodes cenchoa (Linnaeus, 1758)

Leptodeira annulata (Linnaeus, 1758)

Ligophis lineatus (Linnaeus, 1758)

Oxyrhopus formosus (Wied, 1820)

Imantodes lentiferus (Cope, 1894)

x x

1 1

Oxyrhopus melanogenys (Tschudi, 1845)

x x

Oxyrhopus occipitalis (Wied-Neuwied, 1824)

Oxyrhopus petolarius (Linnaeus, 1758)

Oxyrhopus trigeminus (Duméril and Bibron, 1854)

Philodryas argentea (Daudin, 1803)

Philodryas viridissima (Linnaeus, 1758)

Philodryas olfersii (Lichtenstein, 1823)

Pseudoboa coronata Schneider, 1801

Pseudoboa neuwiedii (Duméril, Bibron and Duméril, 1854)

Pseudoeryx plicatilis (Linnaeus, 1758)

Sibon nebulatus (Linnaeus, 1758)

x 1 1

Siphlophis cervinus (Laurenti, 1768)

Siphlophis compressus (Daudin, 1803)

Taeniophallus brevirostris (Peters, 1863)

Taeniophallus nicagus (Cope, 1895)

Thamnodynastes lanei Bailey, Thomas and Silva Jr., 2005

Thamnodynastes pallidus (Linnaeus, 1758)

Xenodon rabdocephalus (Wied, 1824)

Xenodon severus (Linnaeus, 1758)

Xenodon werneri (Eiselt, 1963) Xenopholis scalaris (Wucherer, 1861)

x x

Xenopholis undulatus (Jensen, 1900)

Elapidae Leptomicrurus collaris (Schlegel, 1837)

Micrurus diutius (Burger, 1955)

Micrurus filiformis (Günther, 1859)

Micrurus hemprichii (Jan, 1858)

Micrurus lemniscatus (Linnaeus, 1758)

Micrurus psyches (Daudin, 1803)

Micrurus surinamensis (Cuvier, 1817)

Leptotyphlopidae Epictia albifrons (Wagler, 1824)

Epictia tenella Klauber, 1939 Siagonodon cupinensis (Bailey and Carvalho, 1946)

152

1 x

Cuad. herpetol. 34 (2): 145-162 (2020) Siagonodon septemstriatus (Schneider, 1801)

Trilepida dimidiata (Jan, 1861) Trilepida macrolepis (Peters, 1857)

Typhlopidae Amerotyphlops brongersmianus (Vanzolini, 1976)

Amerotyphlops reticulatus (Linnaeus, 1758)

Viperidae Bothrops atrox (Linnaeus, 1758)

Bothrops bilineatus (Wied, 1821)

Bothrops brazili Hoge, 1954

Bothrops taeniatus Wagler, 1824

Crotalus durissus Linnaeus, 1758

Lachesis muta (Linnaeus 1766)

1 x x

Atractus zidoki (3.85%) (Table 4). Using the method of Pitfall Traps with Drift Fences, ten lizards (Alopoglossus angulatus, Arthrosaura kockii, Bachia flavescens, Iphisa elegans, Kentropyx calcarata, Lepidoblepharis heyerorum, Plica

recorded. Dipsadidae was the family with the highest number of species (35 species; 61.4% of total). Atractus latifrons was the most abundant species (n= 7; 5.38%), followed by Typhlophis squamosus and Micrurus lemniscatus (each with 4.61%), and

Table 3. Data on activity, habitat and microhabitat of lizards recorded in the Serra do Navio region (in alphabetical order). Legend: D= Diurnal, N= Nocturnal, FP= Primary Forest, FS= Secondary Forest, Tr= Terrestrial, Cz= Cryptozoic, Aq= Aquatic, Fss= Fossorial, Arb= Arborial. Conservation Status (IUCN, 2019): LC= Least Concern; References: 1= Hoogmoed (1973), 2= Gasc et al. (1983), 3= Cunha et al.(1985), 4= Dixon and Soini (1986), 5= Hoogmoed and Avila-Pires (1989), 6= Martins (1991), 7= Avila-Pires (1995), 8= Vitt et al. (2008), 9= Magnusson and Lima (1984), 10= Dixon and Soini (1975), 11= Hoogmoed and Avila-Pires (1991), 12= AvilaPires et al. (2010). Activity

Habitat

Amphisbaena alba

Amphisbaena fuliginosa

Species

Alopoglossus angulatus

Ameiva ameiva

Arthrosaura kockii

Arthrosaura reticulata

Bachia flavescens

Cercosaura argulus

Cercosaura ocellata

Chatogekko amazonicus

Cnemidophorus cryptus

Cnemidophorus lemniscatus

Copeoglossum nigropunctatum

Dactyloa punctata

Gonatodes annularis

Gonatodes humeralis

Hemidactylus mabouia

Iphisa elegans

Kentropyx calcarata

1, 4

4 5, 6, 7, 11

7, 11

1, 4, 5, 6, 7

1, 6, 7

4, 5, 7

x x

Arb

3,7,14

7, 10, 11 7

3, 7

7, 11

References

Fss

3, 4, 5, 7, 11

Iguana iguana

Conservation Status (IUCN, 2019)

Microhabitat

x x

5, 7, 8, 11

7, 8

7, 10, 11

1, 5, 6, 7, 9, 11

7 x x

1, 5, 7, 11

153

A. L. C. Prudente et al. - Squamata diversity of Serra do Navio, Brazil Lepidoblepharis heyerorum

Loxopholisguianense

5, 7, 11

1, 2, 5, 7

Loxopholispercarinatum

Neusticurus bicarinatus

Neusticurussurinamensis

Norops chrysolepis

1, 4, 6, 7

Norops fuscoauratus

4, 7

Norops ortonii

4, 7

Plica plica

Plica umbra

4, 7

Polychrus marmoratus

1, 4, 7

Pseudogonatodes guianensis

Ptychoglossus brevifrontalis

4, 7

7, 11

7, 12

4, 7

Thecadactylus rapicauda

x x

1, 7

1, 3, 6, 7

7, 11, 12

x x

Tretioscincus agilis

Tupinambis teguixin

Uracentron azureum

Varzea bistriata

x x x x x

4, 7

7, 11

Table 4. Data on activity, habitat and microhabitat of snakes recorded in the Serra do Navio region (in alphabetical order). Legend: D= Diurnal, N= Nocturnal, FP= Primary Forest, FS= Secondary Forest, Tr= Terrestrial, Cz= Cryptozoic, Aq= Aquatic, Fss= Fossorial, Arb= Arborial. Conservation Status (IUCN, 2019): LC= Least Concern; References: 1= Cunha and Nascimento (1978), 2= Cunha et al.(1985), 3= Dixon and Soini (1986), 4= Hoogmoed and Avila-Pires (1991), 5= Cunha and Nascimento (1993), 6= Martins and Oliveira (1999), 7= Maschio (2008), 8= Avila-Pires et al. (2010), 9= Santos-Costa et al. (2015), 10= Maciel et al. (2003), 11= Bailey et al. (2005), 12= Fraga et al.(2013), 13= Ascenso et al. (2019); 14= Melo-Sampaio et al. (2019). Activity

Habitat

Amerotyphlops reticulatus

Apostolepis quinquilineata

Species

Anilius scytale

Atractus latifrons

Atractus zidoki

Atractus trefauti

Boa constrictor

Bothrops atrox

Bothrops bilineatus

Bothrops brazili

Bothrops taeniatus

Chironius multiventris

Arb

References

1, 3, 19 2, 8

3, 7, 12

5, 22

x x

3 x

1, 6

1, 4, 6, 14 x

1, 2

1, 2, 3 x

Corallus caninus

Corallus hortulanus

x x

Dipsas catesbyi

Dipsas indica

1, 2, 3,9 14

154

Fss

Clelia clelia

Dendrophidion dendrophis

Conservation Status (IUCN, 2019)

Atractus aboiporu

Chironius fuscus

Microhabitat

3, 5, 6, 7

5, 6, 7

1, 5, 6, 7

1, 3, 6, 7

1, 6, 7

1, 3, 6

1, 8, 12

1, 3, 6

Cuad. herpetol. 34 (2): 145-162 (2020) Drepanoides anomalus

Drymarchon corais

Drymoluber dichrous

Epictia albifrons

Erythrolamprus aesculapii

Erythrolamprus breviceps

Erythrolamprus miliaris

Erythrolamprus poecilogyrus

Erythrolamprus reginae

3, 6, 7

1, 2, 5, 7

1,3, 6, 7

1, 2, 3, 6

3, 6,12

3 10

Erythrolamprus rochai Erythrolamprus typhlus

13 x

Helicops angulatus Hydrodynastes gigas

3, 6, 7, 12

x x

1, 5, 12

1, 2, 3, 5, 6

Imantodes cenchoa

1, 5, 12

Leptodeira annulata

2,6, 7, 19

1, 6

1, 2, 5, 6, 7

6, 7

1, 5, 6

2, 3, 6

3, 6

Leptophis ahaetulla

Mastigodryas boddaerti

Micrurus lemniscatus Micrurus surinamensis

Oxybelis aeneus

Oxyrhopus melanogenys Oxyrhopus petolarius

x x

x x x

Philodryas argentea

Philodryas viridissima

Pseudoboa coronata

Pseudoboa neuwiedi

Rhinobothryum lentiginosum

Siagonodon septemstriatus Siphlophis compressus

Spilotes sulphureus

Taeniophallus brevirostris

Taeniophallus nicagus

Thamnodynastes lanei Typhlophis squamosus Xenodon rabdocephalus

Xenodon severus

Xenopholis scalaris

1, 3, 6,

1, 3, 6

8, 12

x x

1, 3, 4, 6

x x

1, 2, 3, 5

Spilotes pullatus

LC x

1, 2, 5, 6 LC

1, 5

8, 12

1, 5, 12

5, 6, 7,

1, 3, 6

LC x

6 11

1, 6

1, 3, 5, 6

1, 3

1, 2, 3, 6

plica, Pseudogonatodes guianensis, Thecadactylus rapicauda, and Tretioscincus agilis) and seven snakes were collected (Amerotyphlops reticulatus, Atractus trefauti, Atractus zidoki, Dendrophidion dendrophis, Erythrolamprus aesculapii, E. reginae, and Typhlops squamosus). We recorded four species of lizards (Gonatodes annularis, Neusticurus bicarinatus, Norops chrysolepis, and Norops ortonii) and eight of

snakes (Corallus hortulanus, Dipsas indica, Oxybelis aeneus, Philodryas viridissima, Philodryas argentea, Pseudoboa coronata, Rhinobothryum lentiginosum, and Xenopholis scalaris) using the method of Time Constrained Search. We recorded seven species of lizards (Ameiva ameiva, Arthrosaura reticulata, Chatogekko amazonicus, Gonatodes humeralis, Leposoma guianense, Norops fuscoauratus, and Plica umbra), 155

A. L. C. Prudente et al. - Squamata diversity of Serra do Navio, Brazil and one of snake using both methods (Drepanoides anomalus). Among the 15 sites we compared, Serra do Navio is the region with the largest number of snakes and lizard species (n= 95) and the largest number of exclusive species (17 species, four lizards - Amphisbaena alba, Cnemidophorus lemniscatus, Hemidactylus mabouia, Varzea bistriata; and 13 snakes - Atractus trefauti, Atractus latifrons, Atractus aboiporu, Atractus zidoki, Drepanoides anomalus, Erythrolamprus breviceps, Erythrolamprus miliaris, Erythrolamprus poecilogyrus, Erythrolamprus rochai, Oxybelis aeneus, Siagonodon septemstriatus, Thamnodynastes lanei, and Xenodon severus) (Fig. 2). Serra do Navio shares 16 species with Serra da Mocidade and 41 species with Almerim (Fig. 2). Ameiva ameiva was the only species that occurs

in all localities and five other species occured at all sites (Bachia flavescens, Chatogekko amazonicus, Kentropyx calacarata, Loxopholis guianense, Siagonodon septemstriatus, and Plica umbra) except Serra da Mocidade. Comparining with the other sites analyzed, Serra da Mocidade has seven exclusive species (Atractus riveroi, Chironius septentrionalis, Dipsas pavonina, Drymobius rhombifer, Micrurus remotus, Norops planiceps, and Tretioscincus oriximinensis) among 24 species known for the region (Moraes et al., 2017). In fact, the dissimilarity analysis using Jaccard index showed Serra da Mocidade as the most exclusive site, while Serra do Navio is close to Almerim (Fig. 3). Most sites in northern Pará constitute a clade with four sites in Tumucumaque, while the northernmost area of Tumucumaque, Trombetas, and Grão Pará another clade (Fig. 3).

Figure 2. Cluster dendrogram based on dissimilarity matrix by Jaccard index. Localities are as follow: MOCIDADE - Serra da Mocidade, Roraima State; GRAOPAC – Central Grão-Pará Ecological Station; GRAOPAS – South Grão-Pará Ecological Station; GRAOPAN - North Grão-Pará Ecological Station; ALMEI – Almeirim; SNAVIO – Serra do Navio; TUMUCU_I – TUMUCU_V – Tumucumaque Mountain National Park sites; MAICURU – Maicuru Biological Reserve; PARU – Paru State Forest; FARO – Faro State Forest; TROMB – Trombetas State Forest.

156

Cuad. herpetol. 34 (2): 145-162 (2020)

Figure 3. Number of species (number above bars) and species sharing and exclusivity by site analyzed (balls indicate the presence of species at the site). Localities are as follow: MOCIDADE - Serra da Mocidade, Roraima State; GRAOPAC – Central Grão-Pará Ecological Station; GRAOPAS – South Grão-Pará Ecological Station; GRAOPAN - North Grão-Pará Ecological Station; ALMEI – Almeirim; SNAVIO – Serra do Navio; TUMUCU_I – TUMUCU_V – Tumucumaque Mountain National Park sites; MAICURU – Maicuru Biological Reserve; PARU – Paru State Forest; FARO – Faro State Forest; TROMB – Trombetas State Forest.

Discussion The total of 95 species record for the Serra do Navio region represents a significant part of Squamata diversity known for the state of Amapá, which total 160 species by considering the data from Avila-Pires (2005), Lima (2008), Campos et al. (2015) and Costa and Bérnils (2018). Among 17 exclusive species of Serra do Navio, three species (Atractus aboiporu, A. trefauti, and Erythrolamprus rochai) were recently described from the collections performed in this study, clearly indicating the importance of further herpetological inventories and studies of communities in the Amazon (Ascenso et al., 2019; MeloSampaio et al., 2019). Some species of lizards and snakes commonly known in Amapá were not recorded in this study, such as Amphisbaena vanzolini, Amapasaurus tetradactylus, Chironius flovolineatus, Colobosaura modesta, Epicrates cenchria, Eunectes murinus, Lachesis muta, Mastigodryas bifossatus, Norops auratus, and Uranoscodon superciliosus (Lima, 2008; Campos et al., 2015). Probably, this result owes to the insufficient sampling effort and the collection methods

used. Another aspect that may have influenced this result is related to habit and species abundance. Efficiency in the registration of fossil and aquatic species requires a specific collection methodology, as well as the registration of rare and difficult to detect species. For lizards, the most efficient sampling method was the Pitfall Traps with Drift Fences, responsible for registering mainly cryptic species, such Alopoglossus angulatus, Arthrosaura kockii, Bachia flavescens and Iphisa elegans, which were hardly registered by other techniques, illustrating the importance of passive sampling in the study of leaf litter or fossorial/ semifossorial species (Ribeiro Junior et al., 2008). For snakes the Time Constrained Search was the methodology registered more species, eight in total, against seven registered by Pitfall Traps with Drift Fences, however, with regard to richness estimates, this method is considered limited because there is a tendency for the observer to find more conspicuous and / or larger species (Hartmann et al., 2009). According to the parameters of abundance of Maschio (2008), the species present in this work reached an intermediate level of abundance, less than 5%, except Leposoma guianense, which was dominant (22%). 157

A. L. C. Prudente et al. - Squamata diversity of Serra do Navio, Brazil The Serra do Navio community consists mainly of diurnal lizards and nocturnal snakes, with terrestrial and cryptozoic habits, present in pristine and altered environments. This pattern is observed in several studies developed in the Amazon (Silva et al., 2011; Santos-Costa et al., 2015). Despite the primarily diurnal habit of lizards, some species, such as Alopoglossus angulatus, Arthrosaura reticulata, Bachia flavecens, Gonatodes annularis, and Lepidoblepharis heyerorum may exhibit nocturnal behavior (Avila-Pires, 1995). Hoogmoed and Avila-Pires (1989) observed that the large number of small diurnally active lizards at night in the Serra do Navio region was related to daytime unfavorable daytime microclimate conditions. On the other hand, according to the authors, moonlight was insufficient to activate daytime lizards. The same patterns was observed for snakes, where some nocturnal species can be active during day, such as Bothrops atrox. In forest environments it is common to note that some species of snakes may use different substrates, such as Philodryas viridissima, which is mainly arboreal but may eventually forage on the forest floor (Dixon and Soini, 1986; Martins and Oliveira, 1999). This behavior allows it to capture more prey in different microhabitats, as well as provinding opportunities for rest, such as when individuals sleep on the foliage or in an area at least 30 cm above the ground to avoid attacks by terrestrial predators such as snakes, ants and spiders (Martins, 1993; SantosCosta et al., 2015). The foraging substrate may also vary among the lizards, for example Neusticurus bicarinatus, a semi-aquatic species, and Tretioscincus agilis, an arboreal species, may forage on the forest floor (Cunha et al., 1985; Avila-Pires, 1995). Dissimilarity analysis shwoed a general pattern of clustering by spatial proximity, and a most singular fauna at Serra da Mocidade, which must be attributed to the altidudinal distinctiveness (mean 996m), reaching at least twice the altitude of the other sites (0-500m). Fortunately, sampling methods and effort were similar at the sites we compared, with all the studies using pitfall traps and active search, and lasting 7–14 days. We also checked for taxonomic consistence among the studies. While Moraes et al. (2017) found a mixed compositional influence at Serra da Mocidade including assemblages typical of other mountain ranges and lowland forest habitats in the region, at the other sites reported here most of the taxa were widely distributed in Amazonia or, 158

at least, north of Amazonas River. Compared to the herpetofauna from other 14 north Brazilian Amazon sites, Serra do Navio had a most similar species composition to the Tumucumaque Mountains and northern Pará sites, geographically closer regions. Regarding the conservation status of the 95 species registered for the Serra do Navio region, 75 are listed as "Least Concern" according to IUCN (2019), and for the remaining of the species there are no results (Tables 3 and 4). For the lizard Copeoglossum nigropunctatum there is a tendency for the population decrease, according to IUCN (2019), due to the populations being severely fragmented. Amapasaurus tetradactylus, described based on two specimens from the upper Maracá basin, Amapá, Brazil, remained known for more than 30 years based only on these two specimens (Avila-Pires et al., 2013). Although classified with "Least Concern" status in IUCN (2019) A. tetradactylus is considered rare and currently only 37 specimens collected in eight localities are known, five of them in the state of Amapá (Avila-Pires et al., 2013). The fact that only four collections expeditions resulted in the description of three new species of snakes indicates an urgent need for further herpetological inventories in this region, highlighting the importance of community studies in the Amazon in general. Mainly when considering the increase in deforestation in the region, promoted by mining activity. On the occasion of the collections expeditions in Pedra Branca do Amapari, two of the seven sampled areas were affected by artisanal-scale mining (garimpo), a process that causes extensive environmental degradation, soil pollution and watercourses polluted by mercury, which can lead to the accumulation of this metal in food chains (Jernelov and Lann, 1971; Veiga and Hinton, 2002; Asner et al., 2013; Teixeira et al., 2018). Furthermore, a recent study indicates that small-scale mining represents 64% of the total mining area in the Brazilian Amazon, a fact of concern due to socio-environmental impacts for Amazonian ecosystems and for local communities, since it does not follow environmental protocols for the recover degraded areas (Lobo et al., 2018). Currently, all seven areas inventoried at that time are located in an industrial-mineral complex, in operation since 2007, with an expected useful life of 20 years. If artisanalscale mining activity already causes significant impacts, those caused by industrial-scale activity are

Cuad. herpetol. 34 (2): 145-162 (2020) even more extensive, although not only restricted to the mine area, they may include impacts related to the establishment of mining infrastructure, opening of new roads and urban expansion to support a growing workforce (Sonter et al., 2017). The state of Amapá presents great importance in a conservationist scenario, as it is inserted in the largest area of endemism in the Amazon, Guianan area of endemism. The association of primary and secondary data contributed to obtain a more representative list of Squamata species that occur in the state. However, studies covering other regions can assist in the recognition of species not yet reported for Amapá, as well as new taxa. Acknowledgments We are grateful to the Museu Paraense Emílio Goeldi (MPEG) for logistical support, and to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (ALCP - productivity grant number 30.2611/2018-5 and PROTAX 44.0413/2015-0) and the Fundação Amazônia de Amparo a Estudos e Pesquisas (FAPESPA) for financial support (processes 2016/111449). We thank Glenn Shepard (native speaker) for English revisions. We thank the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) for concession of fauna collection license. Literature cited

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Cuad. herpetol. 34 (2): 145-162 (2020) Travassos. A.E.M. & Galatti, U. 2011. Squamate Reptiles from municipality of Barcarena and surroundings, state of Pará, north of Brazil. Check List (Online) 7: 220-226. Sonter, L. J.; Herrera, D.; Barret, D.J.; Galford, G.L.; Moran, C.J. & Soares-Filho, B.S. 2017. Mining drives extensive deforestation in the Brazilian Amazon. Nature Communications 1013 Teixeira, R.A.; Fernandes, A.R.; Ferreira, J.R.; Vasconcelos, S.S. & Braz, A.M.S. 2018. Contamination and Soil Biological Properties in the Serra Pelada Mine-Amazonia, Brazil. Revista Brasileira de Ciência do Solo [online] 42, e0160354. Veiga, M.M. & Hinton, J.J. 2002. Abandoned Artisanal Gold Mines in the Brazilian Amazon: A Legacy of Mercury Pollution. Natural Resources Forum 26: 15-26. Vitt, L.J.; Magnusson, W.E.; Avila-Pires, T.C.S. & Lima, A.P. 2008. Guia de Lagartos da Reserva Adolpho Ducke, Amazônia Central: 176. Manaus: Attema. Appendix Material analyzed Lizards and amphisbaenians- Alopoglossus angulatus- Pedra Branca do Amapari: MPEG 19585, MPEG 19595, MPEG 19597– 8, MPEG 19608, MPEG 19611, MPEG 19613; Serra do Navio: MPEG 15033, MPEG 15095, MPEG 15150–5, MPEG 15182–5. Ameiva ameiva- Pedra Branca do Amapari: MPEG 19174, MPEG 19607, MPEG 19610, MPEG 19614, MPEG 19697–18; Serra do Navio: MPEG 2472, MPEG 15110. Amphisbaena alba - Pedra Branca do Amapari: MPEG 19217; Sera do Navio: MPEG 1189. Amphisbaena fuliginosa - Pedra Branca do Amapari: MPEG 19591. Arthrosaura kockii- Pedra Branca do Amapari: MPEG 19056, MPEG 19060, MPEG 19182, MPEG 19185, MPEG 19201–2, MPEG 19664–71; Serra do Navio: MPEG 12170–1. Arthrosaura reticulata- Pedra Branca do Amapari: MPEG 19181, MPEG 19210, MPEG 19586, MPEG 19594, MPEG 19596; Serra do Navio: MPEG 15059. Bachia flavescens- Pedra Branca do Amapari: MPEG 19672–5; Serra do Navio: MPEG 1878. Cercosaura argulus- Serra do Navio: MPEG 15149, MPEG 15186–7. Cercosaura ocellata- Serra do Navio: MPEG 15115. Chatogekko amazonicus- Pedra Branca do Amapari: MPEG 19057, MPEG 19059, MPEG 19196, MPEG 19198, MPEG 19602, MPEG 19639–53, MPEG 21820; Serra do Navio: MPEG 12168, MPEG 15018–9, MPEG 15028–9, MPEG 15063–6, MPEG 15093, MPEG 15101–2, MPEG 15131–2, MPEG 15137, MPEG 15191–5, MPEG 15204. Cnemidophorus cryptus- Serra do Navio: IEPA 1908. Cnemidophorus lemniscatus- Serra do Navio: MPEG 15017, MPEG 15037, MPEG 15075–8, MPEG 15090–1, MPEG 15096, MPEG 15112, MPEG 15116, MPEG 15190, MPEG 15205. Copeoglossum nigropunctatum- Pedra Branca do Amapari: MPEG 19186, MPEG 19609, MPEG 19636–7, MPEG 19814–20. Dactyloa punctata- Serra do Navio: IEPA1907. Gonatodes annularis- Pedra Branca do Amapari: MPEG 19213, MPEG 19592, MPEG 19627–31; Serra do Navio: MPEG 15080, MPEG 15087, MPEG 15100, MPEG 15148. Gonatodes humeralisPedra Branca do Amapari: MPEG 19061, MPEG 19063; Serra do Navio: MPEG 15030, MPEG 15126, MPEG 15177, MPEG 16175–7. Hemidactylusmabouia- Serra do Navio: MPEG 15022–7. Iphisa elegans- Pedra Branca do Amapari: MPEG 19200, MPEG 19207, MPEG 19600, MPEG 19772–97; Serra do Navio: MPEG 15081, MPEG 15188. Kentropyx calcarata- Pedra Branca do Amapari: MPEG 19184, MPEG 19195, MPEG 19197, MPEG 19199, MPEG 19589, MPEG 19599, MPEG 19757, MPEG 19798–13; Serra do Navio: MPEG 15015–6, MPEG 15039, MPEG 15073, MPEG 15082, MPEG 15097, MPEG

15111, MPEG 15123–4, MPEG 15129, MPEG 15138, MPEG 15173–4, MPEG 15180–1. Lepidoblepharis heyerorum- Pedra Branca do Amapari: MPEG 19623–6, MPEG 19638; Serra do Navio: MPEG 15040, MPEG 15051, MPEG 15061–2, MPEG 15079, MPEG 15134–6, MPEG 15146, MPEG 15178. Loxopholis guianense- Pedra Branca do Amapari: MPEG 19203–4, MPEG 19208, MPEG 19211, MPEG 19581, MPEG 19603, MPEG 19605, MPEG 19616–7, MPEG 19719–56; Serra do Navio: MPEG 1919, MPEG 1992, MPEG 12169, MPEG 12172, MPEG 15034–5, MPEG 15042–7, MPEG 15054–8, MPEG 15067–71, MPEG 15083–6, MPEG 15088–9, MPEG 15094, MPEG 15103–7, MPEG 15121–2, MPEG 15130, MPEG 15139, MPEG 15141–3, MPEG 15156–72, MPEG 15196–8, MPEG 15201–3. Loxopholis percarinatum- Serra do Navio: MPEG 15140. Neusticurus bicarinatus- Pedra Branca do Amapari: MPEG 19175, MPEG 19179–80; Serra do Navio: MPEG 15031, MPEG 15038, MPEG 15048, MPEG 15176. Neusticurus surinamensis- Pedra Branca do Amapari: MPEG 19058, MPEG 19618; Serra do Navio: IEPA1906, MPEG 15032, MPEG 15049, MPEG 15072, MPEG 15074, MPEG 15098, MPEG 15109. Norops chrysolepis- Pedra Branca do Amapari: MPEG 19178, MPEG 19183, MPEG 19205, MPEG 19212, MPEG 19215–6, MPEG 19593, MPEG 19601, MPEG 19612, MPEG 19662, MPEG 19676–96; Serra do Navio: MPEG 1700–1, MPEG 15041, MPEG 15052–3, MPEG 15119– 20, MPEG 15133, MPEG 15199–200, MPEG 19173. Norops fuscoauratus- Pedra Branca do Amapari: MPEG 19062, MPEG 19587, MPEG 19654–6, MPEG 19659, MPEG 19661; Serra do Navio: MPEG 15036. Norops ortonii- Pedra Branca do Amapari: MPEG 19657–8, MPEG 19660, MPEG 19663. Plica plica-Pedra Branca do Amapari: MPEG 1828, MPEG 19189–91, MPEG 19209, MPEG 19590, MPEG 19619–22; Serra do Navio: MPEG 2471, MPEG 15014, MPEG 15020–1, MPEG 15092, MPEG 15118, MPEG 15125, MPEG 15144–5, MPEG 15175, MPEG 15189. Plica umbra- Serra do Navio: MPEG 2470, MPEG 15050, MPEG 19176–7, MPEG 19192–4, MPEG 19206. Polychrus marmoratus- Pedra Branca do Amapari: MPEG 19583–4. Pseudogonatodes guianensis- Pedra Branca do Amapari: MPEG 19606, MPEG 19632–4; Serra do Navio: MPEG 15060, MPEG 15147, MPEG 15179. Ptychoglossus brevifrontalis- Pedra Branca do Amapari: MPEG 19615.Thecadactylus rapicauda- Pedra Branca do Amapari: MPEG 19635; Serra do Navio: MPEG 1851, MPEG 15099. Tretioscincus agilis- Pedra Branca do Amapari: MPEG 19187–8, 19214, MPEG 19604, MPEG 19758–71; Serra do Navio: MPEG 12173. Tupinambis teguixin- Pedra Branca do Amapari: MPEG 19582, MPEG 31197; Serra do Navio: MPEG 2473. Uracentron azureum- Serra do Navio: MPEG 1784, MPEG 6467. Varzea bistriata- Serra do Navio: MPEG 15128. Snakes- Amerotyphlops reticulatus- Pedra Branca do Amapari: MPEG 19782, MPEG 22849. Anilius scytale- Pedra Branca do Amapari: MPEG 19686; Serra do Navio: MPEG 26349–50. Apostolepis quinquilineata- Pedra Branca do Amapari: MPEG 22842–3, MPEG 19822, MPEG 19824. Atractus aboiporuPedra Branca do Amapari: MPEG 19783, MPEG 25796–7. Atractus latifrons- Pedra Branca do Amapari: MPEG 19781, MPEG 25790–5. Atractus trefauti- Pedra Branca do Amapari: MPEG 25788, MPEG 26584; Serra do Navio: MPEG 16382. Atractus zidoki- Pedra Branca do Amapari: MPEG 23225–8; Serra do Navio: MPEG 16437. Boa constrictor- Serra do Navio: MPEG 18349. Bothrops atrox- Pedra Branca do Amapari: MPEG 19793, MPEG 26581; Serra do Navio: MPEG 26564–5.

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A. L. C. Prudente et al. - Squamata diversity of Serra do Navio, Brazil Bothrops bilineatus- Pedra Branca do Amapari: MPEG 22850. Bothrops brazili- Pedra Branca do Amapari: MPEG 19688–90, MPEG 19697, MPEG 19790. Bothrops taeniatus- Pedra Branca do Amapari: MPEG 19680. Chironius fuscus- Pedra Branca do Amapari: MPEG 25757; Serra do Navio: MPEG 180, MPEG 26593–4. Chironius multiventris- Serra do Navio: MPEG 330, MPEG 18351. Clelia clelia- Pedra Branca do Amapari: MPEG 25758. Corallus caninus- Pedra Branca do Amapari: MPEG 19683. Corallus hortulanus- Pedra Branca do Amapari: MPEG 19678, MPEG 19935, MPEG 26595; Serra do Navio: MPEG 26566, MPEG 26596. Dendrophidion dendrophis- Pedra Branca do Amapari: MPEG 26012. Dipsas catesbyi- Serra do Navio: MPEG 26578. Dipsas indica- Pedra Branca do Amapari: MPEG 22848. Drepanoides anomalus- Pedra Branca do Amapari: MPEG 22851; Serra do Navio: MPEG 26585. Drymarchon corais- Pedra Branca do Amapari: MPEG 19791, MPEG 25759; Serra do Navio: MPEG 18350. Drymoluber dichrous - Pedra Branca do Amapari: MPEG 19792; Serra do Navio: MPEG 18348. Epictia albifrons- Pedra Branca do Amapari: MPEG 22846. Erythrolamprus aesculapii- Pedra Branca do Amapari: MPEG 19700, MPEG 22841. Erythrolamprus breviceps- Pedra Branca do Amapari: MPEG 19698. Erythrolamprus miliaris- Serra do Navio: MPEG 334–5. Erythrolamprus poecilogyrus- Serra do Navio: MPEG 196. Erythrolamprus reginae- Pedra Branca do Amapari: MPEG 19780, MPEG 19788. Erythrolamprus rochaiPedra Branca do Amapari: MPEG 25680–1. Erythrolamprus typhlus- Serra do Navio: IEPA1910. Helicops angulatus- Pedra Branca do Amapari: MPEG 19685. Hydrodynastes gigas- Serra do Navio: MPEG 26580. Imantodes cenchoa- Serra do Navio:

IEPA1909. Leptodeira annulata- Serra do Navio: MPEG 26576. Leptophis ahaetulla- Pedra Branca do Amapari: MPEG 19684; Serra do Navio: MPEG 26574. Mastigodryas boddaerti- Serra do Navio: MPEG 181. Micrurus lemniscatus- Pedra Branca do Amapari: MPEG19692–4; Serra do Navio: MPEG 16695, MPEG 26571–2. Micrurus surinamensis- Serra do Navio: MPEG 26570. Oxybelis aeneus- Pedra Branca do Amapari: MPEG 22840. Oxyrhopus melanogenys- Serra do Navio: MPEG 26579. Oxyrhopus petolarius- Pedra Branca do Amapari: MPEG 19696. Philodryas argentea Pedra Branca do Amapari: MPEG 19687; Serra do Navio: 26590. Philodryas viridissima- Pedra Branca do Amapari: MPEG 19681–2; Serra do Navio: MPEG 327, MPEG 329. Pseudoboa coronata- Pedra Branca do Amapari: MPEG 19676. Pseudoboa neuwiedii- Pedra Branca do Amapari: MPEG 26591. Rhinobothryum lentiginosum- Pedra Branca do Amapari: MPEG 19789. Siagonodon septemstriatus- Sera do Navio: MPEG 18492.Siphlophis compressus- Pedra Branca do Amapari: MPEG 26574, MPEG 26576. Spilotes pullatus- Sera do Navio: IEPA1911. Spilotes sulphureus- Pedra Branca do Amapari: MPEG 19794, MPEG 25760; Serra do Navio: MPEG 333. Taeniophallus brevirostris- Pedra Branca do Amapari: MPEG 19699, MPEG 19785, MPEG 19820–1. Taeniophallus nicagus- Pedra Branca do Amapari: MPEG 19786. Thamnodynastes lanei- Serra do Navio: MPEG 26589. Typhlophis squamosus- Pedra Branca do Amapari: MPEG 19787, MPEG 22844–5; Serra do Navio MPEG 26586–8. Xenodon rabdocephalus- Pedra Branca do Amapari: MPEG 19691; Serra do Navio: MPEG 328, MPEG 331–2. Xenodon severus- Pedra Branca do Amapari: MPEG 22847. Xenopholis scalaris- Pedra Branca do Amapari: MPEG 19677.

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Trabajo

Estados de desarrollo en Anadia bogotensis: aportes a la comprensión de la evolución del plan corporal en Gymnophthalmoidea (Squamata) Adriana Jerez1, Andrea Bonilla-Garzón2, David Samuel Castellanos Montilla3 Laboratorio de Ecología Evolutiva, Departamento de Biología, Facultad de Ciencias, Universidad Nacional de Colombia, Sede Bogotá. Carrera 45 N° 26-85, Bogotá, Colombia. 2 Universidad Autónoma de Baja California Sur, Km 5.5 Carretera al Sur, Mezquitito, La Paz, Baja California Sur 23080, México. 3 Laboratorio de Ecología Evolutiva, Departamento de Biología, Facultad de Ciencias, Universidad Nacional de Colombia, Sede Bogotá. Carrera 45 N° 26-85, Bogotá, Colombia. 1

Recibido: 15 Abril 2020 Revisado: 18 Mayo 2020 Aceptado: 05 Junio 2020 Editor Asociado:

J. Goldberg

doi: 10.31017/CdH.2020.(2020-018)

ABSTRACT Embryonic development in Anadia bogotensis and body plan evolution in Gymnophthalmoidea (Squamata). Gymnophthalmoidea lizards inhabit in Central and South America from lowlands to highland Andes. This clade presents species with different body plans; lacertiform species exhibit short and robust bodies and well-developed limbs whereas serpentiform species have elongate bodies and limb reduction. Between these two extreme body plans, we found intermediate forms such as Anadia bogotensis, with a less elongated body and limbs fully developed but not very robust. We describe the embryonic development of Anadia bogotensis, and compare it with serpentiform species of Gymnophthalmidae, and lacertiform species of Teiidae and Alopoglossidae. We found differences in the development time in somites and limbs. With respect to lacertiform species, there is an accelerated development of somites in serpentiform gymnophthalmids, which is involved in body elongation. Besides, hypomorphosis is the heterochronic perturbation involved in limb reduction. Therefore, there are differences in the development time of different structures, which are related to the evolution of body plans in Gymnophthalmoidea. Key words: Body elongation; Heterochrony; Limb development; Gymnophthalmidae; Somites. RESUMEN Los lagartos del clado Gymnophthalmoidea se encuentran distribuidos en zonas bajas y altas de los Andes de América. Este clado presenta especies con diferentes planes corporales, desde lacertiformes con cuerpo robusto y extremidades bien desarrolladas, a especies serpentiformes con cuerpos elongados y extremidades reducidas a ausentes. Entre estos dos extremos, encontramos especies con formas intermedias como Anadia bogotensis que exhibe un cuerpo menos elongado y extremidades pentadáctilas. En este trabajo, describimos el desarrollo embrionario de la lagartija altoandina Anadia bogotensis, y lo comparamos dentro del clado Gymnophthalmoidea con especies serpentiformes de Gymnophthalmidae, y especies lacertiformes de Teiidae y Alopoglossidae. Estas especies presentan diferencias en el desarrollo de somitas y las extremidades. Respecto a especies lacertiformes, la aceleración es responsable de un mayor número de somitas y el alargamiento corporal, y la hipomorfosis de la reducción y pérdida de las extremidades en las especies serpentiformes de Gymnophthalmidae. Por lo tanto, cambios heterocrónicos están involucrados en la evolución del plan corporal en Gymnophthalmoidea. Se necesitan información del desarrollo de una mayor cantidad de especies en este clado, para ampliar esta hipótesis. Palabras clave: Alargamiento corporal; Desarrollo de extremidades; Gymnophthalmidae; Heterocronías; Somitas.

Introducción Los cambios más conspicuos entre formas lacertiformes y serpentiformes en Squamata se concentran en

la miniaturización del cráneo, la elongación y reducción de volumen corporal y la reducción y pérdida

Autor para correspondencia: arjerezm@unal.edu.co

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A. Jerez et al. - Desarrollo en Anadia bogotensis de extremidades (Presch, 1975; Gans, 1975; Lande, 1978; Griffith, 1990; Greer, 1991; Wiens y Slingluff, 2001; Grizante et al., 2012). Brandley et al. (2008) con base en datos morfométricos encontraron que el alargamiento corporal y la reducción de extremidades son rasgos morfológicos que evolucionan juntos en la transición de formas lacertiformes a serpentiformes; y que las formas intermedias, entre estos dos extremos, han permanecido en la naturaleza por largos periodos en la historia evolutiva de los Squamata. Un grupo en el cual se pueden analizar estas variaciones es el clado Gymnophthalmoidea, conformado por Alopoglossidae, Teiidae y Gymnophthalmidae (Goicoechea et al., 2016). En Gymnophthalmidae, Pellegrino et al. (2001) determinaron que existe alargamiento corporal cuando el número de vértebras es mayor a 27, una condición del plan corporal serpentiforme, que evolucionó independientemente cinco veces en esta familia. Además, resaltan la existencia de géneros como Anadia, Euspondylus y Proctoporus que presentan de 27 a 29 vértebras, indicando la existencia de formas intermedias. Posteriormente, Grizante et al. (2012) con base en datos morfométricos establecieron que el alargamiento corporal es una característica de Gymnophthalmidae y Alopoglossidae, categorizando las especies en formas menos elongadas y más elongadas. Finalmente, en Gymnophthalmoidea existen especies lacertiformes con 25 a 26 vértebras, y por lo tanto se considerada que no presentan alargamiento corporal, y sus extremidades son robustas y generalmente pentadáctilas, como Aspidoscelis en Teiidae (Hoffstetter y Gasc, 1969; Veronese y Krause, 1997). El desarrollo embrionario es una fase crítica para lagartos altoandinos como Anadia bogotensis, que se distribuye entre los 2000 a 4000 m s.n.m en el altiplano Cundiboyacense de Colombia (Jerez y Calderón-Espinosa, 2014). Las hembras de esta especie depositan solo dos huevos en nidos comunales (Clavijo y Fajardo, 1981, Medina-Rangel, 2013) y los embriones se desarrollan en condiciones extremas. En el caso del ecosistema de páramo se ha registrado que los nidos están expuestos a condiciones fluctuantes de temperaturas (0 °C a 30 °C), un amplio rango de humedad (1,9 a 48,4%) y alta radiación solar (Calderón-Espinosa et al., 2018). Estos son factores que no solo pueden llegar a ser determinantes para el completo desarrollo de los embriones, sino que también imponen presiones selectivas que influencian las características fenotípicas importantes para 164

la sobrevivencia durante la vida postnatal (Warner y Andrews, 2002). Sin embargo, en el neotrópico los estudios sobre el desarrollo de especies altoandinas son inexistentes, a pesar de que pocas habitan en los ambientes paramunos del altiplano Cundiboyacense, como es el caso de A. bogotensis, Riama striata, Stenocercus trachycephalus, Anolis heterodermus y Atractus crassicaudatus (Castaño et al., 2000; Paternina y Capera-M, 2017; Méndez-Galeano y Pinto-Erazo, 2018). Existen alrededor de 6512 especies de lagartos en el mundo (Uetz et al., 2018) pero las descripciones sobre los estados de desarrollo aún no son abundantes, como destacan Fabrezi et al. (2017). Tal es el caso de la familia Gymnophthalmidae, que solo cuenta con la descripción de los lagartos serpentiformes Nothobachia ablephara y Calyptommatus sinebrachiatus (Roscito y Rodrigues, 2012 a). Por lo tanto, en este trabajo describimos el desarrollo embrionario del gimnoftálmido altoandino Anadia bogotensis, una forma intermedia y menos elongada, y lo comparamos con especies serpentiformes en Gymnophthalmidae y especies lacertiformes de Teiidae y Alopoglossidae. Esto con el fin de comparar el desarrollo de las características relacionadas con las transformaciones del plan corporal y discutir las heterocronías implicadas en su evolución, dentro del clado Gymnophthalmoidea. Materiales y métodos Los nidos de Anadia bogotensis fueron encontrados en la vereda Las Moyas, municipio de La Calera (Departamento de Cundinamarca, Colombia), a 3100 m s.n.m sobre la vertiente occidental de la Cordillera Oriental de los Andes en Colombia. Lo nidos comunales variaron entre dos a 56 huevos, encontrándose bajo rocas, inmersos en tierra húmeda y cáscaras en descomposición de anteriores nidadas. Los embriones no fueron incubados y se fijaron en formol al 10% y conservados en alcohol etílico al 70%. El tiempo de incubación para esta especie es de 180 a 210 días (Clavijo y Fajardo, 1981). En total se incluyeron 55 embriones, que se clasificaron en 14 estados con base en características de la morfología externa. Con fines comparativos se usaron los caracteres propuestos por Werneburg (2009) para análisis comparados de embriones en vertebrados. Para identificar patrones heterocrónicos en el clado Gymnophthalmoidea (Goicoechea et al., 2016) se eligieron de los caracteres propuestos

Cuad. herpetol. 34 (2): 163-174 (2020) por Wenerburg (2009) solo las somitas y las extremidades, ya que son características observables durante el desarrollo embrionario y significativas en la evolución del plan corporal en Squamata. Para esto se compararon los cambios observados en Anadia bogotensis con otras especies de Gymnophthalmidae, Alopoglossidae y Teiidae (Goicoechea et al., 2016), y se consideraron los tiempos de desarrollo con base en Billy (1988), Roscito y Rodrigues (2012a) y Lungman et al. (2019). Para determinar las variaciones se establecieron características para tres planes corporales, con base en Pellegrino et al. (2001) y Grizante et al. (2012) para gimnoftálmidos: a) Lacertiforme: tronco y extremidades robustas, sin alargamiento corporal y con 26 vértebras presacras; en este análisis se incluyeron el alopoglossido Ptychoglossus bicolor y los teíidos Aspidoscelis uniparens y Salvator merianae (Billy, 1988; Veronese y Krause, 1997; Lungman et al., 2019; Jerez, obs. pers.). b) Intermedio: tronco y extremidades menos robustas, menos elongadas, con 27 a 29 vértebras presacras, como se observa en Anadia bogotensis (Jerez, obs. pers.). c) Serpentiforme: troncos delgados, reducción y pérdida de extremidades, muy elongadas contando con más de 30 vértebras presacras, como se observa en Nothobachia ablephara y Calyptommatus sinebrachiatus (Roscito y Rodrigues, 2012a; Grizante et al., 2012). Resultados Se describen las características de los embriones de Anadia bogotensis desde el momento de la ovoposición, estado 1, hasta que el embrión exhibe características similares al neonato, estado 14. Por lo tanto, para cada estado se incluyeron características de la morfología externa, iniciando con la región cefálica con el desarrollo del mesencéfalo, los órganos sensoriales y los arcos faríngeos; siguiendo con la región troncal con el desarrollo de las somitas, las extremidades y los órganos genitales; y finalizando con la región caudal con el desarrollo de la cola. También, se adicionaron características del tegumento como el desarrollo de las escamas y la pigmentación. La talla promedio de los neonatos fue de 23,36 mm longitud hocico-cloaca (n=11). Estado 1 (Fig. 1A) Cabeza: flexión cervical de 90˚. El mesencéfalo se proyecta dorsalmente. Ojo: se insinúa la vesícula óptica.

Arcos faríngeos: los esbozos del primer y segundo arco faríngeo están presentes; estos corresponden al proceso mandibular y el arco hioideo, respectivamente. Somitas: 10 a 15 pares. Cola: el esbozo de la cola es corto y no presenta somitas. Estado 2 (Fig. 1B) Cabeza: el mesencéfalo es prominente. Ojo: el ojo es grande y exhibe el contorno de la vesícula del cristalino en la región central de la vesícula óptica. Se observa la fisura coroidea casi cerrada. Se destaca una leve pigmentación en la región medial del ojo. Oído: la plácoda ótica es grande y se ubica hacia la región lateral del cuello del embrión. Nariz: la plácoda nasal se evidencia como un pequeño orificio en la región nasal del embrión. Arcos faríngeos: se observan cuatro arcos y las tres primeras hendiduras faríngeas. El primer arco faríngeo está constituido por el proceso maxilar dorsalmente, y el proceso mandibular ventralmente. El proceso maxilar se extiende anteriormente, a nivel del borde anterior de la vesícula del cristalino; mientras que el proceso mandibular se extiende a nivel del borde posterior de la vesícula del cristalino. Somitas: 30-35 pares. Extremidades: se observa el esbozo de la extremidad anterior y posterior, cada uno de los cuales es tan alto como ancho. Cola: es prominente, se curva una vez y se visualizan las somitas. Estado 3 (Fig. 1C) Ojo: la fisura coroidea está cerrada. Arcos faríngeos: solo se observan tres arcos faríngeos, y solo la primera hendidura faríngea permanece abierta. El proceso maxilar se extiende anteriormente a nivel del borde anterior del ojo, mientras que el proceso mandibular no presenta cambios. Somitas: 35 a 40 pares. Extremidades: los esbozos de las extremidades son más largos que anchos. Cola: presenta dos vueltas. Estado 4 (Fig. 1D) Ojo: completamente pigmentado, y se delimita una región concéntrica más oscura, que corresponde al iris con la pupila en el centro de la vesícula óptica. 165

A. Jerez et al. - Desarrollo en Anadia bogotensis

Figura 1. Estados de desarrollo en Anadia bogotensis, desde la ovoposiciรณn en el estado 1 (A), hasta antes del nacimiento en el estado 14 (N). En los estados 2 (B) al estado 8 (H) se destacan los cambios en el desarrollo de las extremidades.

166

Cuad. herpetol. 34 (2): 163-174 (2020) Arcos faríngeos: la primera hendidura faríngea casi cerrada. Extremidades: en cada esbozo se empieza a delimitar el estilopodio y el zeugopodio. Distalmente, el autopodio se ensancha destacando la condición de forma de remo del esbozo. Papila urogenital: se observa una papila pequeña ubicada medial y ventralmente, en la base de los esbozos de la extremidad posterior. Estado 5 (Fig. 1E) Arcos faríngeos: todas las hendiduras faríngeas cerradas y no se observan arcos faríngeos, salvo por los derivados del primer arco. El extremo del proceso maxilar alcanza la prominencia frontonasal; mientras que el proceso mandibular se extiende anteriormente, a la altura del borde anterior de la pupila. Extremidades: se hace evidente la flexión a nivel del codo y la rodilla, delimitándose claramente el estilopodio y el zeugopodio. El autopodio se ensancha y deprime formando la placa digital. Estado 6 (Fig. 1F) Ojo: se observan las papilas esclerales. Arcos faríngeos: el extremo distal de cada uno de los procesos mandibulares se extiende anteriormente, y se encuentran entre sí, medialmente. Extremidades: la placa digital exhibe cinco crestas digitales y presenta el borde anterior serrado. Estado 7 (Fig. 1G) Ojo: no se observan las papilas esclerales. Arcos faríngeos: el proceso maxilar se fusiona con el proceso frontonasal. El proceso mandibular se desarrolla hasta el punto de cierre con la mandíbula superior. Extremidades: los dedos se observan independientes y solo se conserva la membrana interdigital en la región basal. Las garras empiezan a diferenciarse. Región urogenital: se observa el esbozo de los hemipenes. Escamas: se empiezan a diferenciar las escamas en la región dorsal del tronco, incluyendo la cola. Estado 8 (Fig. 1H) Ojo: dorsalmente se cubre de tegumento, y ventralmente se empieza a diferenciar el párpado inferior como un engrosamiento de tegumento. Extremidad: los dedos se encuentran totalmen-

te libres entre sí, desaparece totalmente la membrana interdigital. Cola: es robusta y muy larga. Estado 9 (Fig. 1I) Ojo: se encuentra cubierto de tegumento, y el párpado inferior continúa desarrollándose, pero no alcanza aún la región del iris. Extremidades: dedos con garras completamente diferenciadas. Escamas: se empiezan a diferenciar las escamas en la región ventral del tronco. Estado 10 (Fig. 1J) Cabeza: se alarga posteriormente y el mesencéfalo ya no sobresale notablemente. Ojo: el párpado inferior cubre el ojo hasta el borde inferior del iris. Escamas: se diferencian las escamas en el hocico, la gula, los dedos y la cola. Estado 11 (Fig. 1K) Ojo: el párpado inferior cubre el ojo hasta el borde inferior de la pupila. Escamas: todo el cuerpo con escamas diferenciadas, pero con pigmentación solo en la región dorsal del cuerpo. Estado 12 (Fig. 1L) Escamas: aumenta la pigmentación en la región dorsal y se extiende hacia las regiones laterales del tronco. Se observa pigmentación en la región dorsal de la cabeza. Estado 13 (Fig. 1M) Ojo: el párpado inferior alcanza a cubrir la región ventral de la pupila. Oído: la membrana timpánica es evidente. Escamas: la pigmentación es uniforme en las escamas de la región dorsal del tronco, y se incrementa en la región dorsal y lateral de la cabeza. Estado 14 (Fig. 1N) Cabeza: desaparece completamente el abultamiento de la región parietal y occipital de la cabeza y se observa uniforme. Ojo: el párpado inferior cubre casi completamente el ojo. Escamas: todas las escamas del cuerpo completamente diferenciadas y con la coloración similar a la del adulto. 167

A. Jerez et al. - Desarrollo en Anadia bogotensis Discusión Anadia bogotensis es una especie altoandina con actividad reproductiva continua, nidos comunales, una postura constituida por dos huevos y un desarrollo embrionario entre 180 a 210 días (Clavijo y Fajardo, 1981; Jerez y Calderón-Espinosa, 2014). En escamados, la temperatura y la humedad en la cual se desarrollan los embriones afecta el fenotipo de los neonatos (Andrews, 2000; Brown y Shine, 2004). A pesar de las condiciones extremas del subpáramo y páramo en las cuales se desarrollan los embriones de A. bogotensis presentaron un desarrollo normal, es decir, no se encontraron embriones, ni neonatos con deformaciones. Por otro lado, se han reportado en los mismos sitios de nidación, huevos en descomposición, afectados por hongos, deshidratados y atacados por hormigas (Clavijo y Fajardo, 1981; Medina-Rangel, 2013; Calderón-Espinosa et al., 2018). Algunos clados ovíparos de Lepidosauria presentan un desarrollo embrionario entre 100 a 460 días (Sphenodon, Furcifer, Chamaeleo, Trachylepis, Varanus, Saint-Girons, 1985; Fleming, 1994). Sin embargo, a diferencia de las especies de estos géneros, A. bogotensis exhibe distribución altoandina a paramuna (2200 a 4000 m s.n.m), y los embriones se desarrollan bajo condiciones ambientales fluctuantes y extremas de temperatura y humedad, junto con una alta radiación (Calderón-Espinosa et al., 2018). Además, en las especies ovíparas de escamados se ha encontrado que las temperaturas bajas aumentan el tiempo total de incubación (Qualls y Andrews, 1999; Parker y Andrews, 2007). Por lo tanto, estos factores ambientales podrían estar implicados en un periodo de incubación que se extiende entre 180 a 210 días en A. bogotensis (Clavijo y Fajardo, 1981), ya que es mayor respecto a otras especies de gimnoftálmidos hasta hoy conocidos que habitan en tierras bajas, como N. ablephara y C. sinebrachiatus, cuyo periodo de incubación es de 45 días (Roscito y Rodrigues, 2012a). Adicionalmente, A. bogotensis no presenta retención embrionaria, y probablemente tampoco diapausa embrionaria, ya que el embrión es depositado cuando está finalizando la neurulación (estado 1). Condición que comparte con Ptychoglossus bicolor, A. uniparens, S. merianae, N. ablephara y C. sinebrachiatus que habitan principalmente en tierra bajas en el neotrópico (Billy, 1988; Roscito y Rodrigues, 2012a Lungman et al., 2019; Jerez, obs. pers). En este 168

sentido, a pesar de que A. bogotensis alcanza a distribuirse sobre los 4000 m, no exhibe estrategias como la retención embrionaria relacionada con una mayor sobrevivencia de los embriones en climas fríos, y que ha sido asociada a la evolución de la viviparidad en escamados (Qualls y Andrews 1999, Andrews, 2000). Foster et al., (2020) encontraron que existen factores fisiológicos como la adecuación del útero, el intercambio gaseoso y la respuesta inmune que varían entre poblaciones ovíparas y vivíparas, los cuales dependen de la expresión génica diferencial durante el ciclo reproductivo de las hembras y están asociadas a la evolución de la viviparidad. Por lo tanto, en un clado como Gymnophthalmoidea donde no ha evolucionado la viviparidad (Vitt y Caldwell, 2009), y considerando su condición de ectotermos, deben existir factores fisiológicos para que las especies mantengan las características de su modo reproductivo ovíparo y para que los embriones sobrevivan en estos ambientes. Factores que aún no conocemos y que son fundamentales para el diseño de estrategias de conservación. Respecto a lagartos lacertiformes, Rieppel (1984) estableció cambios morfológicos del cráneo en varias especies ápodas, en un escenario donde la miniaturización y la fosorialidad orientaron dichos cambios. En el caso de los gimnoftálmidos, las especies serpentiformes fosoriales y semifosoriales exhiben cabezas más pequeñas, variaciones craneales, y cambios asociados con los órganos de los sentidos, como pérdida del párpado y del tímpano (Pellegrino et al., 2001; Tarazona y Ramírez-Pinilla, 2008; Barros et al., 2011; Roscito y Rodrigues, 2010, 2012 b; Holovacs et al., 2019). En formas intermedias como Anadia bogotensis no se observan reducciones en la región cefálica durante el desarrollo (Fig. 1). En general, A. bogotensis, P. bicolor, A. uniparens, y S. merianae desarrollan completamente la región facial asociada al primer arco branquial, y exhiben los mismos cambios en los ojos y el oído, aunque presentan leves diferencias en los tiempos de desarrollo, que no derivan en transformaciones evidentes (Tabla 1). Sin embargo, en C. sinebrachiatus el ojo se reduce de tamaño y junto con la abertura del oído son cubiertos por escamas en el último estado (12) antes del nacimiento (Roscito y Rodrigues, 2012 a); cambios que probablemente también ocurren en N. ablephara hacia el final del desarrollo embrionario. Siendo estas transformaciones las más evidentes en la región cefálica, y que han sido asociado con hábitos fosoriales en gimnoftálmidos serpentiformes

Cuad. herpetol. 34 (2): 163-174 (2020) Tabla 1. Desarrollo de características asociadas a la cabeza como la región facial, los ojos y el oído en diferentes especies del clado Gymnophthalmoidea. E: estado de desarrollo; D: días después de la ovoposición; H: horas después de la ovoposición; (?): sin información de tiempo y/o estado de desarrollo. Especies Eventos Primer arco faríngeo formado

Ptychoglossus bicolor

Aspidoscelis uniparens

Salvator merianae

Anadia Nothobachia bogotensis ablephara

Calyptommatus sinebrachiatus

E1/1D

E3/20H

E3/3D

E1/1D

E1/2-4D

E1/2-3D

Fusión de los proceso maxilar y nasal

E10/D(?)

ED(?)

E7/D(?)

E4/14D

E7/15-17D

Proceso mandibular completo, cerrando con la mandíbula superior

E12/D(?)

E13/23D

E10/15D

E7/D(?)

E6/18-20D

E9/20D

Aparición vesícula óptica

E1/1D

E2/4H

E3/3D

E13/D(?)

E1/2-4D

Fisura coroidea cerrada

E7/D(?)

E10/2D

E6 (6D)

E3/D(?)

E2/6-8D

E3/5D

Párpados completos

E18/D(?)

E17/70D

E17 (45D)

E14/D(?)

ED(?)

E11/26-34D

ED(?)

E12/45D

El ojo se reduce y es cubierto por una escama Papilas esclerales

E11/D(?)

E6/D(?)

Vesícula ótica evidente

E1/1D

E3/20H

E2/D(?)

E1/2-4D

E1/2-3D

Membrana timpánica diferenciada

E18/D(?)

E15/46D

E15/33D

E13/D(?)

ED(?)

E12/45D

ED(?)

E12/45D

Roscito y Rodrigues (2012a)

Tímpano cubierto por una escama Fuente

Este trabajo

Billy (1988)

(Pellegrino et al., 2001; Roscito y Rodrigues, 2012 a). Las papilas esclerales fueron observadas en los embriones de A. bogotensis y P. bicolor (Tabla 1). Estas estructuras son indispensables para desarrollar los osículos y anillos esclerales (Hall, 2015), los cuales se observan en el esqueleto de embriones avanzados de A. bogotensis y P. bicolor (Jerez, obs. pers.). Los anillos esclerales han sido registrados para Aspidoscelis y otros teíidos y gimnoftálmidos por Atkins y Franz-Odendaal (2016). Estos mismos autores encuentran que en Squamata los anillos esclerales son más pequeños en especies fotópicas y fosoriales, respecto a especies escotópicas y no fosoriales. Por lo tanto, la ausencia de las papilas y anillos esclerales en las especies serpentiformes y fosoriales C. sinebrachiatus y N. ablephara apoya este patrón (Roscito y Rodrigues, 2012a, b), y desde estados embrionarios se evidencia que estas estructuras no se desarrollan, respecto a especies lacertiformes y formas intermedias como A. bogotensis. La evolución del plan corporal lacertiforme y serpentiformes en Squamata está relacionada con transformaciones evidentes en el tronco, entre las cuales se encuentran el alargamiento corporal con el aumento de las vértebras presacras (Gans, 1975; Griffith, 1990; Wiens y Slingluff, 2001; Greer y Wadsworth, 2003), y cuya diferenciación depende

Lungman et al. (2019)

Este trabajo

del desarrollo de somitas durante la embriogénesis. Al momento de la ovoposición, especies intermedias (menos elongadas) como A. bogotensis y las especies lacertiformes (no elongadas) A. uniparens, S. merianae y P. bicolor presentan entre 9 y 16 pares de somitas (Fig. 2, Billy, 1988; Lungman et al., 2019; Jerez, obs. pers.). Mientras que las especies serpentiformes (más elongadas) como C. sinebrachiatus y N. ablephara presentan 36 y 46 pares de somitas, respectivamente (Fig. 2, Roscito y Rodrigues, 2012 a). Indicando que al final de la neurulación e inicio de la organogénesis, las formas lacertiformes e intermedias presentan un bajo número de somitas, respecto a las especies serpentiformes. Esto corresponde al patrón observado en vertebrados, donde el alargamiento corporal en tetrápodos está relacionado con un mayor número de somitas, y a un fenómeno de aceleración durante la somitogénesis (Singarete et al., 2015). Además, en Squamata se asocia con la diferenciación de un mayor número de vértebras en especies serpentiformes, respecto a especies lacertiformes (Stokely, 1947; Hoffstetter y Gasc, 1969; Presch, 1975; Greer, 1987, 1991; Choquenot y Greer, 1989; Caputo et al., 1995; Wiens y Slingluff, 2001; Greer y Wadsworth, 2003). Werneburg (2009) establece un rango máximo de pares de somitas entre 46 a 50 pares en la 169

A. Jerez et al. - Desarrollo en Anadia bogotensis

Figura 2. Desarrollo de somitas, plan corporal, estados y tiempo total de desarrollo en especies de las familias Alopoglossidae, Teiidae y Gymnophthalmidae (Goicoechea et al., 2016). En el momento de la ovoposición al inicio del desarrollo (α), las barras cortas representan el rango de somitas entre 9 y 16 pares en P. bicolor, A. uniparens, S. merianae y A. bogotensis; las barras medinas representan rango mayor, de 36 a 46 pares de somitas, en C. sinebrachiatus y N. ablephara. Cuando se completa el desarrollo de las somitas (β), las barras medianas representan el rango de somitas entre 35 a 40 pares, mientras que las barras más largas representan un rango de 52 y 53 pares. La información se obtuvo con base en Billy (1988), Roscito y Rodrigues (2012a), Lungman et al. (2019) y Jerez (obs. pers.). E: estado de desarrollo; D: días después de la ovoposición; H: horas después de la ovoposición; (?): sin información de tiempo y/o estado de desarrollo.

región precaudal de los vertebrados. A. bogotensis y P. bicolor exhiben 35 y 40 pares de somitas, pero N. ablephara y C. sinebrachiatus presentan 52 y 53 (Fig. 2, Roscito y Rodrigues, 2012a). No obstante, Billy (1988) observó en A. uniparens entre 56 a 62 pares de somitas, número que probablemente incluye las somitas de la cola, ya que no se ajusta al número máximo de pares de somitas observado en otras especies de lagartos lacertiformes, como Anolis (32) y Zootoca vivipara (50) (Dufaure y Hubert, 1961; Sanger et al., 2008). Entonces, dentro de Gymnophthalmidae y Alopoglossidae el número de somitas de especies menos elongadas y lacertiformes como A. bogotensis y P. bicolor, es mucho menor que las especies serpentiformes durante todo el desarrollo. 170

Por lo tanto, respecto a A. bogotensis, el número de somitas es notablemente mayor en las especies serpentiformes de Gymnophthalmidae, destacando la aceleración (Peramorfosis, Reilly et al., 1997) como la perturbación heterocrónica relacionada con este aumento de somitas, como se observa en Gymnophthalminae (Fig. 2). Grizante et al. (2012) encontraron que en Gymnophthalmidae evolucionó conjuntamente el aumento de la longitud del tronco, la reducción de volumen corporal y la reducción y pérdida de extremidades. La relación entre el alargamiento y la reducción de volumen corporal fue un patrón registrado por Gans (1975) para Squamata, en especies serpentiformes. Las formas intermedias

Cuad. herpetol. 34 (2): 163-174 (2020) como A. bogotensis son menos elongadas y solo exhiben una aparente reducción del diámetro y volumen del tronco, a pesar de que exhibe entre 27 a 29 vértebras presacras (Jerez, obs. pers.). Para Grizante et al. (2012) las especies con mayor alargamiento corporal son delgadas, y corresponden a especies que presentan mayor número de vértebras, indicando que la reducción de volumen evoluciona conjuntamente con un alto número de somitas en Gymnophthalmidae. Anadia bogotensis es una especie pentadáctila, condición compartida con P. bicolor, A. uniparens y S. merianae (Billy, 1988; Lungman et al., 2019; Jerez, obs. pers.); mientras que las otras dos especies exhiben extremidades muy cortas, pero varían en su morfología, N. ablephara exhibe un dedo en la extremidad anterior y dos dedos en la extremidad posterior, y C. sinebrachiatus no exhibe extremidad anterior y la posterior presenta un solo dedo (Roscito y Rodrigues, 2012a, b). Estas diferencias entre especies pentadáctilas y especies con reducciones se

destacan desde el desarrollo, ya que en general estas especies empiezan a desarrollar las extremidades entre los estados 1 al 4, que corresponden al segundo y cuarto día después de la ovoposición y probablemente así sea para A. bogotensis y P. bicolor. Sin embargo, se destaca el momento en el que terminan de desarrollarlas, P. bicolor, A. uniparens y S. merianae completan el desarrollo de la extremidad hacia el estado 13 y 14, día 27 después de la ovoposición en las dos últimas especies (Fig. 3); mientras que en A. bogotensis, N. ablephara y C. sinebrachiatus ocurre en los estados 9 al 11 (Fig. 3), hacia los días 23 y 24 en las dos últimas especies, que además exhiben grandes reducciones en las extremidades. Respecto a las especies pentadáctilas, el desarrollo de la extremidad termina más tempranamente en las especies serpentiformes, con reducciones drásticas como se representan en la figura 3; siendo, la hipomorfosis (Paedomorfosis) la perturbación heterocrónica relacionada con la reducción en las extremidades. Por lo tanto, en Gymnophthalmidae

Figura 3. Desarrollo y momentos de aparición de la extremidad anterior y posterior en especies de las familias Alopoglossidae, Teiidae y Gymnophthalmidae (Goicoechea et al., 2016). Los eventos del desarrollo se obtuvieron de Billy (1988), Roscito y Rodrigues (2012a), Lungman et al. (2019) y Jerez (obs. pers). E: estado de desarrollo; D: días después de la ovoposición; H: horas después de la ovoposición; (?): sin información de tiempo y/o estado de desarrollo.

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A. Jerez et al. - Desarrollo en Anadia bogotensis un desarrollo truncado de las extremidades (hipomorfosis según Reilly et al., 1997) se reconoce como el mecanismo involucrado en la reducción de las extremidades en este grupo (Fig. 3). Las cuales incluyen reducción de tamaño de toda la extremidad, reducción del número de dedos, hasta la pérdida de toda la extremidad como se observa en Gymnophthalminae (Fig. 3). En los vertebrados, la expresión de Sonic hedgehog (Shh) durante el desarrollo de las extremidades es responsable de especificar el eje anteroposterior (zona de actividad polarizante), mantener la expresión de FGF8 involucrada en la proliferación de la mesénquima y especificar el eje próximo-distal de los miembros (Gilbert, 2010). Shapiro et al. (2003) encontraron en Hemiergis (Scincidae), que respecto a especies pentadáctilas la reducción en la concentración de Shh está relacionada con la reducción y pérdida de las extremidades en especies serpentiformes del mismo género. Si bien, no existen estos análisis en especies pentadáctilas como A. bogotensis en gimnoftálmidos, si se han realizado en especies serpentiformes. Roscito et al. (2014) determinaron para C. sinebrachiatus que el esbozo de la extremidad anterior se desarrolla solo por 9 a 10 días, y cuando se detiene el desarrollo del esbozo no se detecta la expresión de Sonic hedgehog, mientras que, si se detectó en el esbozo de la extremidad posterior, hasta desarrollar una extremidad corta y reducida (Roscito y Rodrigues, 2012 b; Roscito et al., 2014). Por lo tanto, es posible que Gymnophthalmidae comparta el mismo patrón de la expresión de Sonic hedgehog (Shh) descrito para Hemiergis, entre especies pentadáctilas y especies con reducciones. En conclusión, las tablas de desarrollo ofrecen información para analizar la evolución de características particulares en los diferentes clados. Los embriones de A. bogotensis exhiben un desarrollo normal, a pesar de las condiciones ambientales extremas en las que habitan. Respecto a la evolución del plan corporal en Gymnophthalmoidea, al comparar el desarrollo de las somitas y las extremidades de A. bogotensis con otras especies, encontramos que respecto a especies lacertiformes y serpentiformes existen cambios heterocrónicos que involucran dos perturbaciones diferentes. Por un lado, la evolución del alargamiento corporal está relacionado con la aceleración en el desarrollo de las somitas (Peramorfosis), mientras que la reducción de extremidades se asocia con hipomorfosis (Paedomorfosis). Sin embargo, se necesitan descripciones de un mayor 172

número de especies con información de tiempos de incubación en este clado, para desarrollar con mayor soporte estas hipótesis. Agradecimientos Los autores agradecen al Laboratorio de Equipos Ópticos Compartidos (LEOC) del Departamento de Biología, Facultad de Ciencias, Universidad Nacional de Colombia, Sede Bogotá. Este estudio fue financiado por el Programa Nacional de Semilleros de Investigación, Creación e Innovación, 2013-2015, Universidad Nacional de Colombia, Sede Bogotá. A Itza Hinumaru Torres y Juan C. Ríos-Orjuela por la digitalización de las figuras. Al editor y a los revisores anónimos por sus valiosas observaciones y sugerencias. Literatura citada

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Diet overlap of three sympatric species of Leptodactylus Fitzinger (Anura: Leptodactylidae) in a Protected area in the Brazilian Amazon Raimundo Rosemiro de Jesus Baia1, Patrick Ribeiro Sanches1, Fillipe Pedroso dos Santos1, Alexandro Cezar Florentino2, Carlos Eduardo Costa-Campos1 Laboratório de Herpetologia, Departamento de Ciências Biológicas e da Saúde, Universidade Federal do Amapá, Campus Marco Zero do Equador, 68903-419, Macapá, Amapá, Brazil. 2 Laboratório de Absorção Atômica e Bioprospecção, Programa de Pós-Graduação em Biodiversidade Tropical (PPGBio), Universidade Federal do Amapá, Campus Marco Zero do Equador, Macapá, 68903-419, Amapá, Brazil. 1

Recibido: 10 Febrero 2020 Revisado: 27 Abril 2020 Aceptado: 08 Julio 2020 Editor Asociado:

D. N a y a

doi: 10.31017/CdH.2020.(2020-006)

ABSTRACT Closely related species are often similar in morphological and ecological characters, which may lead them to compete when occurring in sympatry. In this sense, we analyzed trophic niche overlap among three Leptodactylus species, Leptodactylus macrosternum, L. fuscus and L. aff. podicipinus, in a floodplain environment from a Protected area in the Brazilian Amazon. In addition, we applied Network and Non-metric multidimensional scaling (NMDS) analysis. We found 18 prey categories, most of them belonging to Arthropoda (94.4%). Coleoptera, Isoptera, Diptera and Hymenoptera were the most abundant prey on the diet shared among the three species. The rarefaction curve of prey richness did not reach an asymptote, indicating that the diet composition may be higher by increase the sample. The species presented a broad niche breadth, however, no relationship between jaw width and prey size were found in the studied species. Despite the line-up in NMDS with Bray Curtis Index indicated that the species’ diets are similar with few different attributes, with some food items overlapping among species (Stress= 0.00201), the niche overlap between the pair of species was not high (Ojk < 0.7). Therefore, we believe interactions such as competition would be better demonstrated addressing data on prey availability and microhabitat use patterns. Key words: Trophic Niche; Overlapping; Similarity; Anurans. RESUMEN Las especies relacionadas filogenéticamente a menudo presentan similares en caracteres morfolociales y ecológicos, lo que puede llevarlos a competir cuando cuando ocurren en simpatría. En este sentido, analizamos la superposición de nicho trófico entre tres especies simpatríca del genero Leptodactylus (Leptodactylus macrosternum, L. fuscus y L. aff. podicipinus) en un entorno de planicie aluvial de una área protegida en la Amazonía brasileña. Además, aplicamos análisis de Network y Escalamiento multidimensional no métrico(NMDS). Encontramos 18 categorías de presas, la mayoría pertenecientes al orden de los artrópodos (94.4%). Coleoptera, Isoptera, Diptera e Hymenoptera fueron las presas más abundantes en la dieta compartida entre las tres especies. La curva de rarefacción de la riqueza de presas no alcanzó una asíntota, lo que indica que la composición de la dieta puede ser mayor al aumentar la muestra. Las especies presentaron una amplia amplitud de nicho, sin embargo, no se encontró relación entre el ancho de la mandíbula y el tamaño de la presa en las especies estudiadas. A pesar de que la alineación en NMDS con el Índice Bray Curtis indicó que las dietas de las especies son similares con pocos atributos diferentes y con algunos alimentos superpuestos entre especies (Estrés= 0.00201), la superposición de nicho entre el par de especies no fue alta (Ojk <0.7). Por lo tanto, creemos que las interacciones como la competencia se demostrarían mejor abordando los datos sobre la disponibilidad de presas y los patrones de uso de microhabitat. Palabras clave: Nicho trófico; Superposición; Similitud; Anuros.

Introduction Ecological studies on trophic niche allow to make characterizations about the structure and dynamic

of a population or community (Putman, 1994). This niche dimension includes, among other factors, the

Author for correspondence: patricksanchs@gmail.com

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R. R. Baia et al. - Diet overlap of sympatric Leptodactylus description of the diet composition and the use of food resource among the species (Schoener, 1974; Sih and Christensen, 2001). The way the species use the resources on environment strictly depends on intrinsic and extrinsic factors, such as foraging habits and nutritional demands, ontogenetic development, changes in resource availability and competition (Schoener, 1974; Putman, 1994). These factors affect the structure and coexistence patterns of communities and produces variation in the degree of overlap in resource use among species at a local scale (Schoener, 1974; Gordon, 2000). Also influences on the exchange of organisms and energy across ecosystem, affecting food web structure (Marczak et al., 2007; McDonald-Madden et al., 2016). Measures of niche overlap are useful to quantify the degree to which two or more species overlap in their utilization of resources, being applied in studies of species interactions and community structure (Hurlbert, 1978). However, the food webs are also a important representation of the interactions between species in an ecosystem (McDonald-Madden et al., 2016), which describe the trophic links between consumers, and can be a powerful tool not only in represent species interaction in a ecosystem but for the management of complex ecosystems in terms of conservation (May, 1974; Pimm et al., 1991). Evolutionary related species often share morphological characteristics and similar ecological functions, as a resulting of sharing a common ancestor, and expected to exhibit little niche differentiation (Losos, 2008). In this sense, resource competition and niche partitioning may occur in closely related species when they share the same spatial habitat (Violle et al., 2011; Schoener, 1974). Among amphibians, the anuran lineage is the most ecologically diverse (Duellman and Trueb, 1994). As predators of invertebrates, a rich taxonomic group, the anurans exhibit high diet plasticity and several degrees of specialization related to prey selection (Toft, 1980, 1995; Solé and Rödder, 2010); this makes them important test cases for studying mechanisms of diet segregation that facilitate species coexistence. The Leptodactylidae is one of the most widely distributed anuran families in the world and comprise 218 species occupying a wide range of environments (Frost, 2020). Leptodactylids species usually consume invertebrate prey (Rodrigues et al., 2004) but also can predate on anurans or other vertebrates (De-Sá et al., 2014). This study evaluates the diet composition and trophic niche overlap among three 176

sympatric Leptodactylus species, namely Leptodactylus aff. podicipinus, L. fuscus and L. macrosternum from in a protected area in northern Brazil. In addition, we provide a network analysis to better understand the interactions between species in this study. Materials and methods The Rio Curiaú Environmental Protection Area (hereafter APA Curiaú) is located north of the Municipality of Macapá, Amapá state, Brazil. It is established in the Curiaú river basin which covers 40% of the 21,700 hectares of the area’s extent. Vegetation is predominantly composed of várzeas forests, such as lowland marshes and swamps. APA Curiaú is composed of permanent and temporary lakes and foodplains, supporting a rich anuran community (Lima et al., 2017). The region’s climate is tropical monsoonal (Am from the Köppen Geiger system, see Peel et al., 2007) and the rainy season last from January to June (Silva et al., 2013). The study took place in two areas where the three target species occur in sympatry within APA Curiaú, Fazenda Toca da Raposa (00° 09' 00.7”; 051° 02' 18.5”) and Lago do Dezivaldo (00° 9' 12.4”; 51° 0' 53.9”), respectively Point 1 and Point 2 (Fig. 1). Both areas are characterized as floodplain environments dominated by typical floodplain vegetation, such as herbaceous and grasses, and surrounded by narrow bands of várzea forest composed of large and medium sized trees and shrubs (Lima et al., 2017). The campaigns were conducted between July 2013 and June 2014. We collected the specimens for two nights in a row in each campaign, always starting early night (19:00 h) and lasting until 23:00 h. Three people in each sampling point participated of the collections and the search effort corresponded to 12 person-hours per day in each sampling point. We located the target species by using auditory and visual search (Heyer et al., 1994) along all the floodplain and adjacent várzea forest. We placed the captured specimens inside individual plastic bags for identification and posterior examination of dietary aspects. We measured the snout-vent length (SVL) of specimens using a digital caliper (0.01 mm precision) and, body mass using a Pesola dynamometer (0.1g precision). We collected frogs under permit number #41586-1 issued by SISBIO/ICMBio and housed all specimens in the Herpetological Collection of Universidade Federal do Amapá (Appendix 1).

Cuad. herpetol. 34 (2): 175-184 (2020) For each prey category we applied the Importance Value Index (IVI) described by Gadsden and Palácios-Orona (1997) using the sum of the percentages of number (N%), frequency (F%) and volume (V%).

We measured trophic niche breadth of the three sympatric frog species using the Levins index (B) described by Pianka (1986). Where B = Levins index (trophic niche breadth); i= prey category; n = number of categories; pi = numerical or volumetric proportion of the category of prey i in the diet:

Figure 1. Rio Curiaú Environmental Protection Area, State of Amapá, Brazil, showing the two sampling points: Point 1 - Fazenda Toca da Raposa and Point 2 - Lake Dezivaldo.

We euthanized the collected frogs with cream anesthetic 2% Lidocaine (applying through the animal's skin), and fixed them in 10% formaldehyde for posterior preservation in alcohol at 70%.. Afterwards, we dissected the specimens and removed stomach contents through a ventral longitudinal incision and gathered carefully all contents into plastic tubes filled with 70% ethanol to interrupt continued digestion. The stomach contents were analyzed under stereo microscopes and identified to the lowest possible taxonomic level, with the aid of dichotomy keys (Borror and Delong, 2011; Rafael et al., 2012). Larval forms of insects were placed in different categories from the adults. Some noninsect invertebrates where difficult to identify in the level of order and, therefore, were placed into major taxonomic categories. For each food item, we measured the length and the width using digital calipers (0.01 mm precision) and prey volume (mm3) was estimated using the formula for ellipsoid bodies (Griffiths and Mylotte, 1987). Where V represents prey volume, l = item length e w = item width:

We calculated standardized measure of Levin’s index (Lst) which limits the value on a scale from 0 to 1 according to the formula (Hurlbert, 1978): Lst = (B - 1)/(n -1), where n represents the number of resources (prey categories) registered and B represents the Levin’s measure of niche breadth. Values closer to 0 we attributed to a more specialist diet, while values closer to 1 we considered a more generalist diet (Krebs, 1989). We used the absolute number of each prey item (N) to calculate the dietary overlap between L. aff. podicipinus, L. fuscus and L. macrosternum in the study area by applying Pianka’s index equation, in which the value ranges from 0 (no overlap) to 1 (complete overlap) (Pianka, 1973). The Pianka’s index was calculated using the following equation, where pij (or pik) is the absolute frequency of food item i in diet j (or k).

We performed a Spearman correlation test to determine the existence of correlation between jaw-width (JW) and the volume of the largest prey for each specimen. Statistical tests were performed using BioEstat 5.0 software (Ayres et al., 2007). Analyzes used to quantify the amplitude of the ecological niche and 177

R. R. Baia et al. - Diet overlap of sympatric Leptodactylus niche overlap of the species were carried out in the program Ecosim 7.0 (Gotelli and Entsminger, 2001). The network of associations were formed through the number of species collected in the two sampling areas and correlated with the number of prey consumed by the specimens. This analysis considers the prey predator relationship and was performed in the R (R core team 2017) statistical software, using the bipartite package that focuses on the definition of patterns in webs (Dormann et al., 2009). To analyze the sampling size and taxonomic richness of prey consumed by the three frog species we plotted rarefaction curves based on the number of specimens and food items using ESTIMATES 9.1 (Gotelli and Colwell, 2001). Non-metric multidimensional scaling (NMDS) with Bray-Curtis similarity distances were used to assess the similarity pattern between species using the abundance data for each species. In this analysis, we used the R statistical environment (R core team 2017) and the Vegan" library (Oksanen et al., 2017).

and larval forms of Diptera (13.03); other prey such as Coleoptera (IVI= 12.84) and Acari (IVI= 11.22) also were representative in the diet of the species. We identified six prey categories in the diet of L. macrosternum at sampling point 2, in which the most important prey categories were larval Lepidoptera (IVI= 24.31) and Chilopoda (IVI= 22.14). In terms of number, however, the most abundant prey in the diet of L. macrosternum were Coleoptera (28.57%) and Hymenoptera (21.43%) (Table 2). The niche breadth was slightly broader in sampling point 2 population (Lst= 0.84), than in sampling point 1 population (Lst= 0.76) and intermediate (Lst= 0.48) considering both sampling sites. There were no significant correlation between the highest volumetric prey and frog jaw width (JW) for L. macrosternum (rs= -0.0626, p= 0.7471). The diet composition of Leptodactylus fuscus consisted of only two prey categories at both sampling sites. Individuals primarily consumed Coleoptera, comprising 85.71% of the prey consumed at sampling point 1 and it was the only prey found in the stomachs of individuals at sampling point 2 (Table 3). Considering both populations, the niche of L. fuscus was broad (Lst= 0.74). As expected, no significant correlation between the highest volumetric prey and frog jaw width (JW) were found for L. fuscus (rs= -0.4524, p= 0.2603). With regards to prey richness in the diet of Leptodactylus aff. podicipinus, we found 11 prey categories. Individuals from sampling point 1 consumed primarily Coleopterans (IVI= 31.47), followed by Blattaria (IVI= 25.29) and Orthoptera (IVI=9.38). At sampling point 2 the diet of L. aff. podicipinus consisted of six prey categories and was dominated by Lepidoptera (IVI= 22.19), Orthoptera (IVI= 20.2) and Coleoptera (IVI= 19.96). Niche breadth was narrower in sampling point 1 (Lst= 0.52), broader in sampling point 2 (Lst= 0.91) and intermediate at both sampling sites (Lst= 0.66). We found no significant relationship between the highest volumetric prey and frog jaw width (JW) for L. aff. podicipinus (rs= 0.2508, p= 0.2266).

Results We collected 107 individuals from the three Leptodactylus species, the number of individuals collected in each sampling point are reported in Table 1. The contents found in the stomachs of Leptodactylus macrosternum, L. fuscus and L. aff. podicipinus from the two sites are reported, respectively, in Table 2, Table 3 and Table 4. All identifiable prey items were placed in 18 Orders, comprising terrestrial invertebrates most of them belonging to Arthropoda (94.4%) (Table 1). The rarefaction curve did not reach the asymptote and indicated the higher taxonomic richness in the diet of L. macrosternum (Fig. 2). We analyzed 53 stomachs from Leptodactylus macrosternum and found 16 prey categories. Diet of both populations was composed mostly of arthropods, including both larval and adult forms. At sampling point 1 the most important prey in the diet of L. macrosternum were Isoptera (IVI= 15.66)

Table 1. Species, total number of specimens collected (N), Number of species collected at Point 1 - Toca da Raposa farm and Point 2 - Dezivaldo Lake, total richness of prey consumed and of the two sampled points, and dominant prey category in anurans collected in Rio CuriaĂş Environmental Protection Area. Species

Point 1

Point 2

Richness of prey consumed

Dominant prey category

Leptodactylus macrosternum

Hymenoptera

Leptodactylus fuscus

Coleoptera

Leptodactylus aff. podicipinus

Coleoptera

178

Cuad. herpetol. 34 (2): 175-184 (2020) Table 2. Prey categories found in the stomachs of Leptodactylus macrosternum in two locates (Point 1 - Toca da Raposa farm and Point 2 - Dezivaldo Lake) at Rio Curiaú Environmental Protection Area. N = number of items consumed; F = frequency of items; V = prey volume (mm3); IVI = Index of Value Importance. Prey Category

Point 1

Point 2

IVI

Acari

27.17

6.45

0.17

0.02

11.22

Aranae

4.35

12.9

32.82

3.98

7.08

Blattaria

1.09

3.23

54.57

6.62

3.64

Coleoptera

10.87

22.58

41.82

5.07

12.84

28.57

157.72

8.87

20.81

Diptera

2.17

6.45

3.85

0.47

3.03

Diptera larvae

4.35

3.23

160.58

19.47

13.03

Haplotaxida

2.17

3.23

277.95

33.7

9.01

Hemiptera

1.09

3.23

184.03

22.31

8.87

Hymenoptera

7.61

22.58

19.01

2.3

10.83

21.43

11.57

0,65

15.69

Isoptera

36.96

9.68

2.88

0.35

15.66

Lepidoptera larvae

1.09

3.23

45.51

5.52

3.28

21.43

16.67

619.31

34.82

24.31

Neuroptera

1.09

3.23

1.62

0.2

1.5

Opilione

14.29

16.67

18.81

1.06

10.67

Orthoptera

7.14

8.33

65.08

3.66

6.38

Chilopoda

7.14

8.33

905.94

50.94

22.14

100

822.52

100

1778.43

100

Total

Table 3. Prey categories found in the stomachs of Leptodactylus fuscus in two locates (Point 1 - Toca da Raposa farm and Point 2 Dezivaldo Lake) at Rio Curiaú Environmental Protection Area. N = number of items consumed; F = frequency of items; V = prey volume (mm3); IVI = Index of Value Importance. Prey Category

Point 1 N

Point 2 V

IVI

100

1.19

100

1.19

100

Coleoptera

85.71

8.99

44.77

68.49

Hymenoptera

14.29

11.09

55.23

31.51

Total

100

20.08

100

Table 4. Prey categories found in the stomachs of Leptodactylus aff. podicipinus in two locaties (Point 1 - Toca da Raposa farm and Point 2 - Dezivaldo Lake) at Rio Curiaú Environmental Protection Area. N = number of items consumed; F = frequency of items; V = prey volume (mm3); IVI = Index of Value Importance. Prey Category Aranae

Point 1

Point 2

IVI

8.57

11.11

40.06

7.8

9.16

Blattaria

2.86

3.7

355.9

69.3

25.29

Coleoptera

48.57

44.44

7.09

1.38

31.47

28.57

2.06

2.75

19.96

Diptera

8.57

11.11

4.13

0.8

6.83

14.29

1.89

2.52

10.36

Haplotaxida

2.86

3.7

2.68

0.52

2.36

Hemiptera

8.57

11.11

13.92

2.71

7.46

Isoptera

11.43

3.7

2.61

0.51

5.21

Lepidoptera

14.92

14.29

28.47

37.99

22.19

Mantodea

14.92

16.21

21.63

16.73

Odonata

2.86

3.7

3.02

0.59

2.38

14.29

2.31

3.08

10.55

Orthoptera

5.71

7.41

84.14

16.38

9.38

14.29

32.02

20.2

Total

100

513.54

100

74.94

100

179

R. R. Baia et al. - Diet overlap of sympatric Leptodactylus Table 5. Trophic niche overlap between the three Leptodactylus species collected at Point 1 - Toca da Raposa and Point 2 - Lake Dezivaldo at Rio Curiaú Environmental Protection Area. Point 2

Point 1 L. macrosternum L. fuscus

L. fuscus

L. aff. podicipinus

L. fuscus

L. aff. podicipinus

0.49

0.52

0.48

0.35

0.64

When analyzing trophic niche overlap for pairs of species, we found the lowest overlap between L. macrosternum and L. aff. podicipinus at sampling point 2 (Ojk= 0.35) and the highest overlap between L. fuscus and L. aff. podicipinus at sampling point 1 (Ojk= 0.64). Overall, none of the species showed high overlap values to consider overlap in the use of resource (Ojk > 0.7) (Table 5). We found association of 14 prey categories in the diet of the three Leptodactylus species, showing Coleoptera, Isoptera, Diptera and Hymenoptera as the most abundant prey on the diet shared among the three species at sampling point 1, exhibiting more than one association in network analysis (Fig. 3A). At sampling point 2, we verified 11 prey categories with Coleoptera and Orthoptera showing more than one association between species, representing important items on the diet of the three frog species (Fig. 3B). The line-up in NMDS with Bray Curtis Index indicated that the species’ diets are similar with few different attributes, with some food items overlapping among species (Stress= 0.00201) (Fig. 4). Discussion We hypothesized that the three Leptodactylus species would consume the same types of prey given that morphological and ecological traits associated with feeding mechanisms are presumably similar in closely related species, driving species into resource competition and niche overlap. However, there is

Figure 2. Rarefaction curves of the three Leptodactylus species diet, relating taxonomic richness to the number of individuals sampled.

180

no strong evidence supporting high overlap among the food resources consumed by the three species at both sampling sites. On the other hand, the three species exhibited broad niche breadth, which can be indication of a generalist feeding habit and variation in the use of resources. It has been stated that populations with broader niche are likely to exhibit generalist behavior related to greater variation and diversification in the use of food resource among individuals in comparison to populations of specialist species with a narrower niches (Toft, 1980, 1995; Bolnick et al., 2007). This variation can be related to extrinsic factors, including shifts in resource availability and interspecific competition (Schoener, 1974; Sih and Christensen, 2001). An appreciation on studies about the diet of Leptodactylus species reveals a generalist and opportunistic feeding behavior pattern (e.g. Rodrigues et al., 2004; Sanabria et al., 2005; Solé et al, 2009). We suggest that the studied species, except for L. fuscus (due to the small sample found in the stomachs), exhibited a generalist behavior with a consumption of many different prey categories, with none of the food resources accounting more than 50% of the diet, which reflects in a broader niche breadth compared to specialists (Toft, 1980, 1995; Bolnick et al., 2007; Solé and Rödder, 2010). It would be expected a positive correlation between predator size and prey volume or prey length in Leptodactylus, given that this species usually feed on fewer but larger prey items (Rebouças and Solé, 2015). However, it contrasts with most studies on Leptodactylus species, which reported a lack of relationship between predator and prey size (Solé et al., 2018; Sanabria et al., 2005; Sugai et al., 2012; Teles et al., 2018). We believe lack of correlation between predator and prey size in our study, as well in other studies with Leptodactylus species, is probably related to the lack of juveniles in our sample and to the small sample obtained, which would consistently improve analysis. We observed through NMDS analysis, similarities between the items consumed by the studied species. These data indicate that relative high overlap

Cuad. herpetol. 34 (2): 175-184 (2020)

Figure 3. Network of interactions between prey and predators of Leptodactylus species for the two sampling points, (A) Point 1 - Toca da Raposa Farm and (B) Point 2 - Lake Dezivaldo in Rio CuriaĂş Environmental Protection Area.

181

R. R. Baia et al. - Diet overlap of sympatric Leptodactylus

Figure 4. Non-metric multidimensional scaling (NMDS) for Leptodactylus species according to food items at two sampling points: Point 1 - Toca da Raposa Farm and Point 2 - Lake Dezivaldo in a Rio Curiaú Environmental Protection Area. Sequence of food item codes: 1 - Coleoptera, 2 - Diptera, 3 - Hymenoptera, 4 - Lepidoptera, 5 - Lepidoptera immature, 6 - Mantodea, 7 - Odonata, 8 - Opilione, 9 - Orthoptera, 10 - Chilopoda, 11 - Acari, 12 - Araneae, 13 - Blattaria, 14 - Coleoptera, 15 - Diptera, 16 - Diptera immature, 17 - Haplotaxida, 18 - Hemiptera, 19 - Hymenoptera, 20 - Isoptera, 21 - Lepidoptera immature, 22 - Neuroptera, 23 - Odonata, 24 - Chilopoda.

between L. aff. podicipinus and L. fuscus at sampling point 1 may be related to the consumption of Coleoptera, which was the most important prey on the diet for both species (IVI = 68.49, 31.47; respectively). Although measures of niche breadth and niche overlap and other particular metrics are useful in studies estimating competition, the taxonomic level that the prey resources are identified has an important effect on the results obtained (Greene and Jaksić, 1983). A more refined taxonomic identification of prey items would probably give better results on niche measures, since anuran species are not only able to discriminate prey by size, but also taxonomically (Toft, 1980, 1995; Solé and Rödder, 2010). Altough phyllogenetic-based argument is relevant, there are several factors influencing resource sharing among sympatric anurans, including differences in size, prey availability (Sabagh et al., 2010), variation in feeding strategies (Toft, 1980; 1981) and different patterns of microhabitat use 182

(Van Sluys and Rocha, 1998). Also, the low degree of overlap observed between the three species may be an artifact of sample size of our study, as shown in the rarefaction curve the taxonomic prey richness is still underestimated, and more specimens sampled may reveal the presence of additional categories in the diet of the studied species. Furthermore, a more complex analysis, including availability of resources and microhabitat use patterns, would improve our conclusions about how these three frog species coexist in floodplain environment in Area de Proteção Ambiental Rio Curiaú, northern Brazil. Literature cited

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Trabajo

Herpetofauna of the Environmental Protection Area Delta do Parnaíba, Northeastern Brazil Kássio Castro Araújo1, Arthur Serejo Neves Ribeiro2, Etielle Barroso de Andrade3, Ocivana Araújo Pereira2, Anderson Guzzi2, Robson Waldemar Ávila1 Programa de Pós-Graduação em Ecologia e Recursos Naturais, Bloco 902, Centro de Ciências, Universidade Federal do Ceará – UFC, Campus do PICI, Av. Humberto Monte, s/n, 60455-760 Fortaleza, Ceará, Brasil. 2 Curso de Ciências Biológicas, Centro de Ciências do Mar, Universidade Federal do Piauí – UFPI, Campus Ministro Reis Veloso, Av. São Sebastião, 2819, Planalto Horizonte, 64202-020, Parnaíba, Piauí, Brasil. 3 Grupo de Pesquisa em Biodiversidade e Biotecnologia do Centro-Norte Piauiense – BIOTECPI, Instituto Federal de Educação, Ciência e Tecnologia do Piauí – IFPI, Campus Pedro II, Rua Antonino Martins de Andrade, 750, Engenho Novo, 64255-000, Pedro II, Piauí, Brasil. 1

Recibido:

Julio

2019

Revisado: 30 Enero 2020 Aceptado: 27 Julio 2020 Editor Asociado:

D. B a l d o

doi: 10.31017/CdH.2020.(2019-038)

ABSTRACT Recent studies on Brazilian coastal zones and restinga environments revealed a high richness of amphibian and reptile species. However, there is still a lack of information about herpetofauna diversity in coastal zones of Northeastern Brazil. This study provides a checklist of amphibians and reptiles inhabiting the Environmental Protection Area (EPA) Delta do Parnaíba, Northeastern Brazil, suggesting conservation actions. To elaborate the checklist, we searched in seven electronic databases and check the following scientific collections: Zoological collection of Universidade Federal do Piauí (UFPI) and Herpetological collection of Universidade Regional do Cariri (URCA). In addition, we sampled 16 areas along the EPA Delta do Parnaíba close to the river branches and temporary ponds that compose the Parnaíba River Delta (December 2015 to April 2017) to fill gaps of information about herpetofauna in some regions from the EPA. We recorded 86 species (34 amphibians and 52 reptiles), including four anurans, one crocodilian, 14 snakes, 12 lizards and two amphisbaenians reported for the first time for the EPA Delta do Parnaíba. In addition, we added the first record of the snake Oxybelis fulgidus in Piauí state. The EPA Delta do Parnaíba shows high herpetofaunal richness; thus, we suggest that conservation actions should be taken to preserve the restingas environments in the Parnaíba River Delta and its high diversity of amphibians and reptiles. Key words: Checklist; Amphibians; Reptiles; Parnaíba River Delta. RESUMO As áreas costeiras e ambientes de restinga têm sido bastante estudados nos últimos anos. Estes ambientes apresentam uma elevada riqueza de anfíbios e répteis, no entanto ainda existem lacunas de informações sobre a diversidade da herpetofauna nas áreas costeira da região Nordeste do Brasil. O presente estudo fornece uma lista dos anfíbios e répteis que ocorrem na Área de Proteção Ambiental (APA) Delta do Parnaíba, Nordeste do Brasil, e sugestões que auxiliem na conservação destas espécies na região. Para a elaboração da lista da herpetofauna do Delta do Parnaíba nós realizamos uma pesquisa bibliográfica em publicações científicas disponíveis em sete banco de dados eletrônicos, e consultamos os acervos das seguintes coleções científicas: Coleção Zoológica do Delta do Parnaíba, da Universidade Federal do Piauí (UFPI) e Coleção Herpetológica da Universidade Regional do Cariri (URCA). Adicionalmente, para preencher algumas lacunas sobre a herpetofauna da APA Delta do Parnaíba nós amostramos 16 áreas ao longo da APA próximas aos braços dos rios e lagoas temporárias que formam o Delta do Parnaíba (dezembro de 2015 e abril de 2017). Nós registramos 86 espécies (34 anfíbios e 52 répteis), sendo que quatro espécies de anfíbios anuros, um crocodilo, 14 espécies de serpentes, 12 lagartos e duas anfisbenas tiveram seus primeiros registros para a APA Delta do Parnaíba. Além disso, adicionamos o primeiro registro Oxybelis fulgidus para o estado do Piauí. A APA Delta do Parnaíba possui uma rica herpetofauna; portanto, sugerimos que ações de conservação sejam tomadas para preservar a restinga no delta do Rio Parnaíba e sua alta diversidade de anfíbios e répteis. Palavras-chave: Inventário; Anfíbios; Répteis; Delta do Rio Parnaíba.

Author for correspondence: kassio.ufpi@gmail.com

185

K. C. Araujo et al. - Herpetofauna of the Delta do Parnaíba Introduction Species inventories are crucial for decisions about natural environments management and conservation (Silveira et al., 2010). Faunal conservation is essential to biological and ecological stability and maintenance of biological diversity (Almeida, 1996). However, despite being considered one of the countries with the highest biodiversity worldwide (Lewinson and Prado, 2004), there is still a lack of information about Brazilian biodiversity and extensive areas remain understudied. There are 548 Conservation Units in Brazil, both federal and state Units (Brasil, 2020), and the establishment of these "Biodiversity Islands" has been an important tool for natural resources preservation and conservation in Brazil (Hassler, 2005). Historically, the biodiversity data generated for these conservation areas, mainly in the Caatinga domain, were based on inaccurate data (Leal et al., 2005), a situation that has only improved in the last decade with an increase of studies in the region (Camardelli and Napoli, 2012; Pedrosa et al., 2014; Benício et al., 2015; Calixto and Morato, 2017; Marinho et al., 2018; Campos et al., 2019); however, since these studies do not cover all Conservation Units, it is necessary to gather more data for a consistent ecological database. Therefore, it is important to elaborate adequate management strategies and plans that aimed the conservation of these environments and the species living there. Among the Brazilian Conservation Units, the Environmental Protected Area (EPA) Delta do Parnaíba had a considerable number of studies about local herpetofauna recently published, including amphibian checklists (Silva et al., 2007; Loebmann and Mai, 2008; Andrade et al., 2014; 2016), reptile distribution records (Loebmann et al., 2006; Batistella et al., 2008; Santana et al., 2009; Silva-Leite et al., 2009; 2010a; 2010b; Roberto et al., 2012), and ecological relationships (Araújo et al., 2018). However, there is still a lack of information about reptile species and undersampled areas in the EPA Delta do Parnaíba. The local fauna may reflect the conservation status from a given geographic region because some species have their important functions closely linked to environmental alterations. Therefore, these species are considered bioindicators of environment quality, being important to measure the conservation status of an area (Hodkinson and Jackson, 2005). Among 186

the vertebrates, both amphibians and reptiles are considered important environmental bioindicators (Pianka and Vitt, 2003; Toledo, 2009). Moreover, they are highly threatened (IUCN, 2020), and climate changes, habitat loss, and fragmentation are the main causes of declines and extinctions (Rodrigues, 2005; McCallum, 2007; Alroy, 2015; Andrade, 2015). Therefore, it is important to provide herpetofaunal checklists to evaluate the conservation status from a region and plan future actions that aimed to maintain biological diversity. In recent years, new amphibians and reptiles species were described in Brazil (e.g. Fernandes and Hamdan, 2014; Lourenço et al., 2014; Magalhães et al., 2014; Pansonato et al., 2014; Colli et al., 2015; Maciel et al., 2015; Carvalho et al., 2016; Franco et al., 2017). However, without carrying out exhaustive checklists and fieldworks, many Brazilian species could become extinct before scientists even have a chance to identify them. Thus, the present study provides an amphibian and reptile checklist from the Environmental Protection Area (EPA) Delta do Parnaíba, Northeastern Brazil. Material and methods Study area The Environmental Protection Area (EPA) Delta do Parnaíba was instituted from Federal Decree n° 99,274 on 06 June 1990 for preservation and conservation of natural water resources, fauna and flora from region. The EPA has approximately 3,138 km² encompassing the Brazilian municipalities of Ilha Grande, Parnaíba, Luís Correia and Cajueiro da Praia, in Piauí state; Araioses and Tutóia, in Maranhão state; Chaval and Barroquinha, in Ceará state (Brasil, 2002; Fig. 1). The EPA Delta do Parnaíba is located within a transitional area between Caatinga and Cerrado morphoclimatic domains (Ab’Saber, 1977). Despite mangrove forests being present in the Parnaíba River Delta (Brasil, 2006), the restinga is the predominant physiognomy, located on a quaternary environment, characterized by sandy soils with high salt concentrations and covered predominantly by herbaceous and shrubby xerophytic vegetation (Xavier et al., 2015). This physiognomy was labeled in three basic formations: grasses, shrub and arboreal, being the families Fabaceae, Poaceae, Cyperaceae, and Euphorbiaceae

Cuad. herpetol. 34 (2): 185-199 (2020) most abundant in the Piauí state coastal vegetation (see. Santos-Filho et al., 2010; 2015). Sampling The bibliographic reference searches to elaborate the herpetofaunal checklist from the EPA Delta do Parnaíba was carried out in scientific publications available from seven electronic databases (Google, Google Scholar, PubMed, Scielo, Science Direct, Scopus and Web of Science) using 18 keywords combined amongst itself in English and Portuguese (Alligators, Amphibians, Anurans, Ceará state, Coastal zone, Crocodiles, Gymnophiona, Lizards, Maranhão state, Parnaíba River Delta, Piauí state, Reptiles, Serpents, Snakes, Snakes blind, Squamata, Testudines and Turtles). Furthermore, the following scientific collections were consulted: Zoological collection of Universidade Federal do Piauí (UFPI) and Herpetological collection of Universidade Regional do Cariri (URCA). The data compilation of the collections and literature records occurred from February 2017 to March 2020. We also sampled 16 areas along the EPA Delta do Parnaíba located between the coordinates 2°49’15.39” S; 42°17’34.82” W (WGS84 datum and 26 m a.s.l) and 2°59’30.83” S; 41°11’34.48” W (WGS84 datum, 10 m a.s.l). Samples were carried out near river branches and temporary ponds that compose the Parnaíba River Delta (December 2015 to April 2017). The sampled areas are located in Tutóia and Araioses municipalities, Maranhão state; Ilha Grande, Parnaíba and Cajueiro da Praia, Piauí state; Chaval and Barroquinha, Ceará state (see Fig. 1). Herpetofaunal sampling occurred during the nocturnal period (06:00 p.m. to 00:00 a.m., sampling effort of approximately 1.248 hours/4 researchers) employing visual (Crump and Scott Junior, 1994) and auditory surveys (Zimmerman, 1994). The voucher specimens were deposited in the Zoological collection of Universidade Federal do Piauí (UFPI) and Herpetological collection of Universidade Regional do Cariri (URCA). The species nomenclature follows Frost (2020) and Costa and Bérnils (2018). Statistical analyzes Species distributions and associations with other Brazilian morphoclimatic domains (see Ab'Saber, 1977) were obtained from literature to amphibian records (see Bastazini et al., 2007; Ferrão et al., 2012; Valdujo et al., 2012; Dal Vechio et al., 2013; 2015; Roberto et al., 2013; Gondim-Silva et al., 2016;

Andrade et al., 2017; Freitas et al., 2017) and reptile records (see Bertoluci et al., 2009; Condez et al., 2009; Scartozzoni et al., 2009; Loebmann and Haddad, 2010; Recoder et al., 2011; Dal Vechio et al., 2013; 2015; Guedes et al., 2014; Freitas et al., 2016; 2017; Costa and Bérnils, 2018; Uetz et al., 2020). Species that occur in the four Brazilian morphoclimatic domains were considered of wide distribution. The herpetofaunal conservation status was obtained from IUCN (2020). We also search for herpetofaunal scientific publications performed in the Brazilian restingas in the above-cited electronic databases. This literature was used to compare the composition and species richness of the EPA Delta do Parnaíba with other studies performed along the Brazilian coastal zone. For amphibians, we used published databases from the states of Amapá (Araújo and Costa-Campos, 2014), Ceará (Borges-Leite et al., 2014; Roberto and Loebmann, 2016), Maranhão (Miranda, 2007), Bahia (Bastazini et al., 2007; Rocha et al., 2008; Gondim-Silva et al., 2016; Dantas et al., 2019), Espírito Santo (Rocha et al., 2008; Oliveira et al., 2020), Rio de Janeiro (Rocha et al., 2008; Silva et al., 2008; Telles et al., 2012; Carmo et al., 2019; Martins et al., 2019), São Paulo (Narvaes et al., 2009; Vilela et al., 2011; Zina et al., 2012), Santa Catarina (Pacheco, 2012; Wachlevski and Rocha, 2016; Argaez et al., 2017), and Rio Grande do Sul (Colombo et al., 2008; Quintela et al., 2009; Oliveira et al., 2013). For reptile, we used published databases from the states of Maranhão (Miranda et al., 2012), Ceará (Borges-Leite et al., 2014; Roberto and Loebmann, 2016), Rio Grande do Norte (Freire, 1996), Paraíba (Freire, 1996; Falcão, 2009; Sampaio et al., 2018), Bahia (Couto-Ferreira et al., 2011; Dias and Rocha, 2014; Travassos et al., 2015; Marques et al., 2016; 2017; Fazolato et al., 2019a, 2019b; Marques and Tinôco, 2019; Travassos et al., 2019a, 2019b), Espírito Santo (Silva-Soares et al., 2011; Rocha et al., 2014), Rio de Janeiro (Rocha et al., 2004; Carvalho et al., 2007; Lamonica, 2007; Rocha and Sluys, 2007; Martins et al., 2012; 2019), São Paulo (Marques and Sazima, 2004; Hartmann, 2005; Cicchi et al., 2009), Santa Catarina (Ghizoni-Junior et al., 2009; Kunz et al., 2011; Dacol, 2015; Argaez et al., 2017), and Rio Grande do Sul (Santos et al., 2012; Souza-Filho and Verrastro, 2012). Sea turtles recorded in the Parnaíba River Delta also occur along the Brazilian coast (Costa and Bérnils, 2018). Subsequently, we created a presence and ab187

K. C. Araujo et al. - Herpetofauna of the Delta do Parnaíba

Figure 1. Schematic map of the Environmental Protection Area Delta do Parnaíba (shaded area), Northeastern Brazil. Red triangles are the sampled areas while black circles are herpetofauna literature records.

sence species matrix to compare the amphibian and reptile species composition from the Parnaíba River Delta to the studies above cited. From the matrix, we performed a Cluster Analysis using the Jaccard similarity coefficient (Magurran, 1988; Krebs, 1999). The geographic distances among the restinga areas compared were measured using ArcGIS software (Esri, 2008) and their relationship with the sampled species richness from these studies was obtained using Mantel test (Manly, 1994). Statistical analyzes were performed on R software, using Vegan package (Oksanen et al., 2016). Results Amphibian species composition We recorded in the EPA Delta do Parnaíba 34 amphibian species (Table 1) belonging to 14 genera and seven families: Bufonidae (3 spp.), Hylidae (14 spp.), Leptodactylidae (11 spp.), Microhylidae (2 spp.), Phyllomedusidae (2 spp.), Odontophrynidae (1 sp.) and Typhlonectidae (1 sp.). 188

Regarding the amphibian species composition from the restingas of the Parnaíba River Delta and other herpetofaunal scientific publications performed in the Brazilian restingas environments, the states of Ceará (J’ = 0.625) and Maranhão (J’ = 0.501) was more similar to the Parnaíba River Delta, presenting 25 and 17 species in common, respectively. On the other hand, the restingas areas from São Paulo (J’= 0.015), Rio de Janeiro (J’ = 0.034), Santa Catarina (J’ = 0.048), and Rio Grande do Sul states (J’ = 0.050) were more distinct in relation to amphibian species composition (Fig. 2). No species was common to all restingas analyzed; however, nine species were recorded only in the restingas environments from the Northeastern states: Rhinella jimi, Boana raniceps, Scinax fuscomarginatus, S. x-signatus, Leptodactylus macrosternum, L. fuscus, L. troglodytes, Pleurodema diplolister and Pseudopaludicola mystacalis. Boana raniceps and L. macrosternum are also common to Amapá state, in North region. Conversely, S. alter and L. latrans were common to all the restingas environments

Cuad. herpetol. 34 (2): 185-199 (2020) Table 1. Amphibian species recorded in the EPA Delta do Parnaíba, with their voucher, IUCN status and the morphoclimatic domains of occurrence (MDO): Caatinga (CA), Cerrado (CE), Atlantic rain forest (AT), Amazon rain forest (AM) domains and wide distribution (WD). The localities in the Parnaíba River Delta where the species were recorded: Maranhão state (Araioses - 1, Tutoia - 2), Piauí state (Ilha Grande - 3, Parnaíba - 4, Cajueiro da Praia - 5) and Ceará state (Barroquinha - 6, Chaval - 7). The new species records to the Parnaíba River Delta (*). Taxon

Voucher

IUCN status

MDO

Localities

Rhinella granulosa (Spix, 1824)

CZDP (I1) 0101

CA, AT

1, 3, 4, 5, 6, 7

Rhinella jimi (Stevaux, 2002)

CZDP (I1) 0337

CA, AT

1, 2, 3, 4, 5, 6, 7

Rhinella mirandaribeiroi (Gallardo, 1965)

CZDP (I1) 0281

1, 3, 4, 5

Order Anura Bufonidae

Hylidae Boana crepitans (Wied-Neuwied, 1824)

CHDP-0585

Boana punctata (Schneider, 1799)

CZDP (I1) 0095

4, 5

Boana raniceps (Cope, 1862)

CZDP (I1) 0484

1, 2, 3, 4, 7

Dendropsophus minusculus (Rivero, 1971)

CZDP (I1) 0478

1, 2, 3, 4

UFPB 4519

4, 5

CZDP (I1) 0463

1, 3, 4, 5, 7

Dendropsophus rubicundulus* (Reinhardt & Lütken, 1862)

URCA-H12132

CA, CE

Dendropsophus soaresi* (Caramaschi & Jim, 1983)

CZDP (I1) 0634

CA, CE, AT

1, 5, 6, 7

Scinax fuscomarginatus (Lutz, 1925)

CZDP (I1) 0026

1, 3, 4

Scinax fuscovarius (Lutz, 1925)

CHDP 0456

1, 3, 6

Scinax nebulosus (Spix, 1824)

UFPB 4533

3, 4

Scinax gr. ruber (Laurenti, 1768)

CZDP (I1) 0637

1, 3, 4, 5, 6

Scinax x-signatus (Spix, 1824)

CZDP (I1) 0466

1, 2, 3, 4, 5, 6, 7

UFPB 4530

4, 5

Adenomera cf. hylaedactyla (Cope, 1868)

CZDP (I1) 0479

AM, CE, AT

1, 2, 3, 4, 7

Leptodactylus macrosternum Miranda-Ribeiro, 1926

CZDP (I1) 0032

1, 2, 3, 4, 5, 6, 7

Leptodactylus fuscus (Schneider, 1799)

CZDP (I1) 0009

1, 2, 3, 4, 5, 6, 7

Leptodactylus natalenses Lutz, 1930

CZDP (I1) 0021

CA, AT

1, 3, 4, 5

Leptodactylus vastus Lutz, 1930

CZDP (I1) 0452

CA, CE, AT

1, 2, 3, 4, 5, 6, 7

Leptodactylus pustulatus (Peters, 1870)

CZDP (I1) 0471

1, 3, 4, 5

Leptodactylus troglodytes Lutz, 1926

CZDP (I1) 0076

1, 2, 3, 4, 5, 6, 7

Physalaemus albifrons (Spix, 1824)

CZDP (I1) 0519

CA, CE, AT

1, 2, 3, 4, 5, 6, 7

Physalaemus cuvieri Fitzinger, 1826

CZDP (I1) 0497

1, 2, 3, 4, 5, 6, 7

Pleurodema diplolister (Peters, 1870)

CZDP (I1) 0012

CA, CE, AT

1, 2, 3, 4, 5, 6, 7

Pseudopaludicola mystacalis (Cope, 1887)

CZDP (I1) 0474

1, 2, 3, 4, 5, 6, 7

Dermatonotus muelleri* (Boettger, 1885)

CZDP (I1) 0641

1, 4, 5

Elachistocleis piauiensis Caramaschi & Jim, 1983

CZDP (I1) 0498

CA, CE

1, 3, 4, 5, 6, 7

CZDP (I1) 0642

1, 3, 4, 5, 6

Pithecopus azureus* (Cope, 1862)

CZDP (I1) 0676

1, 2

Pithecopus nordestinus (Caramaschi, 2006)

CZDP (I1) 0477

CA, CE, AT

3, 4, 5

Dendropsophus minutus (Peters, 1872) Dendropsophus nanus (Boulenger, 1889)

Trachycephalus typhonius (Linnaeus, 1758) Leptodactylidae

Microhylidae

Odontophrynidae Proceratophrys cristiceps (Müller, 1883) Phyllomedusidae

Order Gymnophiona

189

K. C. Araujo et al. - Herpetofauna of the Delta do Parnaíba Typhlonectidae Chthonerpeton tremembe Maciel, Leite, Silva-Leite, Leite & Cascon, 2015

from the Southeastern and Southern states analyzed. Corroborating these differences, we observed that the dissimilarity in amphibian composition increases with geographic distance (r = 0.809, p-value < 0.005, Fig. 3A). Reptile species composition We recorded 52 reptile species (Table 2) belonging to three orders: Crocodylia (two species), Squamata (42 species) and Testudines (seven species). For Crocodylia order, we registered two Alligatoridae species belonging to two genera. Among Squamata, we recognize 41 species (37 genera) belonging to the following families: Amphisbaenidae (2 spp.), Boidae (4 spp.), Colubridae (8 spp.), Dipsadidae (14 spp.), Elapidae (1 sp.), Gekkonidae (2 spp.), Gymnophthalmidae (1 sp.), Iguanidae (1 sp.), Mabuyidae (1 sp.), Sphaerodactylidae (1 sp.), Teiidae (5 spp.), Tropiduridae (2 spp.), and Viperidae (1 sp.). Testudines has seven species belonging to seven genera and three families: Chelidae (1 sp.), Cheloniidae (5 spp.), and Emydidae (1 sp.). Reptile composition from states of Maranhão (J = 0.557) and Ceará (J = 0.537) was more similar

Figure 2. Amphibian composition similarity and distance found in the EPA Delta do Parnaíba (DP) and other coastal zones and restingas environments from the states of Amapá (AP), Ceará (CE), Maranhão (MA) Bahia (BA), Espirito Santo (ES), Rio de Janeiro (RJ), São Paulo (SP), Santa Catarina (SC), and Rio Grande do Sul (RS). Cophenetic correlation coefficient (r = 0.915).

190

MPEG 35526

to the Parnaíba River Delta, presenting 34 and 43 species in common, respectively. On the other hand, the restingas areas from Santa Catarina (J = 0.103), São Paulo (J’= 0.106), and Rio Grande do Sul (J’ = 0.137) were more distinct in relation to reptile species composition, respectively (Fig. 4). Despite the high reptile diversity along the Brazilian restinga environments, only the Cheloniidae species and the lizard Hemidactylus mabouia was common to all coastal environments analyzed above-cited. The lizard species Ameivula ocellifera and Tropidurus hispidus were common to Nor-

Figure 3. Mantel test between amphibians (A) and reptiles (B) richness dissimilarity and geographic distance.

Cuad. herpetol. 34 (2): 185-199 (2020) Table 2. Reptiles species recorded in the EPA Delta do Parnaíba, with their voucher, IUCN status and the morphoclimatic domains of occurrence (MDO): Caatinga (CA), Cerrado (CE), Atlantic rain forest (AT), Amazon rain forest (AM) domains and wide distribution (WD). The localities in the Parnaíba River Delta where the species were recorded: Maranhão state (Araioses - 1, Tutoia - 2), Piauí state (Ilha Grande - 3, Parnaíba - 4, Cajueiro da Praia - 5) and Ceará state (Barroquinha - 6, Chaval – 7). The new species records to the Parnaíba River Delta (*). Taxon

Voucher

IUCN status

MDO

Localities

INPA- H 16020

4, 5

Caretta caretta (Linnaeus, 1758)

CZDP (J1) 0002

3, 4, 5

Chelonia mydas (Linnaeus, 1758)

CZDP (J1) 0005

3, 4, 5

Dermochelys coriacea (Vandelli, 1761)

CZDP (J1) 0001

3, 4, 5

Eretmochelys imbricata (Linnaeus, 1766)

CZDP (J1) 0003

3, 4, 5

Lepidochelys olivacea (Eschscholtz, 1829)

CZDP (J1) 0007

3, 4, 5

Personal observation

1, 3, 4, 5

CZDP (J4) 0001

1, 3, 4

Personal observation

1, 3, 4

Amphisbaena alba* Linnaeus, 1758

CZDP (J5) 0006

3, 4

Amphisbaena vermicularis* Wagler, 1824

CZDP (J5) 0005

3, 4

Boa constrictor Linnaeus, 1758

CZDP (J2) 0049

3, 4, 5

Corallus hortulana (Linnaeus, 1758)

CZDP (J2) 0004

3, 4, 5

Epicrates assisi Machado, 1945

CZDP (J2) 0041

CA, CE

Eunectes murinus (Linnaeus, 1758)

CZDP (J2) 0115

3, 4, 5

Chironius carinatus (Linnaeus, 1758)

CZDP (J2) 0072

1, 3, 4, 5

Chironius flavolineatus* Jan, 1863

CZDP (J2) 0047

Drymarchon corais* (Boie, 1827)

CZDP (J2) 0038

Leptophis ahaetulla* (Linnaeus, 1758)

CZDP (J2) 0034

1, 3

Oxybelis aeneus* (Wagler, 1824)

CZDP (J2) 0028

1, 3, 4

Oxybelis fulgidus* (Daudin, 1803)

CZDP (J2) 0078

AM, CA, CE

Spilotes pullatus* (Linnaeus, 1758)

CZDP (J2) 0085

1, 3, 4

Tantilla melanocephala* (Linnaeus, 1758)

CZDP (J2) 0058

Apostolepis cearensis Gomes, 1915

CZDP (J2) 0055

CA, AT

Boiruna sertaneja* Zaher, 1996

CZDP (J2) 0162

CA, CE

Erythrolamprus poecilogyrus (Wied-Neuwied, 1825)

CZDP (J2) 0023

1, 3, 4

Helicops leopardinus (Schlegel, 1837)

CZDP (J2) 0167

3, 4, 5, 6, 7

Hydrodynastes gigas (Duméril, Bibron & Duméril, 1854)

CZDP (J2) 0077

3, 4, 5

Leptodeira annulata* (Linnaeus, 1758)

CZDP (J2) 0123

3, 4

Lygophis paucidens* Hoge, 1953

CZDP (J2) 0075

CA, CE

Order Testudines Chelidae Mesoclemmys tuberculata (Luederwaldt, 1926) Cheloniidae

Emydidae Trachemys adiutrix Vanzolini, 1995 Order Crocodylia Alligatoridae Caiman crocodilus (Linnaeus, 1758) Paleosuchus palpebrosus* (Cuvier, 1807) Order Squamata Amphisbaenidae

Boidae

Colubridae

Dipsadidae

191

K. C. Araujo et al. - Herpetofauna of the Delta do Parnaíba Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854

CZDP (J2) 0030

CA, CE, AT

3, 4

Philodryas nattereri* Steindachner, 1870

CZDP (J2) 0037

CA, CE

1, 3, 4

Philodryas olfersii* (Lichtenstein, 1823)

CZDP (J2) 0039

CA, CE, AT

3, 4

Pseudoboa nigra* (Duméril, Bibron & Duméril, 1854)

CZDP (J2) 0163

CA, CE, AT

1, 3

Psomophis joberti* (Sauvage, 1884)

CZDP (J2) 0045

1, 3, 4

Thamnodynastes hypoconia (Cope, 1860)

CZDP (J2) 0089

CA, CE, AT

3, 4, 5

Xenodon merremii (Wagler, 1824)

CZDP (J2) 0087

3, 4

CZDP (J2) 0044

CA, AT

3, 4

CZDP (J2) 0035

1, 3, 4, 5

Hemidactylus agrius* Vanzolini, 1978

CZDP (J3) 0033

CA, CE

3, 4

Hemidactylus. mabouia* (Moreau de Jonnès, 1818)

CZDP (J3) 0031

1, 2, 3, 4, 5, 6, 7

CZDP (J3) 0030

3, 4, 5

CZDP (J3) 0001

1, 2, 3, 4, 5, 6, 7

CZDP (J3) 0016

CA, CE, AT

3, 4, 5

CZDP (J3) 0027

CA, CE, AT

3, 4

Ameiva ameiva* (Linnaeus, 1758)

CZDP (J3) 0022

3, 4

Ameivula ocellifera* (Spix, 1825)

CZDP (J3) 0024

3, 4

Kentropyx calcarata Spix, 1825

CHUFC L4236

2, 3

Elapidae Micrurus ibiboboca (Merrem, 1820) Viperidae Bothrops gr. atrox (Linnaeus, 1758) Gekkonidae

Gymnophthalmidae Vanzosaura multiscutata* (Amaral, 1933) Iguanidae Iguana iguana* (Linnaeus, 1758) Mabuyidae Brasiliscincus heathi* (Schmidt & Inger, 1951) Sphaerodactylidae Coleodactylus meridionalis* (Boulenger, 1888) Teiidae

Tropiduridae Tropidurus hispidus* (Spix, 1825)

CZDP (J3) 0028

1, 2, 3, 4, 5, 6, 7

Personal observation

CA, AT

4, 5, 7

Salvator merianae* Duméril & Bibron, 1839

CZDP (J3) 0023

3, 4

Tupinambis teguixin* (Linnaeus, 1758)

CZDP (J3) 0015

3, 4

Tropidurus semitaeniatus* (Spix, 1825) Tupinambinae

theastern restingas environments, while the species Bothrops jararaca was common to Southeastern and Southern restinga areas. In addition, 25 reptile species occurs in both restingas of the Parnaíba River Delta, Maranhão, Ceará, and Bahia, reinforcing the hypothesis that the species composition of distant regions tends to be more dissimilar (r = 0.7389, pvalue < 0.001, Fig. 3B). Discussion Amphibian species composition The Brazilian restingas presented high amphibian diversity (Oliveira and Rocha, 2015), with about 192

170 species occurring in these environments and approximately 20% of them were recorded in the present study. The amphibian richness recorded in the Parnaíba River Delta was similar to other local studies undertaken in the restingas of Conde and Mata de São João municipalities, both in Bahia state (Bastazini et al., 2007; Gondim-Silva et al., 2016), and it was higher than other local studies realized in restingas environments from the states of Amapá and Rio de Janeiro (Telles et al., 2012; Araújo and Costa-Campos, 2014). Also, the restingas areas from the states of Bahia and Rio de Janeiro present highest amphibian richness with 71 and 55 species, respectively (see Bastazini et al., 2007; Rocha et al.,

Cuad. herpetol. 34 (2): 185-199 (2020)

Figura 3. Reptile composition similarity and distance found in the EPA Delta do Parnaíba (DP) and other coastal zones and restingas environments from the states of Ceará (CE), Maranhão (MA), Rio Grande do Norte (RN), Paraíba (PB), Bahia (BA), Espirito Santo (ES), Rio de Janeiro (RJ), São Paulo (SP), Santa Catarina (SC), and Rio Grande do Sul (RS). Cophenetic correlation coefficient (r = 0.914).

2008; Silva et al., 2008; Telles et al., 2012; GondimSilva et al., 2016; Carmo et al., 2019; Martins et al., 2019; Dantas et al., 2019). According to the Neutral Biodiversity Theory, species diversity in a given locality could be explained by the functional and competitive equivalence among species (Hubbell, 2001). In addition, this theory predicts the influence of geographic distance on the similarity patterns of species richness of assemblages (Hubbell, 2006). Thus, geographically closer areas tend to be more similar in species composition. This relationship was noted by presence of 10 amphibian species common to Northeastern states. Despite all sampling localities being in the restinga environments, amphibian composition similarity of Northeastern coastal zones may have been influenced by the presence of typical species from the Caatinga and Cerrado domains, whereas in Southeastern and Southern regions by typical species from the Atlantic rain forest. We also registered four new anuran records for the EPA Delta do Parnaíba, confirming Loebmann and Mai (2008) affirmation that Dendropsophus soaresi and Dermatonotus muelleri could occur in the EPA Delta do Parnaíba. Both species were recorded in Cajueiro da Praia municipality, Piauí state. We present the first record of Dendropsophus rubicundulus to Chaval municipality, Ceará state.

This species was recorded in close localities in Ceará state (Silva et al., 2011); however, it has not been previously registered in the EPA Delta do Parnaíba. We recorded the first occurrence of Pithecopus azureus for Tutóia municipality, Maranhão state, increasing the species geographic distribution about 900 km north from Ribeiro Gonçalves municipality, Piauí state (Roberto et al., 2013) and about 600 km north from Parque Estadual do Mirador, Maranhão state (Andrade et al., 2017). Furthermore, we report that Corythomantis greeningi is possibly absent in the Parnaíba River Delta, although has been listed in the Biodiversidade do litoral do Piauí guide (Mai and Loebmann, 2010). This species was recorded outside of the EPA Delta do Parnaíba in distinct environments from our study area. Most species found has wide distribution along the Brazilian morphoclimatic domains (47.1%, 17 species), being Rhinella mirandaribeiroi and Leptodactylus pustulatus endemic to Cerrado domain and transitional zones, while Proceratophrys cristiceps and Chthonerpeton tremembe are endemic to Caatinga domain and transitional zones. It is also noteworthy that C. tremembe is endemic to the Parnaíba River Delta (Maciel et al., 2015) and the treefrog Scinax sp. (gr. ruber) could represent a new species. Overall, the majority of species are classified as Least Concern by IUCN (2020). Species described recently do not contain sufficient data to evaluate their conservation status (Table 1). Reptile species composition Brazil has the third richest reptile fauna in the world, with 795 species (Costa and Bérnils, 2018), and about 218 species occur in restingas environments, being about 24% of these registered in the Parnaíba River Delta. The reptile richness recorded in the Parnaíba River Delta was similar to other studies in Brazilian restingas, except those from Bahia (CoutoFerreira et al., 2011; Dias and Rocha, 2014; Travassos et al., 2015; Marques et al., 2016; 2017; Fazolato et al., 2019a, 2019b; Marques and Tinôco, 2019; Travassos et al., 2019a, 2019b) and Ceará states (Borges-Leite et al., 2014; Roberto and Loebmann, 2016), which present 115 and 71 species, respectively. Likewise, we observed nine reptile species common to Northeastern restingas environments. Considering the Northeastern restingas which are not influenced by typical species from the Atlantic Rain Forest, we observed 27 reptile species common to restingas from the states of Maranhão, Piauí, and 193

K. C. Araujo et al. - Herpetofauna of the Delta do Parnaíba Ceará, being 15 snakes, five lizards, five sea turtles, one crocodile, and one amphisbaenian. Therefore, the reptile composition similarity may be due to presence of typical species from the Caatinga and Cerrado domains, whereas in Southeastern and Southern regions by typical species from the Atlantic Rain Forest. Until now, the knowledge about the Parnaíba River Delta reptiles was based on a succinct field guide (Mai and Loebmann, 2010) and scattered notes on geographic distribution and ecological aspects (e.g. Santana et al., 2009, Silva and Henderson, 2010; Silva-Leite et al., 2009; 2010a; 2010b, Roberto et al., 2012; Silva et al., 2012). Therefore, our list adds 14 snakes, 12 lizards, two amphisbaenians and one crocodylian to the EPA Delta do Parnaíba (see Table 2). Furthermore, we report the first record of Oxybelis fulgidus to Piauí state. This species has a wide distribution along the Amazon Forest and Cerrado domains. We increased this species geographic distribution about 170 km eastern of closest locality in the Maranhão state (Scartozzoni et al., 2009; Costa and Bérnils, 2018). We also present the second record of Tupinambis teguixin for Piauí state, extending its distribution in approximately 190 km north from the nearest previously known record in the municipality of Barras, Piauí (Benício and Fonseca, 2014). Considering the reptile distribution most of them also have wide distribution along the Brazilian morphoclimatic domains (65.3%, 34 species), being Bothrops gr. atrox, Vanzosaura multiscutata, and Trachemys adiutrix endemic to Caatinga domain and transitional zones, the last one restricted to states of Maranhão and Piauí (Ernst et al., 2010). Other eight species were endemic to at least two morphoclimatic domain and transitional zones. Except for Mesoclemmys tuberculata, all Testudines registered in the present study are considered endangered species, being three Cheloniidae species classified as vulnerable to extinction (Caretta caretta, Dermochelys coriacea, and Lepidochelys olivacea), two as endangered (Chelonia mydas and Trachemys adiutrix), and one as critically endangered (Eretmochelys imbricata). Conversely, the Squamata species are classified as least concern or do not contain sufficient data to evaluate their conservation status (IUCN, 2020; Table 2). Therefore, herpetofaunal inventories might improve the species distribution knowledge and, consequently help to create preservation measures for these species. 194

The importance of restinga fragments conservation The intrinsic characteristics of the restingas fragments as temperature, humid, salinity, and vegetation makes these environments isolated microecosystems with a particular biodiversity driven by invasion, extinction, and competition process; thus, more studies are necessary for better comprehension of its dynamics (Rocha and Van Sluys, 2007). These microecosystems harbors high herpetofaunal diversity along the Brazilian restinga environments (Rocha and Bergallo, 1997; Rocha and Van Sluys, 2007; Bastazini et al., 2007; Araújo et al., 2018), including some anuran endemism as Leptodactylus marambaiae and Xenohyla truncata restricted to the restingas of Rio de Janeiro state (Carvalho-e-Silva et al., 2000; Frost, 2020), and also reptiles endemism as Amphisbaena nigricauda and Liolaemus occipitalis endemics to Southern and Southeastern Brazilian restingas, respectively (Rocha and Van Sluys, 2007). Regarding the Northeastern Brazilian restingas, the lizards Glaucomastyx itabaianensis and G. abaetensis, the turtle Trachemys adiutrix, and the amphibian Chthonerpeton tremembe are relevant endemism cases in these environments (Rocha and Van Sluys, 2007; Ernst et al., 2010; Maciel et al., 2015; Rosário et al., 2019). Therefore, the restinga fragments may be considered endemism areas or even so hotspots of herpetofaunal diversity (Silva et al., 2018). Overall, it is important to preserve the restinga fragments due to their high habitat diversity and the biological factors that make these ecosystems so complex (Araujo and Lacerda, 1987). Furthermore, these environments also are susceptible to degradation, given the high human occupation in coastal plains (Marques et al., 2015); thus, biodiversity studies might help the preservation and conservation of these coastal zones. Concluding remarks The Parnaíba River Delta has a mosaic of distinct physiognomies (Santos-Filho et al., 2010), and restinga environments harbors high richness of herpetofauna and great environmental heterogeneity (Araújo et al., 2018). However, these restingas areas have been deforested by intensive anthropic actions, such as, fires, agriculture, housing activities and windfarms. Thus, we suggest that conservation actions should be taken to preserve the restingas environments of the Parnaíba River Delta and its high diversity of amphibians and reptiles.

Cuad. herpetol. 34 (2): 185-199 (2020) Acknowledgements We are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq for the research grant awarded to R.W.A (PQ#303622/20156; 305988/2018-2); To CNPq/FUNCAP/CAPES for partial financial support (PROTAX-Processes 440511/2015-1; 5574685/2017; 88882.156872/201601). ICMBio for the collection permit (29613); and Thiago S. Nascimento, Tássia G. P. Lima, Emanuel C. Barbosa and Antonio G. S for their assistance during fieldwork. We are grateful to the searchers Roberta R. S. Leite, Thiago S. Nascimento and Pedro C. Silva for collecting the most of reptile species deposited in the zoological collection of Universidade Federal do Piauí (UFPI). Literature cited

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Serpentes de uma área de proteção urbana da Floresta Atlântica nordestina brasileira Vanessa do Nascimento Barbosa¹, Jéssica Monique da Silva Amaral¹, Reginaldo Augusto Farias de Gusmão², Luiz Filipe Lira Lima³, José Víctor de Melo Souza³, Ivyson Diogo Silva Aguiar4, Ednilza Maranhão dos Santos³ ¹ Programa de Pós-Graduação em Ecologia e Monitoramento Ambiental, Universidade Federal da Paraíba, Av. Santa Elizabete, 160, Centro, Rio Tinto, Paraíba, Brasil. ² Laboratório de Síntese Ecológica e Conservação da Biodiversidade. Pós-Graduação em Etnobiologia e Conservação da Natureza. Universidade Federal Rural de Pernambuco, Rua Manuel de Medeiros, s/n, Dois Irmãos, Recife, Pernambuco, Brasil. ³ Laboratório Interdisciplinar de Anfíbios e Répteis, Universidade Federal Rural de Pernambuco, Rua Manuel de Medeiros, s/n, Dois Irmãos, Recife, Pernambuco, Brasil. 4 Fundação de Ensino Superior de Olinda; Parque Estadual de Dois Irmãos, Praça Farias Neves, s/n - Dois Irmãos, Recife, Pernambuco, Brasil. Recibido: 23 Enero 2020 Revisado: 16 Junio 2020 Aceptado: 14 Julio 2020 Editor Asociado: A. Prudente doi: 10.31017/CdH.2020.(2020-003)

ABSTRACT Snakes in an urban Protected Area in the Atlantic forest in Northeast, Brazil. The available information on snake taxocenosis in Northeast Brazil is still incipient. To contribute to filling this gap, this study describes the composition of snake species from an Atlantic Forest Protected Area, Dois Irmãos State Park - PEDI, in Pernambuco. Data were collected using the methods: (1) occasional encounters, (2) active search, (3) interception and pitfalls, performed bimonthly for three years. 117 snakes were registered, distributed in five families, 21 genera, 23 species. Xenodon rabdocephalus species had its geographical distribution expanded by 742.2 km from the nearest registered location. The first order Jackknife index estimated a richness of 30 species and the rarefaction curve did not reach asymptote, indicating that there are still species to be found in the study area. The registration of rare and endemic species indicates the good quality of the area, but have highlighted a warning about the warns of the anthropic pressure suffered by PEDI, putting at risk the conservation of its fauna and flora. Key words: Ecology; Inventory; Reptiles; Taxocenosis. RESUMO As informações disponíveis sobre taxocenoses de serpentes no Nordeste do Brasil ainda são incipientes. Para contribuir com o preenchimento desta lacuna, o presente estudo descreve a composição de espécies de serpentes de uma Unidade de Conservação de Mata Atlântica, Parque Estadual Dois Irmãos – PEDI, em Pernambuco. Os dados foram coletados através dos métodos: (1) encontros ocasionais, (2) busca ativa e (3) armadilhas de interceptação e queda, realizados bimestralmente durante três anos. Foram registradas 117 serpentes distribuídas em cinco famílias, 21 gêneros, 23 espécies. A espécie Xenodon rabdocephalus teve sua distribuição geográfica ampliada 742,2 Km da localidade mais próxima registrada. O índice Jackknife de primeira ordem estimou uma riqueza de 30 espécies e a curva de rarefação não atingiu a assíntota, indicando que ainda há espécies a serem encontradas na área de estudo. O registro de espécies raras e endêmicas indica a boa qualidade da área, mas evidenciamos um alerta sobre a pressão antrópica sofrida pelo PEDI, colocando em risco a conservação de sua fauna e flora. Palavras-chave: Ecologia; Inventário; Répteis; Taxocenose.

Introdução A Mata Atlântica é um dos Hotspots mundiais de biodiversidade sendo uma das mais importantes florestas tropicais do mundo (Rodrigues, 2005; SOS Mata Atlântica, 2016). A taxocenose de serpentes desse Bioma é composta por cerca de 190 espécies (Tozetti et al., 2018), o que corresponde a 54% do

total de espécies brasileiras (Costa e Bérnils, 2018). Em sua maioria, as espécies encontradas na Mata Atlântica do Brasil apresentam distribuição cosmopolita, sendo registradas em outros Biomas do país (Guedes et al., 2014; Marques et al., 2015; Marques et al., 2017). Cerca de 28% são endêmicas da Mata

Autor para correspondência: jessica_monique.amaral@hotmail.com

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V. N. Barbosa et al. - Serpentes de uma UC, Nordeste brasileiro Atlântica com 10 espécies encontradas unicamente na porção nordestina (Tozetti et al., 2018). Apesar disto, os estudos sobre as comunidades de serpentes na Mata Atlântica não estão distribuídos de forma homogênea no território brasileiro, existindo lacunas de conhecimento principalmente nas regiões Nordeste e Sul (Condez et al., 2009). Assim, estas regiões podem apresentar um número maior de espécies endêmicas que ainda não foram registradas. Há registros de espécies endêmicas de serpentes em diversos fragmentos urbanos de Mata Atlântica no Nordeste brasileiro (Passos et al., 2010; Nascimento e Santos, 2016; Pereira-Filho et al., 2017). Estes fragmentos urbanos estão sob intensa ação antrópica devido à comunidade aos arredores o utilizarem para extração de madeira, ervas, caça, agricultura e expansão urbana (Navega-Gonçalves e Porto, 2016). Além disso, normalmente há um sentimento de repúdio das serpentes pelas comunidades locais, aumentando a taxa de mortalidade e extinção local neste grupo (Fernandes-Ferreira et al., 2011; Fraga et al., 2013). Desta forma, é evidente a importância das estratégias de conservação e de melhor compreender comunidades de serpentes existentes nos fragmentos urbanos (França et al., 2012). Levando isto em consideração, este trabalho descreve algumas das características (uso do hábitat, composição, abundância e riqueza estimada de espécies) da comunidade de serpentes de uma área de proteção de Mata Atlântica (Parque Estadual de Dois Irmãos), localizada em meio a uma matriz urbana.

rentes estágios sucessionais: uma área denominada de Mata de Dois Irmãos (384,7 ha), onde está localizado o zoológico, constituída por uma floresta primária em estágio de regeneração avançado com idade de pelo menos 80 anos, e uma outra área de floresta secundária com regeneração tardia ou inicial com idade entre 30 e 46 anos, denominada de Fazenda Brejo dos Macacos (773,02 ha) (SEMAS, 2014; Rodrigues, 2019). Procedimento metodológico As coletas ocorreram em seis pontos do Parque Estadual de Dois Irmãos, em um módulo do Programa de Pesquisa em Biodiversidade – PPBio Mata Atlântica, instalado em 2013, abrangendo as duas fitofisionomias do PEDI e na área de visitação do Zoológico. O PPBio foi criado em 2004 com o objetivo de intensificar estudos sobre biodiversidade no Brasil e está estruturado em três componentes principais, são eles: inventários, coleções e temáticos, possui 11 núcleos regionais distribuídos entre os diferentes biomas do Brasil além de, núcleos em outros países como Argentina, Austrália, Libéria, Equador, Reino Unido e Nepal. O Programa segue a metodologia RAPELD de Magnusson et al. (2005) (Fig. 1), o módulo instalado no PEDI é composto por duas trilhas principais de 5 km de extensão cada e espaçadas por 1 km entre si. Em cada trilha há três parcelas distribuídas a cada 500 metros distantes mutualmente, com 250 metros de comprimento divididas em 25 segmentos (10 m de comprimento cada) que seguem a curva de

Material e métodos Área de Estudo. O estudo foi realizado em um módulo instalado no Parque Estadual de Dois Irmãos (PEDI) que é uma Unidade de Conservação de Proteção Integral com 1.157,72 ha localizada na região noroeste da cidade do Recife, Pernambuco, Brasil (8°7'30"S e 34°52'30"W; Fig. 1) onde há 14 ha construídos para abrigar o zoológico do Recife. O clima é do tipo As’ - tropical chuvoso, quente e úmido com temperatura média de 23°C, alta umidade entre os meses de março e agosto (estação seca) e precipitação máxima entre junho e julho (Coutinho et al., 1998). Sua vegetação está classificada como Floresta Ombrófila Densa (Moura-Júnior, 2009) e encontra-se inserido em uma matriz urbana, esta área possui também diferentes corpos d’água como açudes e riachos que deságuam no Rio Capibaribe. O PEDI pode ser dividido em duas áreas com dife202

Figura 1. A- Localização geográfica do Parque Estadual de Dois Irmãos, B- Módulo do PPBio no PEDI, C- Modelo da parcela de 250 metros (Adaptado: Gusmão, 2016).

Cuad. herpetol. 34 (2): 201-209 (2020) nível do terreno (Fig. 1C). Em cada parcela foram realizadas coletas bimestrais no período de outubro de 2014 a novembro de 2017. Na área de visitação do zoológico foi realizada busca ativa, antes e após a saída do módulo e encontros ocasionais. As buscas ocorreram durante 10 dias consecutivos, no período diurno (das 8 às 17 horas) e noturno (das 18 às 23 horas) os dados foram coletados através dos métodos de procura visual limitada por tempo (PVLT; Campbell e Christman, 1982; Martins e Oliveira, 1998), vestígios (V), encontro ocasional (EO) e armadilhas de interceptação e queda - pitfall traps (AIQ; Greenberg et al., 1994; Cechin e Martins 2000) em forma de “Y”, constituídas por quatro baldes de 100 litros interligados por cercas guias de lona com distância de 10 metros entre si. As armadilhas (quatro grids por parcela) foram instaladas seguindo a metodologia RAPELD, em três das seis parcelas, uma na área Fazenda Brejo dos Macacos e duas na Mata de Dois Irmãos, totalizando 4.800 horas/balde. Em relação aos animais capturados, realizamos a biometria, peso, sexo e marcação com picote nas escamas ventrais e bioelastômero para posterior reconhecimento em caso de recaptura (animais maiores também receberam microchips). Como material testemunho 14 espécimes foram coletados e depositados na Coleção Herpetológica e Paeloherpetológica da UFRPE, Nordeste de Pernambuco (Licença Sisbio 11218-1; CHP-UFRPE; Apêndice I). Realizamos uma curva de rarefação visando reduzir o efeito do esforço amostral, obtendo a riqueza extrapolada. Também estimamos a riqueza utilizando os índices de Jackknife 1 e ACE. Utilizou-se também a constância de ocorrência de cada espécie através do método proposto por Dajoz (1983), cujos dados percentuais são obtidos a partir da equação C= p*100/P, onde: C= constância de ocorrência de cada espécie, p= número de idas a campo em que a espécie foi registrada e P= número total de idas a campo. Essa análise define as seguintes categorias para as espécies: constantes (ocorreram em mais de 50% das amostras), acessórias (ocorreram entre 25% e 50% das amostras) e acidentais (ocorreram em menos de 25% da amostra). Para todos os testes foi utilizado o programa Software R (R Development Core Team, 2017).

Figura 2 . Curva de rarefação das espécies de serpentes amostradas no Parque Estadual de Dois Irmãos no período de outubro de 2014 a novembro de 2017.

A curva de rarefação não alcançou a assíntota e a riqueza observada foi menor do que a estimada pelo índice Jackknife 1 (30 espécies), porém igual à riqueza esperada segundo o índice de ACE (23 espécies) (Fig. 3). Reforçando que apesar do grande esforço amostral o fragmento florestal comporta uma maior riqueza de espécies de serpentes ainda desconhecida. O método que resultou um maior número de capturas foi PVLT, com 74 serpentes de 22 espécies (Tabela 1), seguido dos encontros ocasionais com 38 espécimes de 15 espécies e AIQ, que forneceu cinco indivíduos de duas espécies: quatro Tantilla melanocephala (Linnaeus, 1758) e uma Xenodon rabdocephalus (Wied, 1824) (Tabela 1); esta última foi registrada exclusivamente através deste método, acarretando

Resultados Foram registradas 23 espécies de serpentes (21 gêneros de cinco famílias) entre 117 indivíduos encontrados (Fig. 2; Tabela 1) e não houve recaptura.

Figura 3. Curva de estimadores de riqueza de espécies de serpentes do Parque Estadual de Dois Irmãos no período de outubro de 2014 a novembro de 2017.

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V. N. Barbosa et al. - Serpentes de uma UC, Nordeste brasileiro Tabela 1. Riqueza das serpentes do Parque Estadual Dois Irmãos, Recife, Pernambuco, no período de outubro de 2014 a novembro de 2017. Formas de registro: PVLT - Procura visual limitada por tempo, V - Vestígios, AIQ – Pitfall trap e EO – Encontro ocasional; Espécies ameaçadas (*): PAN Herpetofauna Nordestina (ICMBio, 2017). Número de registro – N. Parcelas: Fp- Floresta primária, Fs- Floresta secundária, Z- Zoológico.

Serpentes

Forma de registro

Parcelas

Número de registro

Boidae Boa constrictor constrictor Linnaeus, 1758

PVLT, EO, V

Epicrates cenchria (Linnaeus, 1758)

Corallus hortulana (Linnaeus, 1758)

PVLT, EO

Fp, Z

PVLT

Fs, Z

Colubridae Chironius flavolineatus (Jan, 1863) Dendrophidion atlantica Freire, Caramaschi & Gonçalves, 2010*

PVLT

Fp, Fs, Z

Leptophis ahaetulla (Linnaeus, 1758)

PVLT, EO

Oxybelis aeneus (Wagler in Spix, 1824)

PVLT, EO

Fp, Z

Spilotes pullatus (Linnaeus, 1758)

PVLT, EO

Tantilla melanocephala (Linnaeus, 1758)

PVLT, AIQ

Dipsadidae Atractus maculatus (Günther, 1858)*

PVLT, V

Dipsas neuwiedi (Ihering, 1911)

PVLT, EO

Fp, Z

Erythrolamprus viridis (Günther, 1862)

PVLT, EO

Helicops angulatus (Linnaeus, 1758)

PVLT, EO

Imantodes cenchoa (Linnaeus, 1758)

PVLT

Oxyrhopus petolarius (Linnaeus, 1758)

PVLT

Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854

PVLT

Fp, Z

Philodryas olfersii (Lichtenstein, 1823)

PVLT, EO

Taeniophallus occipitalis (Jan, 1863)

PVLT, EO

Thamnodynastes pallidus (Linnaeus, 1758)

PVLT, EO

Fs, Z

AIQ

Micrurus ibiboboca (Merrem, 1820)

PVLT, EO

Fp, Fs, Z

Micrurus lemniscatus (Linnaeus, 1758)

PVLT, EO

Xenodon rabdocephalus (Wied, 1824) Elapidae

Viperidae Lachesis muta (Linnaeus, 1766)

o primeiro registro para o Estado de Pernambuco, ampliando a distribuição geográfica 742,2 km da localidade mais próxima registrada no município de Catu, estado da Bahia (Marques et al., 2016). Quanto à riqueza nas diferentes áreas, o zoológico rendeu 15 espécies, seguido da floresta mata de Dois Irmãos, com 13, e a Fazenda Brejo dos Macacos com seis. Com relação à composição da comunidade, sete espécies foram registradas apenas na área do zoológico, duas exclusivamente na área de floresta secundária e uma na floresta primária. A floresta primária teve a maior quantidade de espécimes regis204

trados, mas foi a área com maior número de parcelas inseridas (ver Fig. 1). Pelo método de definição da constância de ocorrência de Dajoz (1983), todas as espécies encontradas no PEDI foram consideradas acidentais. As espécies que apresentaram maior número de indivíduos capturados foram: Oxybelis aeneus (N= 18), Leptophis ahaetulla (17), Micrurus ibiboboca (14), Dendrophidion atlantica e Corallus hortulana ambas com 11 indivíduos cada. Em relação ao efeito dos parâmetros abióticos (temperatura média, umidade relativa, pluviosida-

Cuad. herpetol. 34 (2): 201-209 (2020)

Figura 4. Algumas espécies de serpentes registradas no PEDI: A - Boa constrictor; B - Epicrates cenchria; C - Corallus hortulana; D - Chironius flavolineatus; E - Dendrophidion atlantica; F - Leptophis ahaetulla; G - Oxybelis aeneus; H - Spilotes pullatus; I - Tantilla melanocephala (Fotos: Vanessa Barbosa).

de) entre as estações seca e chuvosa na riqueza e abundância de serpentes, registramos apenas um aumento de 12% na abundância de serpentes no período chuvoso (χ2 = 6.231; GL 1; p 0.016). Discussão A curva de rarefação prenuncia que não alcançou a assíntota na última coleta isso indica que apesar do grande esforço para obter dados importantes para a comunidade local, há necessidade de mais

estudos na área sendo fundamental a compreensão e obtenção de informações sobre a riqueza de espécies por serem indispensáveis para subsidiar políticas de conservação (Gotelli e Colwell, 2001). Os inventários de biodiversidade necessariamente têm de ser planejados em torno de procedimentos de estimativas de riqueza (Colwell e Coddington, 1994), reforçando a importância de estudos primários que subsidiem a conservação principalmente em ambientes urbanos que suportam uma fauna endêmica de serpentes, como demostrado no presente estudo. 205

V. N. Barbosa et al. - Serpentes de uma UC, Nordeste brasileiro

Figura 5. Algumas espécies de serpentes registradas no PEDI: A - Erythrolamprus viridis; B - Xenodon rabdocephalus; C - Helicops angulatus; D - Imantodes cenchoa; E - Oxyrhopus petolarius; F - Oxyrhopus trigeminus; G - Dipsas neuwiedi; H - Taeniophallus occipitalis; I - Thamnodynastes pallidus (Fotos: Vanessa Barbosa).

O baixo número de espécies registrado vem sendo apontado para fragmentos urbanos em diversas localidades; por exemplo, Santana et al. (2008) registraram 18 espécies em um fragmento urbano de Mata Atlântica no Nordeste, e isto ressalta que florestas em meio urbano precisam de maior atenção e planejamento (Hamdan et al., 2013). Ressaltamos também que a utilização de mais de um método de amostragem é importante para aumentar as chances de captura de espécies raras que são registradas com maior eficiência através de 206

métodos específicos (Bernarde, 2012); por exemplo, Xenodon rabdocephalus foi capturada apenas pela armadilha de interceptação e queda. Segundo Bernarde (2012), outros fatores além do método de captura adotado podem influenciar a riqueza de espécies encontrada, tais como o esforço amostral e sazonalidade e o grau de preservação da área de estudo. Além disso, ressaltamos que ao trabalhar com serpentes, principalmente em fragmentos urbanos, é fundamental considerar registos de espécimes mortos, pois as serpentes são tidas como

Cuad. herpetol. 34 (2): 201-209 (2020)

Figura 6. Algumas espécies de serpentes registradas no PEDI: A - Atractus maculatus; B - Philodryas olfersii; C - Micrurus ibiboboca; D - Micrurus lemniscatus; E - Lachesis muta (Fotos: Vanessa Barbosa).

animais perigosos pela população local (Fraga et al., 2013) e, devido a essa percepção, em sua maioria são mortas quando encontradas (Fernandes-Ferreira et al., 2011), como a Atractus maculatus que o único indivíduo registrado estava com a cabeça esmagada na trilha. Sendo estas informações utilizadas para a obtenção uma boa compreensão da riqueza de um remanescente florestal para que se possa analisar o grau de conservação de uma área e sua importância ecológica auxiliando na conscientização da comunidade local. A maioria das espécies registradas no presente estudo apresenta ampla distribuição nos biomas brasileiros (Santana et al., 2008; Guedes et al., 2014, Marques et al., 2015), exceto por Atractus maculatus e Dendrophidion atlantica, que são endêmicas da Mata Atlântica nordestina, encontradas apenas em Alagoas (Freire et al., 2010; Passos et al., 2010) e Pernambuco (Nascimento e Santos, 2016; Abegg et al., 2017), além da Paraíba para D. atlantica (Pereira-Filho et al., 2017). Estas espécies apresentam poucos dados ecológicos disponíveis na literatura, sendo fundamental sua conservação para a ciência (Passos et al., 2010; Barbosa et al., 2019; Lima et al., 2019a; Lima et al., 2019b). Assim, apesar da pressão

antrópica sofrida por este remanescente, ele é capaz de suportar populações de espécies endêmicas ressaltando a importância de medidas de conservação em remanescentes urbanos. Nosso trabalho demonstra o potencial do PEDI como área de conservação da comunidade de serpentes devido à sua elevada diversidade para um remanescente urbano, sendo registradas espécies endêmicas da Mata Atlântica, que apresentam poucos dados disponíveis quanto à sua história natural, como Atractus maculatus e Dendrophidion atlantica, e espécies raras, como Lachesis muta e Xenodon rabdocephalus. É importante destacar que L. muta foi registrada por terceiros em área aberta, alertando para uma perturbação ambiental e perda de hábitat, tendo em vista que esta espécie é registrada em ambientes preservados e no interior de mata e a destruição de hábitat e o isolamento das populações são as principais ameaças para a espécie (Vial e Jimenez-Porras, 1967; Rodrigues et al., 2013; Pereira-Filho et al., 2017). O PEDI, por ser um fragmento urbano, sofre constante ação antrópica sendo registrado o corte ilegal de madeira, fogo, trilhas não regulamentadas, animais domésticos asselvajados, clareiras de origem antrópica, espécies invasoras e 207

V. N. Barbosa et al. - Serpentes de uma UC, Nordeste brasileiro degradação de corpos hídricos e urbanização são confirmados como alguns impactos sofridos na área de preservação (Ribeiro et al., 2007; Rodrigues, 2019) além de predação de animais silvestres por animais domésticos das redondezas do PEDI. Desta forma, é necessária a tomada de ações a curto e longo prazo, focadas na comunidade do entorno do PEDI, visando a conservação de sua fauna e flora. Agradecimentos Agradecemos a todos os funcionários do Zoológico de Dois Irmãos e à todos os pesquisadores que auxiliaram em campo; ao Programa de Pesquisa em Biodiversidade – PPBio - Mata Atlântica pelo financiamento (Processo CNPq 457483/2012-1, Edital CNPq nº 35/2012/PPBio/Geoma). VNB e JMSA agradecem ao Conselho Nacional de Pesquisa (CNPq) pela bolsa de mestrado e RAFG pela bolsa de doutorado. Literatura citada

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Cuad. herpetol. 34 (2): 201-209 (2020) J.R.E.B.; Pessoa, L.M.; Santos-Filho, F.S.; Medeiros, D.P.W.; Pimentel, R.M.M. & Zickel, C.S. 2009. Diversidade de plantas aquáticas vasculares em açudes do Parque Estadual de Dois Irmãos (PEDI), Recife-PE. Revista de Geografia 26: 278-293. Nascimento, V. & Santos E.M. 2016. Geographic Distribution: Dendrophidion atlantica. Herpetological Review 47: 261. Navega-Gonçalves, M.E.C. & Porto, T. 2016. Conservação de serpentes nos biomas brasileiros. Bioikos 30: 55-76. Passos, P.; Fernandes, R.; Bérnils, R.S. & Moura-Leite, J.C. 2010. Taxonomic revision of the Brazilian Atlantic Forest Atractus (Reptilia: Serpentes: Dipsadidae). Zootaxa 2364: 1-63. Pereira-Filho, G.A.; Vieira, W.L.S.; Alves, R.R.N.; França, F.G.R.; Rodrigues, J.B. & Montingelli, G.G. 2017. Serpentes da Paraíba: Diversidade e Conservação. João Pessoa. Autores. R Development Core Team. 2017. R: A language and environment for statistical computing. version 2.14. R Foundation for Statistical Computing, Vienna. Ribeiro, E.M.S.; Ramos, E.M.N.F. & Silva, J.S.B. 2007. Impactos Ambientais Causados pelo Uso Público em Áreas Naturais do Parque Estadual de Dois Irmãos, Recife – PE. Revista Brasileira de Biociências 5: 72-74. Rodrigues, M.T. 2005. The conservation of Brazilian reptiles: Challenges of a megadiverse country. Conservation Biology 19: 659-664. Rodrigues, R.; Albuquerque, R.L.; Santana, D.J.; Laranjeiras, D.O.; Protázio, A.S.; França, F.G.R. & Mesquita, D.O. 2013. Record of the occurrence of Lachesis muta (Serpentes, Viperidae) in an Atlantic Forest fragment in Paraíba, Brazil, with comments on the species’ preservation status. Biotemas 26: 283-286. Rodrigues, L.S. 2019. A diversidade arbórea em uma paisagem florestal urbana: efeitos dos estágios sucessionais e de

perturbações antrópicas crônicas. Recife, PE. Dissertação. Universidade Federal Rural de Pernambuco. Santana, G.G.; Vieira, W.L.S.; Pereira-Filho, G.A.; Delfi, F.R.; Lima, Y.C. & Vieira, K.S. 2008. Herpetofauna em um fragmento de Mata Atlântica no Estado da Paraíba, Região Nordeste do Brasil. Biotemas 21: 75-84. SEMAS – Secretaria de Meio Ambiente e Sustentabilidade. 2014. Plano de Manejo – Parque Estadual de Dois Irmãos. Recife. SOS Mata Atlântica, Fundação. 2016. Mata Atlântica 30 anos. Relatório Anual 2016. São Paulo; 2016. Tozetti, A.M.; Sawaya, R.J.; Molina, F.B.; Bérnils, R.S.; Barbo, F.E.; Leite, J.C.M.; Borges-Martins, M.; Recorder, R.; Júnior, M.T.; Argôlo, A.J.S.; Morato, S.A.A. & Rodrigues, M.T. 2018. Répteis; p. 315-364; In: Monteiro-Filho, E.L. & Conte, C.E. (org.). Revisões em zoologia: Mata Atlântica. Curitiba: UFPR. Vial, J.L. & Jimenez-Porras, J.M. 1967. The Ecogeography of the Bushmaster, Lachesis muta, in Central America. American Midland Naturalist 78: 182-187. Apêndice I. Espécies de serpentes coletadas neste estudo e depositadas na Coleção Herpetológica e Paleoherpetológica da Universidade Federal Rural de Pernambuco, Recife, Brasil (CHP-UFRPE). Chironius flavolineatus (CPH-UFRPE 4190), Dendrophidion atlantica (CHP-UFRPE 4239; 4242; 5003), Erythrolamprus viridis (CHP-UFRPE 4241; 4244), Imantodes cenchoa (CHP-UFRPE 4048), Micrurus ibiboboca (CHP-UFRPE 4044; 4191; 4243), Oxybelis aeneus (CHP-UFRPE 4240), Oxyrhopus trigeminus (CHP-UFRPE 3962), Dipsas neuwiedi (CHP-UFRPE 4193) e Tantilla melanocephala (CHP-UFRPE 4192).

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Natural history of Xenodon matogrossensis (Scrocchi and Cruz, 1993) (Serpentes, Dipsadidae) in the Brazilian Pantanal Hugo Cabral1,2,3, Liliana Piatti4, Marcio Martins5, Vanda L. Ferreira4 Programa de Pós-Graduação em Biologia Animal, Universidade Estadual Paulista, 15054-000, São José do Rio Preto, SP, Brazil. 2 Instituto de Investigación Biológica del Paraguay. Del Escudo 1607, Asunción, Paraguay. 3 Mapinguari – Laboratório de Biogeografia e Sistemática de Anfíbios e Répteis, Universidade Federal de Mato Grosso do Sul, 79070-900, Campo Grande, MS, Brazil. 4 Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, 79070-900, Campo Grande, MS, Brazil. 5 Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, 05508-090 São Paulo, SP, Brazil. 1

Recibido: 30 Abril 2020 Revisado: 08 Junio 2020 Aceptado: 28 Julio 2020 Editor Asociado: V. Arzamendia doi: 10.31017/CdH.2020.(2020-026)

ABSTRACT Xenodon mattogrossensis is a neotropical snake restricted to the central part of South America, in the Pantanal wetlands and a few neighbouring areas. The available information about this species in the literature is restricted to geographical distribution, morphological variation and anecdotal information on habitat use. Here we present data on diet, sexual dimorphism and reproduction of X. matogrossensis. We gathered information on diet and reproduction from 72 specimens of X. matogrossensis deposited in scientific collections. This species feeds mainly on amphibians, but also consumes squamate eggs and other small vertebrates. Mature females are generally bigger than mature males considering body size and head width, but males have longer tail than females. The number of follicles and eggs is not related with body size in females of X. matogrossensis. Females showed larger follicle sizes from October to April, however females carrying eggs are found in all stations of the year. The information provided here, associated with others available in the literature can contribute to the assessment of the conservation status of this species and even to design conservation actions in case they are needed in the future. Key words: Diet; Reproductive Biology; Reptiles; Xenodontinae.

Introduction Xenodon matogrossensis (Scrocchi and Cruz, 1993) (Fig. 1) is a Neotropical snake distributed in the central part of South America, in the Pantanal wetlands and neighbouring ecoregions (Beni, Cerrado and Chaco Savannas; Scrocchi and Cruz, 1993; Giraudo, 1997; Strüssmann et al., 2011; Cabral et al., 2015). It is a member of a species group within Xenodon comprising six species that were previously allocated in the genus Lystrophis Cope, 1885 until Zaher et al. (2009) synonymized these genera based on molecular evidences. This species group contains X. dorbignyi (Bibron, 1854), X. histricus (Jan, 1863), X. nattereri (Steindachner, 1867), X. matogrossensis, X. pulcher (Jan, 1863), and X. semicinctus (Duméril, Bibron and Duméril, 1854). These species are distributed mainly in open areas of South America and are characterized by having the rostral scale conspicuously keeled (Scrocchi and Cruz, 1993;

Cabral et al., 2015). Xenodon pulcher, X. semicinctus, and X. matogrossensis show mimetic colour patterns with coral snakes of the genus Micrurus, while the other species of the group show a predominantly pale ground colour with simple bands or ocelli (Cei, 1993; Giraudo, 2002). Members of this species group are considered psamophilic, inhabiting open areas with sandy soil, and feed mainly on anurans, lizards, and squamate eggs (Orejas-Miranda, 1966; Gudynas, 1979; Williams and Scrocchi, 1994; Oliveira et al., 2001; Carreira and Lombardo, 2007; Nenda and Cacivio, 2007, Sawaya et al., 2008). Concerning reproduction, there is information only for X. natteteri, that probably show seasonal reproduction during the hottest months of the year (Sawaya et al., 2008). However, there is only scarce information about the natural history of X. matogrossensis in the literature, being

Author for correspondence: huguitocabral@gmail.com

211

H. Cabral et al. - Natural history of Xenodon matogrossensis limited to notes about geographical distribution and scattered information on morphological variation and habitat use (Cabral et al., 2015; Nogueira et al., 2019). Here we present data on diet, sexual dimorphism and reproduction of X. matogrossensis. Material and methods We examined 72 specimens of X. matogrossensis deposited in the Coleção Zoológica de Referência da Universidade Federal de Mato Grosso do Sul (ZUFMSREP). All records are from Mato Grosso do Sul state (See Appendix I, for specimens examined). For each specimen we recorded the sex and the following morphological variables: (1) snout-vent length (SVL), (2) tail length (TL), (3) head length (HL), (4) head width (HW), (5) number of ventral scales (VS), and (6) number of subcaudal scales (SS). Measurements were made with a measuring tape to the nearest millimeter (SVL and TL), and the remaining variables with a dial calliper to the nearest 0,01 mm. We made a mid-ventral incision to check gut

contents and reproductive characters of the specimens. To describe the diet of X. matogrossensis we identified prey remains to the lowest possible taxonomic level, under a stereoscopic microscope. To describe aspects of reproductive biology, we counted and took measures of all follicles or oviductal eggs in females and recorded the length of the largest testis (mm) in males. Sexual maturity in males was determined by the presence of convoluted ductus deferens (Shine, 1982; Almeida-Santos and Salomão, 2002, Pizzatto and Marques, 2002, 2006). Females were considered mature if they had secundary vitellogenic follicles (enlarged and yellowish ovarian follicles), oviductal eggs or folded oviducts (Blackburn, 1998; Mesquita et al., 2013). Minimum size at maturity was estimated as the smallest reproductive individual of each sex. We estimated the maximum potential clutch size by counting the number of secondary vitellogenic follicles, oviductal eggs (counting only eggs, or follicles when eggs where absents), and tested if clutch size is affected by female size. We also recorded if females showed distended or folded middle oviduct macroscopically (Blackburn, 1998; Almeida-Santos et al., 2014), and if males presented turgid testes macroscopically when freshly killed (Pleguezuelos and Fahd, 2004). This data was used to infer the period of reproductive activity (AlmeidaSantos et al., 2014). The degree of sexual dimorphism (SSD index) was calculated as 1 − (mean adult SVL of the larger sex/mean adult SVL of the smaller sex) (Gibbons and Lovich, 1990; Shine, 1994). Positive and negative values of SSD correspond to females larger than males and vice versa, respectively. We used an analysis of variance (ANOVA) to test for sexual dimorphism in SVL and scale counts. The other morphological variables (TL, HL and HW) often vary with body length, so we used SVL as a covariate in an analysis of covariance (ANCOVA) to compare these variables between sexes. We tested for effects of body size (SVL) of females on follicles and number of eggs using regression analyses. Statistical analyses were performed with package vegan (Oksanen et al., 2013) in R software (R Core Team, 2019). Results

Figure 1. Individual of Xenodon matogrossensis (A) and general view of is habitat at Fazenda Nhumirim, Corumbá, Mato Grosso do Sul state, Brazil (B).

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Females of X. matogrossensis are significantly larger than males (ANOVA F= 4.16, p= 0.049; Table 1), with an SSD index of 0.15. Additional significant differences between mature males and females were

Cuad. herpetol. 34 (2): 211-218 (2020) Table 1. Summary of morphological variables of X. matogrossensis from Mato Grosso do Sul state, Brazil. Numbers in bold indicate significant differences (p < 0.05) between sexes (considering mature individuals).

Morphological Variable

Females N= 33 Mean (Range)

Males N= 39 Mean (Range)

snout-vent length (mm)

294.3 (118-487)

246.2 (115-395)

38.21 (15-61)

40.26 (16-67)

tail length (mm) head length (mm)

17.26 (9.12-26.30)

14.6 (9.80-23.48)

head width (mm)

11.47 (5.94-18.24)

9.32 (5.78-17.42)

135.5 (132-147)

136 (129-145)

26.82 (23-32)

31.08 (25-42)

ventral scale sub-caudal scale

found for tail length (Fig. 2), head width and number of subcaudal scales (ANCOVA F= 23.49, p < 0.001; ANCOVA F= 5.06, p= 0.031; ANOVA F= 24.8, p < 0.001; respectively). We found 13 females and 22 males with evidence of sexual maturity through the macroscopic analysis of the gonads. Among them, the smallest mature female and male measured 123 mm and 180 mm SVL, respectively. We failed to find a significant effect of female body size on the number of follicles (r2 = 0.095, F= 3.023, p= 0.0983) or eggs (r2 = 0.291, F= 1.884, p= 0.186), which varied between 1 and 9 (Fig. 3). As is possible to observe at Figure 3, one of the females was found with 9 eggs, even being much smaller (123 mm SVL) than the other mature females (between 294 and 497 mm, Table 2). Five females presented distended oviduct and

secondary follicles or eggs at the same time (Table 2), what could suggest the occurrence of multiple reproductive events in short periods of time. The seasonal size variation of follicles and testes of the mature specimens analysed showed that females have secondary vitellogenic follicles from October to April and males have large testes (> 20 mm) from July to December (Fig. 4). The number of sexually active specimens (if females showing distended or folded middle oviduct macroscopically, and if males presenting turgid testes) was larger than that of sexually inactive specimens between September to February (Fig. 5). Nevertheless, the distribution of body sizes throughout the year suggests that juvenile recruitment occurs from the end of the wet season (March) to the middle of the dry season (July) and in November/

Figure 2. Variation in tail length in relation to snout-vent length in males (white dots) and females (black dots) of Xenodon matogrossensis.

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H. Cabral et al. - Natural history of Xenodon matogrossensis

Figure 3. Variation in number of secondary follicles (white dots) or eggs (black dots) in relation to snout-vent length in mature females of Xenodon matogrossensis.

December (Fig. 6). Of the 72 specimens analysed, only eight had prey remains in the gut: five had frog remains, two had elongate squamate eggs and one had bones of an unidentified vertebrate. Among amphibian prey, we were able to identify Physalaemus nattereri (Steindachner, 1863) and Rhinella major (MĂźller and Hellmich, 1936) (one record each). We also found

portions of leptodactylid prey in two individuals, as well as digits of an unidentified anuran in one specimen. Discussion Our results indicate that X. matogrossensis shows the typical natural history features of its species group,

Table 2. Summary of reproductive characteristic of mature females of X. matogrossensis from Mato Grosso do Sul state, Brazil. SVL: snout-vent length; FnV: non vitellogenic follicles; Sec. Fol: secondary follicles.

SVL (mm)

Month

FnV

Sec.Fol

Egg

Follicle Size (mm)

Egg Size (mm)

Folded Oviduct

322

Jan

17.2

FALSE

353

Jan

8.55

TRUE

366

Jan

9.55

TRUE

415

Feb

TRUE

441

Apr

16.53

FALSE

123

Sep

36.15

FALSE

386

Sep

5.43

FALSE

487

Jul

31.55

TRUE

294

Dec

9.38

TRUE

395

Dec

32.67

TRUE

406

Dec

23.94

FALSE

339

Nov

TRUE

380

Nov

22.36

FALSE

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Cuad. herpetol. 34 (2): 211-218 (2020)

Figure 4. Temporal variation of testis size of mature males (A), secondary follicles (open circles) or eggs (black circles) in females (B) and snout-vent length of immature (C) (triangles: males; circles: females) of Xenodon matogrossensis.

formerly assigned to Lystrophis: (1) they feed mainly on amphibians, although it also consumes squamate eggs and other small vertebrates; (2) occur in open areas with sandy soils; and (3) they have a seasonal reproduction (Lema et al., 1983; Oliveira et al, 2001; Carreira, 2002). Females showed large follicle sizes from October to April, suggesting that reproduction may be more frequent during this period, even though individuals may be reproductively active throughout the year. Testes are larger in the first half of the rainy season (October to December), what could be an indicative of higher spermatogenesis activity during this period and another indicative of more reproduction events in this period. However, the lack of histological analyses of testes and a higher number of females collected along the years does not allow us to make strong conclusion about the

reproductive cycle of X, matogrossensis here analysed (Almeida-Santos et al., 2014). At the Pantanal region, the period of October to April comprises the hottest and wettest months of the year when several frog species are more actives and breed (Prado et al., 2005). This greater availability of prey in conjunction to suitable conditions for high activities of reptiles could favour seasonal reproduction. Oliveira and Martins (2002) suggested that both the snakes and their prey may be responding to the same climatic conditions to breed and seasonal reproduction was reported for snakes from the wetland and dry plain of Pantanal, such as Micrurus pyrrhocryptus Cope, 1862 (Ă vila et al., 2010), and the viviparous Helicops leopardinus (Schlegel, 1837) (Ă vila et al., 2006), and Bothrops mattogrossensis Amaral, 1925 (Monteiro et al., 2006). The energetic cost of oviparity is lower when compared to viviparity (Gregory et al., 1999; Andrews and Mathies, 2000; Shine, 1980, 1985, 2003), and this lower energy waste might make possible multiple reproduction in the same reproductive season (Almeida-Santos et al., 2014). In this work five females presented distended oviduct and secondary follicles or eggs at the same time, what could suggest the occurrence of multiple reproductive events in short periods of time. Multiple reproductive events were already reported for oviparous populations of Neotropical xenodontines like Xenodon dorbignyi (specie closely related to X. matogrossensis, Oliveira et al., 2011), Erythrolamprus poecilogyrus poecilogyrus (Wied-Neuwied, 1825) (Pinto and Fernandes, 2004), E. miliaris (Linnaeus, 1758) (Eisfeld and Vrcibradic, 2019), and other Xenodontini species (Pizzatto et al., 2008). Nevertheless, the condition of show distended oviduct and secondary follicles

Figure 5. Temporal variation of the occurrence of mature (lighter bars) and immature (darker bars) individuals of Xenodon matogrossensis.

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H. Cabral et al. - Natural history of Xenodon matogrossensis

Figure 6. Temporal variation of snout-vent length of males (white dots) and females (black dots) of X. matogrosssensis.

or eggs at the same time can also be sometimes observed when females are ready to receive the follicles that were not ovulated (Almeida Santos et al. 2014), what require that more studies need be done to confirm our hypothesis of multiple reproductive events in X. matogrossesis. Sexual dimorphism in body size, as observed in X. matogrossensis, is commonly found in other terrestrial snakes. The tail of males accommodates the hemipenes and their associated muscles, what results in longer tail and larger number of subcaudal scales when compared with females (King, 1989). Additionally, despite females usually being bigger than males because of enhanced fecundity (Seigel and Fitch, 1984; Shine, 1993; 1994), female body size does not explain the variation in the number of follicles and eggs in X. matogrossensis. Considering that more than 90% of the mature females measured around 300 mm or more of SVL (Fig. 3), we believe that at this size females of X. matogrossensis could be considered as reproductively actives. Also, early �� maturation imposes a higher cost on females (Madsen and Shine, 1994) and in many species of snakes the immature eggs or early developing follicles will not be recruited and, thus, will not fully develop into eggs (Seigel and Ford, 1987). 216

The information on the natural history of X. matogrossensis provided here, associated with the information on distribution and habitat use available in the literature (Nogueira et al., 2019), can contribute to the assessment of the conservation status of this species and even to design conservation actions in case they are needed in the future. Acknowledgements We would like to thank Gustavo Graciolli (ZUFMS) for allowing us to review specimens under their care and Universidade Federal de Mato Grosso do Sul. HC would like to thank the Consejo Nacional de Ciencia y Tecnología (CONACYT), for partial financial support through the Programa Nacional de Incentivo a Investigadores (PRONII), and Coordenação de Aperfeiçoamento Pessoal de Nível Superior (CAPES, Brazil), Programa de Estudantes-Convênio de Pós-graduação (PEC-PG), for a fellowship. MM thanks Fundação de Amparo à Pesquisa do Estado de São Paulo for a grant (# 2018/14091-1) and CNPq for a research fellowship (# 306961/2015-6). This study was partially funded by CAPES/ Brazil - Finance Code 001 and Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (# 187/2014). Conselho Na-

Cuad. herpetol. 34 (2): 211-218 (2020) cional de Desenvolvimento Científico e Tecnológico (CNPq) provided a researcher’s fellowship to VLF (PQ2/CNPq #309305/2018-7) and partial financial support to project (CNPq #409003/2018-2). Literature cited

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H. Cabral et al. - Natural history of Xenodon matogrossensis in reproductive cycles and activity of the water snake Liophis miliaris (Colubridae) in Brazil. Herpetological Journal 16: 353-362. Pizzatto L.; Jordão R.S. & Marques O.A.V. 2008. Overview of reproductive strategies in Xenodontini (Serpentes: Colubridae: Xenodontinae) with new data for Xenodon neuwiedii and Waglerophis merremii. Journal of Herpetology 42: 153-162. Pleguezuelos, J. & Fahd, S. 2004. Body size, diet and reproductive ecology of Coluber hippocrepis in the Rif (Northern Morocco). Amphibia-Reptilia 25: 287-302 Prado, C., Uetanabaro, M. & Haddad, C. 2005. Breeding activity patterns, reproductive modes, and habitat use by anurans (Amphibia) in a seasonal environment in the Pantanal, Brazil. Amphibia-Reptilia 26: 211-221. R Development Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Sawaya, R. J.; Marques, O. A. V. & Martins, M. 2008. Composição e história natural das serpentes de Cerrado de Itirapina, São Paulo, sudeste do Brasil. Biota Neotropica 8: 127–149. Seigel, R. & Fitch, H. 1984. Ecological patterns of relative clutch mass in snakes. Oecologia 61: 293–301. Seigel, R.A. & Ford, N.B. 1987. Reproductive ecology. 210- 252. In: Seigel, R.A., Collins, J.T. & Novak, S.S. (eds), Snakes: Ecology and Evolutionary Biology. New York: McMillan Publishing Company. Scrocchi, G. & Cruz, F. 1993. Description of a new species of genus Lystrophis Cope and a revalidation of Lystrophis pulcher (Jan, 1863) (Serpentes; Colubridae). Papéis Avulsos de Zoologia 38: 171-186. Shine, R. 1980. “Costs” of reproduction in reptiles. Oecologia 46: 92-100. Shine, R. 1982. Ecology of the australian elapid snake Echiopsis curta. Journal of Herpetology 16: 388-393 Shine, R. 1985. The evolution of viviparity in reptiles: an ecological analysis: 605-694. In: Gans, C. & Billett, F. (eds.), Biology of the Reptilia, Volume 15. John Wiley and Sons. New York, N.Y. Shine, R. 1993: Sexual dimorphism in snakes: 49-86. In: Snakes: Ecology & Behavior, Seigel, R.A. & Collins, J.T., (eds), New York. McGraw-Hill, Inc. Shine, R. 1994. Sexual size dimorphism in snakes revisited. Copeia 1994: 326-346. Shine, R. 2003. Reproductive strategies in snakes. Proceedings of the Royal Society of Biological Sciences 270: 995-1004.

Strüssmann, C., Prado, C.; Ferreira, V. & Kawashita-Ribeiro, R.A. 2011. Diversity, ecology, management and conservation of amphibians and reptiles of the Brazilian Pantanal: a review. 497-521. In: Junk, W.L.; Silva, C.J.; Nunes da Cunha, C. & Wantzen, K.M. (eds.), The Pantanal – Ecology, biodiversity and sustainable management of large neotropical seasonal wetland. Pensoft Publishers. Sofia. Williams, J.D. & Scrocchi, G.J. 1994. Ofidios de agua dulce de la República Argentina. Fauna de agua dulce de la República Argentina 42: 1-55. Zaher, H.; Grazziotin, F.G, Cadle, J.E.; Murphy, G.W.; MouraLeite, J.C. & Bonatto, S.L. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: A revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia (São Paulo) 49: 115-153. Appendix I Specimens examined Xenodon matogrossensis: (BRAZIL): Mato Grosso do Sul: Anastácio - ZUFMSREP 01463, ZUFMSREP 01523, ZUFMSREP 01650, ZUFMSREP 01654; Aquidauana ZUFMSREP 00091, ZUFMSREP 00108, ZUFMSREP 0250, ZUFMSREP 0540, ZUFMSREP 0541, ZUFMSREP 0543, ZUFMSREP 0545, ZUFMSREP 0546, ZUFMSREP 0547, ZUFMSREP 0606, ZUFMSREP 0607, ZUFMSREP 0608, ZUFMSREP 0612, ZUFMSREP 01464, ZUFMSREP 01465, ZUFMSREP 01466, ZUFMSREP 01467, ZUFMSREP 01468, ZUFMSREP 01470, ZUFMSREP 01471, ZUFMSREP 01472, ZUFMSREP 01473, ZUFMSREP 01474, ZUFMSREP 01475, ZUFMSREP 01512, ZUFMSREP 01537, ZUFMSREP 01570, ZUFMSREP 01604, ZUFMSREP 01620, ZUFMSREP 01631, ZUFMSREP 01648, ZUFMSREP 01660, ZUFMSREP 01690, ZUFMSREP 01694, ZUFMSREP 01700, ZUFMSREP 01701, ZUFMSREP 01720, ZUFMSREP 01955, ZUFMSREP 01983, ZUFMSREP 01984, ZUFMSREP 01986, ZUFMSREP 01987, ZUFMSREP 01988, ZUFMSREP 01989, ZUFMSREP 01990, ZUFMSREP 01991, ZUFMSREP 01992, ZUFMSREP 01993, ZUFMSREP 01994, ZUFMSREP 01996, ZUFMSREP 01997, ZUFMSREP 01998, ZUFMSREP 01999, ZUFMSREP 02001, ZUFMSREP 02002, ZUFMSREP 02003, ZUFMSREP 02004, ZUFMSREP 02145, ZUFMSREP 03539; Bodoquena: ZUFMSREP 01995; Corumbá: ZUFMSREP 01291, ZUFMSREP 03542, ZUFMSREP 03540, ZUFMSREP 03541; Miranda: ZUFMSREP 02153; Porto Murtinho: ZUFMSREP 0604, ZUFMSREP 0609, ZUFMSREP 02755.

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A second new species for the rare dipsadid genus Caaeteboia Zaher et al., 2009 (Serpentes: Dipsadidae) from the Atlantic Forest of northeastern Brazil Giovanna Gondim Montingelli1, Fausto Erritto Barbo2, Gentil Alves Pereira Filho3, Gindomar Gomes Santana4, Frederico Gustavo Rodrigues França3, Felipe Gobbi Grazziotin2, Hussam Zaher1 Museu de Zoologia da Universidade de São Paulo, São Paulo, Brazil. Av. Nazaré, 481, 04263-000, Ipiranga, São Paulo, Brazil. 2 Laboratório de Coleções Zoológicas – LCZ, Instituto Butantan, Avenida Vital Brazil, 1500, 05503-900, São Paulo, SP, Brazil. 3 Centro de Ciências Aplicadas e Educação, Departamento de Engenharia e Meio Ambiente, Universidade Federal da Paraíba, 58297-000, Rio Tinto, PB, Brazil. 4 Programa de Pós-Graduação em Ecologia e Conservação, Departamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Estadual da Paraíba. Rua Baraúnas, 351, 58429-500, Campina Grande, PB, Brazil. 1

Recibido: 19 Mayo 2020 Revisado:

Julio

2020

Aceptado: 21 Julio 2020 Editor Asociado: V. Arzamendia doi: 10.31017/CdH.2020.(2020-003) zoobank: urn:lsid:zoobank. org:pub:BFB360F0-28BA4 8 A 1 - A 0 D 2 - B DA 4 C 6 5 8 5 8 5 B

ABSTRACT Caaeteboia is a rare and elusive monotypic genus of Neotropical snake, being one of the least known dipsadids of the Brazilian Atlantic Forest. Here, we assess the morphological and genetic diversity of this genus, comparing these results with several other genera of Xenodontinae. Our combined results revealed the presence of an unknown species from the northeastern portion of the Atlantic Forest. The new species is distributed throughout the enclaves of coastal open forests mixed with savanna-like habitat, locally known as “Floresta de Tabuleiro”, and submontane ombrophilous forests in the Brazilian states of Paraíba and Pernambuco. This new species is easily distinguished from C. amarali by its lower number of dorsal, ventral, and subcaudal scales, and a remarkable dark lateral stripe from the nostril up to the anterior third of the body. The new species extends the distribution of the genus in approximately 700 kilometers northwards, reinforcing the importance of the conservation of small remnants of Atlantic Forest in northeastern Brazil, which still harbor high levels of endemicity and diversity. Key words: Caaeteboia; Atlantic Forest; Taxonomy; Xenodontinae; New Species. RESUMO Caaeteboia é um gênero de serpente raro e monotípico da região Neotropical, sendo um dos dipsadídeos menos conhecidos da Floresta Atlântica brasileira. Neste trabalho, avaliamos a diversidade morfológica e genética desse gênero, comparando-o com outros gêneros de Xenodontinae. Nossos resultados combinados revelaram a presença de uma espécie desconhecida da porção nordeste da Floresta Atlântica. A nova espécie se distribui ao longo dos enclaves de florestas abertas costeiras misturadas com habitats savânicos, conhecidos localmente por “Florestas de Tabuleiro”, e florestas ombrófilas submontanas nos estados da Paraíba e de Pernambuco. Essa nova espécie é distinguida de C. amarali pelo menor número de escamas dorsais, ventrais e subcaudais, e por uma evidente linha escura lateral desde o focinho até o terço anterior do corpo. A nova espécie amplia a distribuição do gênero para aproximadamente 700 quilômetros ao norte, e reforça a importância da conservação dos pequenos remanescentes de Floresta Atlântica no nordeste do Brasil, os quais ainda abrigam altos níveis de endemismo e diversidade. Palavras-chave: Caaeteboia; Floresta Atlântica; Taxonomia; Xenodontinae; Nova Espécie.

Introduction Within the highly diverse fauna of snakes distributed in the Brazilian Atlantic Forest, the rare monospeci-

fic Caaeteboia Zaher et al., 2009 is one of the poorest known genera of Dipsadidae (Zaher et al., 2009;

Author for correspondence: mastigodryas@gmail.com

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G. Montingelli et al. - A second new species of genus Caaeteboia Passos et al., 2012, Fig. 1). Since the description of its type species—Liophis amarali Wettstein, 1930— few specimens were deposited in herpetological collections (Passos et al., 2012). Despite the lack of a comprehensive sampling, C. amarali is known to be a small oviparous and predominantly terrestrial snake that forages actively on the terrestrial and arboreal environments looking for frogs and lizards (Marques et al., 2001; Passos et al., 2012). Recently published studies indicated that Caaeteboia amarali represent a unique lineage, through evidence of DNA sequences, as well as cranial and hemipenial morphology (Zaher et al., 2009, 2018, 2019; Grazziotin et al., 2012; Passos et al., 2012). In recent phylogenetic analyses, the genus is recovered as an independent South American Xenodontine lineage with ambiguous affinities with Xenopholis, Saphenophis, and Hydrodynastes (Grazziotin et al., 2012; Zaher et al., 2018, 2019). To indicate this uniqueness, Zaher et al., (2009) erected a monospecific tribe, Caaeteboini, for C. amarali. Externally, C. amarali is easily distinguished from other Atlantic forest Xenodontine snakes by its light gray head and pale body coloration marked by a “V” shaped dark mark extending backwards from the parietals and forming a vertebral stripe that fades on the anterior portion of the dorsum, and a darkbrown stripe on each side of the head that extends from the nostril to the postocular region, bordering dorsally the light cream supralabials and extending as blotches to the anterior third of the body (Passos et al., 2012). Caaeteboia amarali is known to occur throughout the coastal lowlands of the Brazilian Atlantic Forest, from southern Bahia to southern Santa Catarina states, and the questionable westernmost record of the type-locality, in the state of Minas Gerais (Passos et al., 2012). Two records were recently provided by Passos et al., (2012), from Armação de Búzios, state of Rio de Janeiro, and Sooretama, state of Espírito Santo, filling a persistent gap in the distribution of the genus. In March 2008, a specimen of Xenodontinae was collected at Cruz do Espírito Santo, state of Paraíba, northeastern Brazil, in a fragment of the Atlantic Forest. Ten years later, in July 2018, another specimen with similar characteristics was collected nearby the previous individual, in the municipality of Pedras de Fogo (Fig. 1), also in state of Paraíba. An additional third specimen was recorded from municipality of Saloá, state of Pernambuco, and was handled and photographed in nature, but not collec220

ted. All three exhibit the almost all diagnostic features of the genus Caaeteboia enlisted above. However, these three individuals share characteristics that are easily distinguished from C. amarali, suggesting their recognition as a distinct species. Here we test this hypothesis, employing morphological and genetic data to compare these three individuals with other specimens of Caaeteboia, including the type material of Liophis amarali. The results allowed us to confirm this hypothesis, prompting us to describe a new species for the genus. Material and methods Specimens examined and morphological evaluation We analyzed 15 specimens of Caaeteboia, including 12 individuals of C. amarali and three of the new species (Appendix 1) deposited in the following Brazilian collections (acronyms given in parenthesis): Instituto Butantan (IBSP), São Paulo; Museu de História Natural Capão da Imbuia (MHNCI), Curitiba, Paraná; Museu Nacional, Universidade Federal do Rio de Janeiro (MNRJ), Rio de Janeiro; Museu

Figure 1. Geographic distribution of Caaeteboia amarali (circles) and C. gaeli sp. nov. (triangles). White symbols represent type-localities.

Cuad. herpetol. 34 (2): 219-230 (2020) de Zoologia, Universidade de São Paulo (MZUSP), São Paulo; Coleção Zoológica Gregório Bondar (CZGB), currently belonging to Museu de Zoologia da Universidade Estadual de Santa Cruz (MZUESC), Itabuna, Bahia.We also included in our analyses the data provided by Passos et al., (2012) from their two additional southeastern Brazilian specimens. Head measurements were taken with a digital caliper, with precision of 0.01 millimeter (mm). The snout-vent (SVL) and tail (TL) lengths were taken with a flexible ruler to the nearest millimeter. We consider the first ventral scale the anteriormost wider than taller scale that contacts gulars. Sex of individuals was determined by the presence/absence of hemipenes, checked through an incision at the base of the tail. Additional information from other four specimens from Passos et al., (2012) was included. Hemipenes were prepared using the techniques described by Pesantes (1994) and Zaher & Prudente (2003). Hemipenial terminology follows Dowling & Savage (1960) and Zaher (1999). Specimens from Cruz do Espírito Santo and Pedras de Fogo were collected under permissions number SISBIO 133/06 and 21799-1, respectively. CT-scanning procedures were conducted on a 300-kV μ-focus X-ray source micro computed tomography GE Phoenix v|tome|x M 300 (General Electric Measurement & Control Solutions, Wunstorf, Germany) at the Laboratório de Microtomografia of the Museu de Zoologia, Universidade de São Paulo. The acquired scan data was processed on a high-end computer HP Z820 workstation with eightcore Intel Xeon E5-2660, 2.20 GHz and 128 GB of memory. Reconstruction of raw data was performed using the system supplied software phoenix datos|x reconstruction v. 2.3.0 (General Electric Measurement & Control Solutions, Wunstorf, Germany). Three-dimensional visualization, segmentation, and analysis of the reconstructed data was performed using VGStudio MAX 2.2.3 64 bit (Volume Graphics GmbH, Heidelberg, Germany). DNA sequencing, phylogenetics and divergence assessment We sequenced the mitochondrial genes 12S (small subunit ribosomal RNA), 16S (large subunit ribosomal RNA), and cytb (cytochrome b), and the nuclear gene nt3 (Neurotrophin-3) of the holotype of the new species (MZUSP 19559) for which tissue samples were available. We used the molecular dataset available from Zaher et al., (2018), which already

included one specimen of C. amarali from municipality of Cananéia, state of São Paulo, Brazil (IBSP 72585), and added the representative of the northern population into the alignments by using the “--add" command in the online version of MAFFT v. 7 (Katoh et al., 2017) with default parameters. Genetic divergence between the two individuals of Caaeteboia was evaluated by taking into account the average divergence among species within the Xenodontinae. We used RAxML 8.2.3 (Stamatakis, 2014) to analyze our complete matrix, allowing PartitionFinder 2 to only apply GTR+G as the model of molecular evolution without any correction for proportion of invariant sites, as recommended in the RAxML’s manual. We performed the phylogenetic analysis employing Maximum Likelihood (ML) as the optimality criterion, running 1000 pseudoreplications of non-parametric bootstrap (BS) using the rapid bootstrap algorithm implemented in RAxML (-f a). Such approach, besides the bootstrap analysis, performs 200 complete searches for the best-scoring ML tree using each 5th bootstrap tree as a starting tree for the rapid hill-climbing search. Since the overlap among gene fragments was not complete in our dataset, we took the branch length/patristic distance (absolute time vs. mutation rate) among species as a proxy for the genetic distance. We used the package ape in the R environment to estimate the patristic distance. Results Our phylogenetic analysis (see Supplementary Material) recovered a clade containing the two specimens of Caaeteboia with unambiguous bootstrap support (100%). The analysis of the patristic distances within some genera of Xenodontinae (Fig. 2) indicate that mean value of interspecific distance among all genera is 0.091 (standard deviation of 0.045). The genus Xenopholis Peters, 1869 presents the highest interspecific distance mean (0.263), while the insular genus Borikenophis Hedges & Vidal in Hedges, Couloux & Vidal, 2009 presents the lowest interspecific distance mean (0.006). The genetic distance (estimated by the patristic distance) between the two specimens of Caaeteboia is 0.098. Considering our phylogenetic tree in combination with the estimated patristic distances and the analysis of morphological evidences (see below), we hypothesize that the specimens of genus Caaeteboia 221

G. Montingelli et al. - A second new species of genus Caaeteboia

Figure 2 . Graph comparing interspecific patristic distances among genera of Xenodontinae. Red line indicates the mean value and the orange lines the standard deviation of the mean.

from the northeastern region of Brazil represent an undescribed species, that we formally described herein. Caaeteboia gaeli sp. nov. urn:lsid:zoobank.org:act: urn:lsid:zoobank. org:pub:BFB360F0-28BA-48A1-A0D2-BDA4C658585B (Figs. 3, 4A–B, and 5) Caaeteboia sp. — Pereira-Filho et al., 2017: 170. Serpentes da Paraíba: diversidade e conservação. Holotype MZUSP 19559, an adult male from Mata do Açude Cafundó, Companhia São João, municipality of Cruz do Espírito Santo, state of Paraíba, Brazil 222

(07°10’57”S, 35°05’33”W), collected by Gindomar G. Santana on 1 March 2008 (field number: GGS 784). Right hemipenis prepared and deposited in the Hemipenial Collection of the Museu de Zoologia da Universidade de São Paulo (Fig. 6). Paratype CHUFPB 24395, an adult female from a forested fragment in the municipality of Pedras de Fogo, state of Paraíba, Brazil (07°25’28”S, 34°57’38.3”W), 27 km southwest from the type locality (Fig. 7), collected by Pedro R. A. Albuquerque in July 2018. Etymology The specific name honours Gael Hingst Zaher. GGM,

Cuad. herpetol. 34 (2): 219-230 (2020)

Figure 3. View of the holotype of Caaeteboia gaeli sp. nov. (MZUSP 19559). Upper left: dorsum; bottom left: venter; Upper, middle and bottom right: dorsal, lateral and ventral views of the head, respectively. Scale bars: 10 mm for the entire specimen, and 5 mm for the head.

FEB, GAPF, GGS, FGRF and FGG dedicate this species to the beloved son of the senior author, who sadly left us prematurely in March, 2020. Diagnosis Caaeteboia gaeli sp. nov. is diagnosed by a slender and small body; rounded pupil; eight supralabials (fourth and fifth contacting the orbit); nine infralabials (first to fourth contacting chinshields); loreal absent (fused with prefrontals); a preocular single and wide; two postoculars; temporals 2+2/1+2, or 2+1/2+1; dorsals 15/15/15; at least 158 ventrals, 92–106 paired subcaudals; anal plate divided; continuous dark-brown lateral stripe, bordered in black, extending from nasal, to the anterior portion of body, on rows of dorsals three and four, starting to fade after the10–15th ventrals, weakening towards the end of body; posterior to parietals, “V” shaped dark-mark, extending backwards and forming a weak vertebral stripe fading posteriorly; hemipenial lobes almost completely covered with calyces and naked area restricted to the small and poorly marked

lobular crotch, on the asulcate side; medial edges of lobes poorly demarcated and bordered with spines; lobular crest poorly developed, bearing small spines on its edge (Fig. 6A). Description of holotype Adult male, with a total length (TTL) of 389 mm, snout-vent length (SVL) 252 mm; tail length (TL) 137 mm (54% of SVL), head length (HL) 11.45 mm (4.5% of SVL), head width 6 mm (52% of HL), and head height 3.04 mm. Measurements corresponds to the right side of head. Interorbital distance 5.05 mm; rostro-orbital distance 3.77 mm; naso-orbital distance 2.54 mm. Head distinct from the neck, flattened in lateral view, and rounded in dorsal view. In lateral view, canthus rostralis is distinct, as well from dorsal view. Rostral sub-triangular, twice as long as high, 1.94 mm wide, 0.99 mm high, visible from above; internasal contacting nasal, 0.91 mm long, 1.03 mm wide; prefrontal 1.18 mm long, 1.68 mm wide; frontal sub-pentagonal, 3.2 mm long, 1.48 mm wide; 223

G. Montingelli et al. - A second new species of genus Caaeteboia

Figure 4. Coloration pattern of lateral stripes of specimens of Caaeteboia gaeli sp. nov. (A–B), and C. amarali (C–H), arranged geographically from northeast to southern Brazil. A: MZUSP 19559 (Holotype), Cruz do Espírito Santo, Paraíba; B: specimen not collected, Saloá, Pernambuco; C: CZGB 2371, Uruçuca, Bahia; D: IBSP 46140, Miracatu, São Paulo; E: IBSP 72585, Cananéia, São Paulo; F: IBSP 73202, Jacupiranga, São Paulo; G: IBSP 9907, Alexandra, Paranaguá, Paraná; and H: MNRJ R 1818, Santa Luzia, Tubarão, Santa Catarina. Scale bar: 5 mm.

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Cuad. herpetol. 34 (2): 219-230 (2020) 15/15/15 smooth dorsal scale rows; one preventral, 158 ventrals; anal plate divided; 106 paired subcaudals; caudal spine long and acuminate. Coloration Ground color of body light brown, with dark marks scattered on top of the head and a poorly defined brownish vertebral stripe on the anterior portion of the body that fades posteriorly (Figs. 3, 4A–B, and 5). Well-defined dark-brown lateral stripe, bordering supralabials dorsally and extending posteriorly, on the lateral side of the dorsum, on rows three and four. Ventrally, head and body immaculate whitish-cream, with a small dark spot on each edge of ventrals.

Figure 5. A: Caaeteboia gaeli sp. nov. (CHUFPB 24395 – paratype), from municipality of Pedras de Fogo, state of Paraíba (Photo: Gentil Filho); B: Specimen from Saloá (not collected), state of Pernambuco (Photo: Samuel Cardoso).

supraocular sub-rectangular, 2.96 mm long, 1.47 mm wide; parietal 4.06 mm long, 2.71 mm wide; nasal divided; pre-nasal contacting internasal, prefrontal, and the 1st supralabial, 0.51 mm wide, 0.64 mm high; post-nasal 0.63 mm wide, 0.69 mm high, contacting prefrontal and first and second supralabials; loreal fused with prefrontal, contacting 2nd and 3rd supralabials; preocular 0.62 mm long, 1.17 mm high; eye diameter 1.83 mm; pupil round, postoculars 2/2, upper postocular 0.61 mm long, 1.29 mm high; lower postocular reduced, 0.55 mm long, 0.36 mm high; temporals 1+1+2/1+2 on right and left sides, respectively; upper anterior temporal 0.89 mm long, 0.48 mm width; lower anterior temporal 1.44 long, 0.78 mm width. Supralabials 8/8 (fourth–fifth contacting the orbit), seventh and eighth higher than others; symphysal triangular, 0.85 mm long, 1.33 mm wide; infralabials 9/9, with the first to fourth contacting the first pair, and fourth–fifth contacting the second pair of chinshields; anterior chinshield 2.63 mm long, 0.94 mm wide; posterior chinshield 3.52 mm long, 1.19 mm wide; four gular scale rows,

Hemipenis Hemipenis fully everted and almost maximally expanded. Organ bilobed, semicapitate; semicalyculate; centrolineal sulcus spermaticus bifurcating on distal half of the body, ending on the apex of each lobe; capitulum about half of the size of the body, ornamented by papillate calyces uniformly distributed on sulcate surface and larger and irregular on asulcate side; small naked area restricted to the poorly marked lobular crotch on asulcate side; medial region of lobes poorly demarcated and bordered with spines; lobular crest poorly developed bearing small spines on its edge; hemipenial body and base covered by medium-sized spines, slightly larger on asulcate side; a series of enlarged or hook-like spines on laterals and two on the proximal region of the asulcate side of the body; base with two hook-like spines on the asulcate surface and one on the sulcate (Fig. 6A). Remarks on the Paratype An adult female (CHUFPB 24395; Fig. 6A); with 411 mm TTL, 279 mm SVL, 132 mm TL (47% of SVL), and 12.33 mm HL (4.4% of SVL). Loreal fused with prefrontals, contacting second and third supralabials; one large preocular; postoculars 2/2; supralabials 8/8 (4–5th contacting the orbit); 9/9 infralabials (first–fourth contacting chinshields) temporals 2+1/2+1, on right and left sides, respectively; 15/15/15 smooth dorsal scales; 158 ventrals; anal plate divided; 92 paired subcaudals. Coloration is very similar to the holotype. Comparisons Caaeteboia gaeli differs from C. amarali by the following combination of characters (values of C. 225

G. Montingelli et al. - A second new species of genus Caaeteboia with calyces and naked area restricted to the small and poorly marked lobular crotch on the asulcate side (vs. lobes covered with calyces on sulcate, asulcate and lateral sides, large naked area on the medial surface of lobes and large lobular crotch); medial edges of lobes poorly delimited and bordered with spines (vs. medial edges of lobes strongly delimited and bordered with spines); lobular crest poorly developed bearing small spines on its edge (vs. lobular crest strongly developed bearing enlarged spines on its edge); shorter proximal head of the quadrate and longer supratemporal with a free-ending posterior extremity projecting beyond the braincase (vs. wider proximal head of the quadrate and shorter supratemporal that does not project posteriorly in a free-ending extremity) (Fig. 7); contact between the maxilla and ectopterygoid reaching the level of the post-frontal (sensu Zaher and Scanferla, 2012) in lateral view (vs. maxilla-ectopterygoid contact does not reach the level of the postfrontal); longer angular, three times longer than high (vs. angular twice longer than high); pituitary vein foramen lying between the sphenoid and parietal (vs. pituitary vein clasped by the parietal, sphenoid and prootic). Figure 6. Sulcate (left) and asulcate (right) views of hemipenes. A: Caaeteboia gaeli sp. nov. (MZUSP 19559 – holotype), Cruz do Espírito Santo, Paraíba; B: C. amarali (IBSP 73202), Jacupiranga, São Paulo. Scale bar: 5 mm.

amarali between parenthesis; Table 1): 15/15/15 smooth dorsal scales (vs. 17/17/15 or 17/17/17); 158 ventrals (vs. 165–184); 92–106 paired subcaudals (vs. 112–124); well-defined dark lateral stripe (Fig. 4) extending posteriorly along the lateral sides of the body on rows three and four (vs. ill-defined dark ocular stripe, separate or poorly connected to the first of nearly ten dark blotches that occupies fourth, fifth and sixth rows; dark stripe absent on the body); hemipenial lobes (Fig. 6) almost completely covered

Remarks The specimen from Saloá, Pernambuco (Fig. 5B), although not collected, only handled and photographed in nature, exhibit characteristics that compelled us to consider it as a putative member of this new species. This individual shares with specimens of the genus Caaeteboia eight supralabials, with the fourth and fifth entering the orbit, loreal absent (fused with prefrontal), one preocular, two postoculars and 15 dorsals with no reduction. The dorsal coloration is very similar to the one described for both holotype and paratype of C. gaeli. It presents a continuous dark ocular stripe and does not exhibit dark lateral blotches on the anterior portion of the body as observed in specimens of C. amarali (Fig. 4) but instead a dark

Table 1. Selected characters of meristics and measurements of species of Caaeteboia gaeli sp. nov. and C. amarali. Caaeteboia gaeli sp. nov. SVL (mm)

Caaeteboia amarali

male

female

males

females

252

279

267–386 (n = 11)

298–365 (n = 2)

TL (mm)

137

132

147–202 (n = 10)

151 (n = 1)

HL (mm)

11.45

12.33

10.87–15.39 (n = 11)

12.22–14.43 (n = 2)

Ventrals

158

165–184 (n = 11)

165–171 (n = 2)

Subcaudals

106

113–125 (n = 10)

112 (n = 1)

Dorsals

226

15/15/15 (n = 2)

17/17/15 (n = 11), 17/17/17 (n = 2)

Cuad. herpetol. 34 (2): 219-230 (2020)

Figure 7. Ct-scan of the skull of Caaeteboia amarali (IBSP 73202, left), and Caaeteboia gaeli (MZUSP 19559, right).

stripe. The close geographic proximity between this sample and those from Paraíba also suggest that all individuals are co-specific. Distribution The distribution of the new species is currently known for three localities, two of them in Floresta de Tabuleiro (Tabuleiro Forest), and one in the submontane ombrophilous Atlantic Forest. The

holotype was collected in Mata do Açude Cafundó, Companhia São João, municipality of Cruz do Espírito Santo (Fig. 8A–D), while the paratype was found in a preserved area in the surroundings of the municipality of Pedras de Fogo, ca. 5 km westwards from Alhandra and 11 km northeast from Caaporã. The specimen from Saloá, Pernambuco, extends the distribution of the species of approximately 270 km southwestwards from the type-locality. This speci227

G. Montingelli et al. - A second new species of genus Caaeteboia Discussion

Figure 8. Habitat types where Caaeteboia gaeli was recorded. A–D: Aspects of the Tabuleiro forest at Mata do Cafundó, PB, and E–G: submontane ombrophilous forest at Saloá, PE.

men was observed in a small Atlantic Forest enclave within the Borborema Plateau (Fig. 8E–G), at an altitude above 700 m and 160 km from the coast towards the interior. Habitat and Natural History The predominant vegetational type where the holotype and paratype were captured is known as “Floresta de Tabuleiro” (Fig. 8). It consists of natural enclaves amidst the ombrophilous forest, characterized by an open-canopy forest with sandy soil, herbaceous vegetation and ground bromeliads, forming savanna-like patches along the low areas of the Northeastern Coast of the Atlantic Forest (between 20 and 100 m.a.s.l.) (Barbosa 2008). The photographed specimen from Saloá (Fig. 5B) occurs in a typical vegetation of submontane forest. The holotype was found within one of the mounted pitfall traps at 10:00 h, while the paratype was captured in activity on the forest floor at 10:15 h. The specimen from Saloá was found inside of a ground bromeliad during the day. 228

With the description of a second species, the diagnosis of Caaeteboia is slightly modified to include the variation observed here. Now, the genus is defined by the presence of eight supralabials, with the fourth and fifth entering the orbit; loreal scale absent (fused with prefrontal); a large and unique preocular, two postoculars; dorsals smooth, in rows of 17/17/15, 17/17/17 or 15/15/15; 158–184 ventrals; anal plate divided; 92–125 subcaudals; a dark lateral stripe that can be well or ill-defined, extending on the lateral of body, on rows three and four, or only connected to the first lateral blotch, not forming a continuous stripe. Variation on the dark lateral blotches may be observed among C. amarali. It can be occasionally fused to form a dark brown stripe anteriorly, a condition observed in the holotype. According to Passos et al., (2012: figs 5, 7), the holotype presents ill-defined blotches, not as high as those observed on the other specimens, restricted only to fourth and fifth rows. Another specimen of C. amarali (CZGB 2371) from the municipality of Uruçuca, Bahia, has also a similar condition. This is not the case observed in C. gaeli, which has a unique well-defined stripe from nostril to laterals of anterior portion of the body (Fig. 4). All remaining specimens of C. amarali exhibited lateral blotches, at least on the anterior portion of the body, on fourth, fifth and sixth rows. The geographic distribution of C. gaeli extends the range of the genus to the northeastern coastal Atlantic Forest, in the states of Paraíba and Pernambuco (Fig. 1). Therefore, Caaeteboia occurs along the Brazilian coastal areas of Atlantic Forest, from southern Santa Catarina (municipality of Tubarão) to northeastern Paraíba state (municipality of Cruz do Espírito Santo), with its westernmost record in Belo Horizonte, state of Minas Gerais (type-locality of C. amarali; Bérnils et al., 2004; Passos et al., 2012). The new species presents an allopatric distribution with C. amarali, with the nearest records of both species being actually distant from each other by approximately 700 kilometers (from the northern record of C. amarali at Uruçuca, Bahia to the southernmost putative record of C. gaeli at Saloá, Pernambuco). This distributional gap may be due to the rarity of both species, with very low densities throughout their natural range. Although the description of this species increases the diversity and the knowledge of Caaeteboia,

Cuad. herpetol. 34 (2): 219-230 (2020) it is still considered as a rare dipsadid genus with a broad distribution in one of the most impacted Brazilian biomes (Ribeiro et al., 2009). Finally, this new species reinforces the importance of conservation measures towards the small remnants of Atlantic Forest of Northeastern Brazil, which still harbors an impressive diversity and endemism, but remain largely unprotected (see MMA maps of the Conservation Units in Brazil, http://www.mma.gov.br/ areas-protegidas/cadastro-nacional-de-ucs/mapas) (Silva and Casteleti 2005; Tabarelli et al., 2005). Acknowledgements We are indebted to Samuel Cardoso for providing data and photographs of the specimen from Pernambuco, and Alberto Barbosa de Carvalho for scanning, segmenting, and producing the micro-ct images used in this study. We appreciate Alexandre R. Percequillo and anonymous reviewers for their comments and suggestions on the manuscript. We are also grateful to Francisco Franco and Valdir Germano (Instituto Butantan, São Paulo - IBSP), and Julio Cesar de Moura-Leite (Museu de História Natural Capão da Imbuia - MHNCI) for allowing us to examine specimens under their care. GGM and FEB was supported by a postdoctoral scholarship from Fundação de Amparo à Pesquisa do Estado de São Paulo (2012/09182-1 and 2012/09156-0). HZ was supported by a Researcher scholarship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (PQ-CNPq 301298/94-7). Funding for this study was provided by Fundação de Amparo à Pesquisa do Estado de São Paulo (BIOTA/FAPESP 2011/50206-9) to HZ. Literature cited

Barbosa, M.R.V. 2008. Floristic Composition of a Remnant of Atlantic Coastal Forest in João Pessoa, Paraíba, Brazil: 439457. In: Thomas, W.W. (ed.), The Atlantic Coastal Forest of Northeastern Brazil. The New York Botanical Garden Press, New York. Bérnils, R.S.; Moura-Leite, J.C. & Morato, S.A.A. 2004. Répteis: 499-536 In: Mikich S.B. & Bérnils R.S. (eds.), Livro Vermelho da Fauna Ameaçada no Estado do Paraná. Instituto Ambiental do Paraná, Curitiba. Dowling, H.G. & Savage, J.M. 1960. A guide to the snake hemipenis: a survey of basic structure and systematic characteristics. Zoologica 45: 17-28. Grazziotin, F.G.; Zaher, H.; Murphy, R.W.; Scrocchi, G.; Benavides, M.A.; Zhang, Y.P. & Bonato, S.L. 2012. Molecular phylogeny of the New World Dipsadidae (Serpentes: Colubroidea): A reappraisal. Cladistics 1: 1-23. Hedges, S.B.; Couloux, A. & Vidal, N. 2009. Molecular phylogeny, classification, and biogeography of West Indian

racer snakes of the Tribe Alsophiini (Squamata, Dipsadidae, Xenodontinae). Zootaxa 2067: 1-28. Katoh, K.; Rozewicki, J. & Yamada, K.D. 2017. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160-1166. Marques, O.A.V.; Eterovic, A. & Sazima, I. 2001. Serpentes da Mata Atlântica - Guia Ilustrado para a Serra do Mar. Holos. Ribeirão Preto. Passos, P.; Ramos, L. & Pereira, D.N. 2012. Distribution, natural history, and morphology of the rare snake Caaeteboia amarali (Serpentes, Dipsadidae). Salamandra 48: 51-57. Pereira-Filho, G.A; Vieira, W.L.; Montingelli, G.G.; Rodrigues, J.B.; Alves, R.R.N. & França, F.G.R. 2017. Diversidade: 55269 In: Pereira-Filho, G.A.; Vieira, W.L.S; Alves, R.R.N. & França F.G.R. (eds.), Serpentes da Paraíba. João Pessoa. Pesantes, O. 1994. A method for preparing hemipenis of preserved snakes. Journal of Herpetology 28: 93-95. Ribeiro, M.C.; Metzger, J.P.; Martensen, A.C.; Ponzoni, F.J. & Hirota, M.M. 2009. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142: 1141-1153. Silva, J.M.C. da & Casteleti, C.H.M. 2005. Estado da Biodiversidade da Mata Atlântica Brasileira: 43-59. In: Galindo-Leal C. & Câmara I.G. (eds.), The Atlantic Forest of South America: biodiversity status, threats, and outlook. Center for Applied Biodiversity Science and Island Press, Washington, D.C. Stamatakis, A. 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313. Tabarelli, M.; Pinto, L.P.; Silva, J.M.C.; Hirota, M.M. & Bedê, L.C. 2005. Desafios e oportunidades para a conservação da biodiversidade na Mata Atlântica brasileira. Megadiversidade 1: 132-138. Wettstein, O. 1930. Eine neue colubridae Schlange aus Brasilien. Zoologischer Anzeiger 88: 93-94. Zaher, H. 1999. Hemipenial morphology of the South American xenodontine snakes, with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. Bulletin of the American Museum of Natural History 240: 1-168. Zaher, H. & Prudente, A.L.C. 2003. Hemipenes of Siphlophis (Serpentes: Xenodontinae) and techniques of hemipenial preparation in snakes: a response to Dowling. Herpetological Review, 34:295-302. Zaher, H. & Scanferla, C.A. 2012. The skull of the Upper Cretaceous snake Dinilysia patagonica Smith-Woodward, 1901, and its phylogenetic position revisited. Zoological Journal of the Linnean Society 164: 194-238. Zaher, H.; Grazziotin, F.G.; Cadle, J.E.; Murphy, R.W.; MouraLeite, J.C. & Bonatto, S.L. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American xenodontines: a revised classification and descriptions of new taxa. Papéis Avulsos de Zoologia 49: 115-153. Zaher, H.; Yánez-Muñoz, M.H.; Rodrigues, M.T.; Graboski, R.; Machado, F.A.; Altamirano-Benavides, M.; Bonatto, S.B. & Grazziotin, F.G. 2018. Origin and hidden diversity within the poorly known Galápagos snake radiation (Serpentes: Dipsadidae). Systematics and Biodiversity16: 1-29. Zaher H.Z.; Murphy, R.W.; Arredondo, J.C.; Graboski, R.; Machado-Filho, P.R.; Mahlow, K.; Montingelli, G.G.;

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Ilha do Mel: MHNCI 2365. SANTA CATARINA: Itapema: IBSP 89902; Tubarão: district of Santa Luzia: MNRJ R 1818. SÃO PAULO: Cananéia: IBSP 72585; Caraguatatuba: IBSP 46701; Jacupiranga: IBSP 73202 (hemipenis prepared); Miracatu: Sítio Quatro Bocas: IBSP 46140.

Appendix 1 List of specimens examined Caaeteboia amarali (n = 13): BRAZIL: BAHIA: Ilhéus: MNRJ R 2997; Jussari: Conjunto Monte Serrat: CZGB 3386; Uruçuca: Lagoa: CZGB 2371, Fazenda Bonfim: MZUSP 20649. PARANÁ: Paranaguá: IBSP 18670, Alexandra: IBSP 9907,

Specimens from literature (Passos et al., 2012) Caaeteboia amarali (n = 4). BRAZIL: ESPÍRITO SANTO: Linhares: Reserva Biológica de Sooretama: MBML 56. RIO DE JANEIRO: Armação dos Búzios: IBSP 67331. SÃO PAULO: Caraguatatuba: IBSP 43050. SANTA CATARINA: Itapoá: MHNCI. © 2020 por los autores, licencia otorgada a la Asociación Herpetológica Argentina. Este artículo es de acceso abierto y distribuido bajo los términos y condiciones de una licencia Atribución-No Comercial 2.5 Argentina de Creative Commons. Para ver una copia de esta licencia, visite http://creativecommons.org/licenses/by-nc/2.5/ar/

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Cuad. herpetol. 34 (2): 231-237 (2020)

Trabajo

Diet of four lizards from an urban forest in an area of amazonian biome, eastern amazon Vinícius A. M. B. de Figueiredo, Naziel S. Souza, Jessica S. C. Anaissi, Patrick R. Sanches, Carlos E. Costa-Campos Universidade Federal do Amapá, Departamento de Ciências Biológicas e da Saúde, Laboratório de Herpetologia, Campus Marco Zero do Equador, 68903-419, Macapá, Amapá, Brazil.

Recibido: 10 Enero 2020 Revisado: 27 Abril 2020 Aceptado: 01 Agosto 2020 Editor Asociado: S. Valdecantos doi: 10.31017/CdH.2020.(2020-001)

ABSTRACT This study described the diet and niche overlap of four lizards from an urban fragment in Amapá state. The samplings were performed through pitfall traps and active visual search. In the stomach analysis, Formicidae and Coleoptera represented 50.79% of the total items. The highest niche overlap value was between Gonatodes humeralis and Tropidurus hispidus, which was not expected due to habitat use. The foraging strategies of all lizards observed have been previously mentioned by several authors. Several studies cite the diet of lizards being basically composed of invertebrates, with few variations, as also demonstrated in this study. Key words: Stomach composition; Niche overlap; Ecology. RESUMEN Este estudio describió la dieta y la superposición de nicho de cuatro lagartos de un fragmento urbano en el estado de Amapá. Los muestreos se realizaron a través de trampas y búsqueda visual activa. En el análisis estomacal, Formicidae y Coleoptera representaron el 50.79% del total de ítems. El valor de superposición de nicho más alto fue entre Gonatodes humeralis y Tropidurus hispidus, que no se esperaba debido a la diferencia en el uso del hábitat. La estrategia de alimentación de todos los lagartos observados ha sido mencionada anteriormente por varios autores. Varios estudios indican que la dieta de los lagartos se compone básicamente de invertebrados, con pocas variaciones, como también se demostró en este estudio. Palabras clave: Composición estomacal; Superposición de nicho; Ecología.

Introduction Some factors are related to the structuring of reptile communities, such as diversity, richness, and species composition (Pianka, 1967; 1974; Vitt and Zani, 1998). It is possible to consider interspecific competition and individual specialization as determining factors in structuring of a community, since there may be overlap in the use of resources between species (Pianka, 1973; Bolnick et al., 2003). Studies on the diet of lizards have increased over the last fifteen years and have contributed to a better understanding of species ecology and foraging strategies (Vitt et al., 1997a). These foraging strategies differ in several characteristics, such as the pattern of activity, presence of prey chemical detection, and diet composition, which can be considered as extreme points on a varying scale of foraging tactics.

Lizards are commonly classified into two categories according to the foraging strategy used: active foragers and sit-and-wait foragers (Huey & Pianka, 1981). There is also an intermediate type called errant foraging, which consists of changing hunting strategies according to opportunities and prey availability (Rocha, 1994). Foraging mode in lizards has been considered fundamental in interpreting ecological characteristics and natural history, such as the type and number of prey ingested (Vitt, 1991). In this paper, we describe the diet of a lizard assembly inserted in an urban forest of Amazonian biome, we calculated the niche breadth and niche overlap of species and we discuss the foraging strategies between them.

Author for correspondence: viniciusantonio31@gmail.com

231

V. A. M. B. de Figueiredo et al. - Diet of four lizards from an urban forest in Brazil Materials and methods Samplings were carried out on an urban area of forest fragment in the Campus Marco Zero of Universidade Federal do Amapá (00000’S, 51004’W), municipality of Macapá, Amapá state, Brazil. This area comprises 90 hectares and presents vegetation characterized by open areas and forest fragments (Fig. 1). The study was carried out from August 2011 to July 2012, monthly and lasting five days each, totaling 12 samplings. The individuals were captured through active visual search and pitfall traps, under a permit Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio/SISBIO number 31814-2). Five pitfalls arrays were Y-shaped (one central bucket linked to three peripheral ones, the three arms forming angles of approximately 120°) with 10 L buckets. Buckets belonging to the same pitfall array were connected by a 5 m long and 50 cm-high plastic drift fence. Pitfall arrays were set 150 m from one another along a transect, in order to provide spatially independent sample units (Greenberg et al., 1994; Cechin and Martins, 2000). Each pitfall array was sampled for a total of 15 consecutive days

in each month of sampling. For active searches, we delimited five transects of 1 km, separating them from each other by 50 m. These transects were traversed linearly and every 10 m of displacement, we shifted up to 5 m left and right to increase the coverage of the microhabitats used by the species (Heyer et al., 1994). In the laboratory, we euthanized the specimens with 2% liquid lidocaine, fixed in 10% formalin and preserved in alcohol at 70%. We removed the stomach contents of lizards and identified posteriorly the prey categories at the level of order and family using a stereomicroscope. Some preys were identified to the family level and others to the order level. Thus, when we talk about items that were identified to the family level, we are referring specifically to items that have been identified up to that taxonomic level. Preys were identified according to identification keys by �� Triplehorn and Johnson (2011) and Rafael et al. (2012). We measured the maximum length and width of all prey items to obtain the prey volume through the Ellipsoid Volume Formula, where V represents prey volume, l = item length e w = item width (Magnusson et al., 2003):

Figure 1. Urban fragment of forest located at the Universidade Federal do Amapá. Black circle: open area. White circles: forest fragment.

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Cuad. herpetol. 34 (2): 231-237 (2020)

We determined the Importance Value Index (IVI) of each prey category in the diet using the sum of the percentages of number (N%), frequency (F%) and volume (V%) (Gadsden & Palacios-Orona, 1997).

In addition, we calculated the trophic niche breadth through Levins’ Trophic Niche Amplitude Index (B) described by Pianka (1986). In this case, we considered the species as a specialist when the value of B is between 0 - 0.50, and values between 0.51 - 1.0 represent generalist individuals:

where B is the Levins index (niche breadth), n is the number of categories and p is the numerical or volumetric proportion of prey category i in the diet. We also analyzed niche overlaps by using EcoSim

Professional (Entsminger, 2014), to compare the mean observed niche overlap of the assemblage to mean simulated niche overlaps through RA3 (Gotelli and Graves, 1996; Entsminger, 2014). Results We recorded 84 individuals distributed in four families and four species (Fig. 2): Dactyloidae (Norops auratus (Daudin, 1802); n=22), Teiidae (Kentropyx striata (Daudin, 1802); n=25), Tropiduridae (Tropidurus hispidus (Spix, 1825); n=25) and Sphaerodactylidae (Gonatodes humeralis (Guichenot, 1855); n=12). Kentropyx striata was only captured in pitfall traps and G. humeralis only by active searches. Diet analysis Of the 84 specimens analyzed, 81 individuals (96.43%) had prey items in their gastrointestinal contents. In the stomach analysis, we identified 19 prey categories belonging to seven orders of Arthropoda (Araneae, Coleoptera, Diptera, Hemiptera, Hymenoptera, Isoptera and Orthoptera), a class of Myriapoda (Chilopoda) and a vertebrate group (Squamata). The most important preys based on the

Figure 2. Specimens of lizards recorded at urban area of forest fragment in the Campus Marco Zero of Universidade Federal do Amapá, municipality of Macapá, Amapá state, Brazil. (A) Norops auratus; (B) Kentropyx striata; (C) Tropidurus hispidus; (D) Gonatodes humeralis.

233

V. A. M. B. de Figueiredo et al. - Diet of four lizards from an urban forest in Brazil importance value index were Formicidae (31.71%) and Coleoptera (19.08%) (Table 1).

Table 2. Prey categories found in the stomach analysis of the Norops auratus (N= 22). N= number; F= frequency of prey; V= volume of prey; IVI= Importance Value Index.

Norops auratus (Daudin, 1802) Ninety-four items were found within nine prey categories (Table 2). Termites presented the higher importance value (25.39%) and ants were the second most representative (18.25%) in the diet. The standardized Levins’ index (Bsta) was 0.37.

Prey

IVI

Araneae

5.32

9.52

1.24

3.95

6.26

Chilopoda

1.05

2.38

0.19

0.60

1.35

Coleoptera

6.38

11.90

6.34

20.18

12.82

Diptera

5.32

9.52

7.29

23.21

12.68

Hemiptera

4.26

9.52

1.21

3.85

5.88

Kentropyx striata (Daudin, 1802) The diet included a variety of invertebrates and some small vertebrates. Of the 25 specimens collected, three individuals (12%) had no stomach contents. We identified 13 prey categories with one belonging to the vertebrate group (Table 3). The index of importance value showed that Coleoptera (26.46%) was more representative in the K. striata diet. The standardized Levins’ index (Bsta) was 0.48.

Formicidae

26.60

26.21

0.62

1.97

18.25

Isoptera

40.43

16.67

5.99

19.06

25.39

Tenebrionidae

4.26

2.38

1.54

4.90

3.85

Orthoptera

6.38

11.90

7.00

22.28

13.52

Total

100

31.42

100

Tropidurus hispidus (Spix, 1825) Twenty-five specimens of T. hispidus were collected Table 1. Prey categories recorded and general composition in the stomach analysis of the lizards. N= number; F= frequency of prey; V= volume of prey; IVI= Importance Value Index. Values and their relative percentages.

and all had stomach contents. We found 276 items within 16 prey categories (Table 4). Based on the importance value index, Formicidae (45.68%) and Coleoptera (17.45%) were the most important prey items. The standardized Levins’ index (Bsta) was 0.12. Gonatodes humeralis (Guichenot, 1855) This lizard consumed five different types of prey and all individuals had food items in their stomachs (Table 5). Coleoptera had the highest importance value index (28.89%) in the diet, followed by Hemiptera (24.86%). The standardized Levins’ index (Bsta) was 0.72.

Prey

IVI

Araneae

4.72

9.62

22.33

5.93

6.75

Chilopoda

0.21

0.64

0.19

0.05

0.30

Coleoptera

10.73

20.51

97.95

26.00

19.08

Diplopoda

0.21

0.64

2.17

0.58

0.48

Diptera

1.50

3.85

16.13

4.28

3.21

Eggs

0.43

1.28

3.17

0.84

0.85

Fruits

0.64

1.28

8.78

2.33

1.42

Prey

Hemiptera

4.29

10.90

26.16

6.95

7.38

Araneae

Pentatomidae

0.21

0.64

1.56

0.41

0.42

Coleoptera

189

40.56

23.72

116.23

30.86

31.71

Diplopoda

Vespidae

0.86

1.92

2.85

0.76

1.18

Eggs

Insecta larvae

4.94

2.56

7.17

1.90

3.13

Isoptera

105

22.53

7.69

20.46

5.43

11.89

Coccinellidae

0.43

0.64

2.49

0.66

0.58

Curculionidae

0.21

0.64

1.69

0.45

0.43

Tenebrionidae

1.07

1.28

3.41

0.91

1.09

Orthoptera

5.58

9.62

26.08

6.92

7.37

Sarcophagidae

0.21

0.64

6.43

1.71

0.85

Vertebrate Squamata

0.64

1.92

11.42

3.03

466

100

156

100

376.67

100

Formicidae

Total

234

Table 3. Food items found in the stomach analysis of the Kentropyx striata (N= 25). N= number; F= frequency of prey; V= volume of prey; IVI= Importance Value Index. F

IVI

16.25

17.95

11.19

12.22

15.47

13.73

25.66

36.61

39.97

26.46

1.25

2.56

2.17

2.37

2.06

1.25

2.56

2.35

2.57

2.13

Fruits

2.50

2.56

3.49

3.81

2.96

Hemiptera

2.50

5.13

0.82

0.90

2.84

Formicidae

7.50

5.13

0.19

4.28

Vespidae

1.25

2.56

2.03

2.22

2.01

Insecta larvae

8.75

7.69

7.06

7.71

8.05

Isoptera

20.00

5.13

3.04

3.32

9.48

Coccinellidae

2.50

2.56

2.49

2.72

2.59

Orthoptera

21.25

17.95

17.57

19.18

19.46

1.87

Vertebrate Squamata

1.25

2.56

2.58

2.82

2.21

100

Total

100

91.59

100

Cuad. herpetol. 34 (2): 231-237 (2020) Table 4. Prey categories found in the stomach analysis of the Tropidurus hispidus (N= 25). N= number; F= frequency of prey; V= volume of prey; IVI= Importance Value Index. Prey

IVI

Araneae

1.09

4.69

5.34

2.24

2.67

Coleoptera

9.78

20.31

53.00

22.28

17.45

Diptera

0.72

3.13

8.84

3.71

2.52

Eggs

0.36

1.56

0.82

0.34

0.76

Fruits

0.36

1.56

5.29

2.22

1.38

Hemiptera

4.35

14.06

17.27

7.26

8.56

Pentatomidae

0.36

1.56

0.66

0.86

Formicidae

154

55.80

32.81

115.28

48.43

45.68

Vespidae

1.09

3.13

0.82

0.34

1.52

Insecta larvae

5.80

1.56

0.11

0.05

2.47

Isoptera

17.39

3.13

9.36

3.93

8.15

Tenebrionidae

0.36

1.56

1.87

0.79

0.90

Curculionidae

0.36

1.56

1.69

0.71

0.88

Orthoptera

1.09

4.69

1.51

0.63

2.14

Sarcophagidae

0.36

1.56

6.43

2.70

1.54

Vertebrate Squamata

0.72

3.13

8.84

3.71

2.52

276

100

238.03

100

Total

Diet overlaps ranged from 0.44 (K. striata and T. hispidus) to 0.71 (G. humeralis and T. hispidus) (Table 6). The highest values of diet overlap were found among species that preferentially feed on Coleoptera (G. humeralis and K. striata) and Formicidae (T. hispidus and N. auratus). Food niche breadth ranged between 0.72 (G. humeralis) to 0.12 (T. hispidus). Discussion This study showed that the lizards sampled were mainly insectivorous. Coleoptera was the most important item in the diets of Gonatodes humeralis and

Table 5. Prey categories found in the stomach analysis of the Gonatodes humeralis (N=12). N= number; F= frequency of prey; V= volume of prey; IVI= Importance Value Index. Prey

IVI

Araneae

6.25

9.09

4.56

29.17

14.84

Coleoptera

37.50

36.37

2.00

12.80

28.89

Formicidae

25.00

27.27

0.14

0.90

17.72

Hemiptera

12.50

18.18

6.86

43.89

24.86

Isoptera

18.75

9.09

2.07

13.24

13.69

Total

100

15.63

100

Kentropyx striata and Formicidae for Tropidurus hispidus. This food preference is reported in the diet of congeners of lizards studied here, suggesting a niche pattern with respect to diet (Vitt, 1991; Miranda & Andrade, 2003; Ferreira et al., 2017). The low number of ants in the diet of K. striata is not expected, considering that ants are among the most abundant arthropods in the Amazon region. Vitt et al. (2011) proposed that the low number of ants found in the diet of K. altamazonica, would be due to the ability of teiid lizards to discriminate prey by chemical cues. This could apply to this study, in which ants did not present significant values in the prey spectrum of K. striata. On the other hand, this food item was the most frequent in the diet of T. hispidus, which is consistent with other studies within the Tropidurus genus (Colli et al., 1992; Perez-Mellado, 1993; Van Sluys, 1993; Fialho et al., 2000; Van Sluys et al., 2004; Kolodiuk et al., 2010). The consumption of other vertebrates by T. hispidus and K. striata was recorded in this study, which has been observed in several studies in the genus Tropidurus (Ribeiro and Freire, 2011; Siqueira et al., 2013) and Kentropyx (Vitt and Carvalho, 1995; Vitt et al., 2011; Franzini et al., 2017), that also documented the consumption of frogs and lizards. Regarding foraging strategies, it had already been suggested the sit-and-wait foraging strategy for G. humeralis (Huey and Pianka, 1981) and T. hispidus (Ferreira et al., 2017), the active foraging for K. striata (Vitt, 1991) and opportunistic tactics for Norops auratus (Vitt et al., 2003). In relation to niche breadth, T. hispidus consumed the largest number of prey among the sampled species and showed the lowest value, being considered the most specialist lizard in this study. This characteristic indicates ants specialist habits, which has already been reported in other Tropidurus Table 6. Dietary Niche overlap values between sampled species in an urban area of a forest fragment in the Campus Marco Zero of Universidade Federal do Amapรก, municipality of Macapรก, Amapรก state, Brazil. Kentropyx striata

Norops auratus

Tropidurus hispidus

Gonatodes humeralis

0.70

0.69

0.71

Kentropyx striata

---

0.67

0.44

---

0.70

Species

Norops auratus

235

V. A. M. B. de Figueiredo et al. - Diet of four lizards from an urban forest in Brazil species (Fialho et al., 2000; Kolodiuk et al., 2010; Ribeiro and Freire, 2011). K. striata also showed a narrow niche breadth value, representing a specialized diet, with Orthoptera being the most abundant prey category, similar to found for K. altamazonica (Vitt et al., 2001) and K. calcarata (Vitt, 1991). The low consumption of ants by teiid lizards is expected (Acosta and Martori, 1990; Schall, 1990; Vitt and Carvalho, 1995; Vitt and Zani, 1996) and is similar to found in our observation. Previous studies also cite niche breadth values similar to those found in our study for G. humeralis (Vitt et al., 1997b; 2000). The low consumption of termites observed here by this species was expected and has been recorded by Miranda and Andrade (2003) in a population of G. humeralis from Maranhão, since this lizard is a sit-and-wait forager and termites are clumped and unpredictably distributed prey (Huey and Pianka, 1981). The niche breadth and importance value index of N. auratus indicated termites specialist, but this is not consistent with previous studies on Norops species, which mentioned other types of prey as dominant food items, such as ants and spiders (Vitt et al., 2008; Mesquita et al., 2015). Teixeira and Giovanelli (1999), studied the ecology of T. torquatus and concluded that this species invests in small and aggregate prey in order to save energy. This could explain the fact that N. auratus and T. hispidus ingested large quantities of termites. Another explanation would be the abundance of these invertebrates in the studied environment, but this statement is only speculative because we did not carried out a study to evaluate it. Regarding food overlap, the overlap value between N. auratus and K. striata does not reflect direct competition. Teiids, in general, are heliothermic, using forest borders, which receive more direct sunlight (Vitt and Colli, 1994), whereas Norops uses the leaf litter of the forest floor. The high overlap of G. humeralis with three of the studied species suggests a similarity in the diets. This is not expected, since this lizard was the only species to be recorded in the forest area and foraging strategies differ among individuals. Shenbrot et al. (1991), suggested that the greater niche overlap of lizards was due to body size differentiation. This could explain the high niche overlap in our case, showing that body size may contribute to the coexistence of sympatric species, despite the microhabitat use be considered a predominant factor allowing coexistence within lizards assemblages. 236

Typically, natural history data forms the basis for understanding relationships between species. The processes that organize lizard assemblages are complex and include historical and current factors. The high prey availability allows a large overlap and the use of shared resources indicated that assemblage of lizards studied does not appear to be trophically structured. We encourage other studies capable of classifying the variables identified here, with sufficient data to allow appropriate comparisons. Acknowledgments We would like to thank Departamento de Pesquisa and Laboratório de Herpetologia, Universidade Federal de Amapá for logistical support. NSS thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (PIBIC/CNPq) for his research fellowship. Literature cited

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Trabajo

Correlation between the granulosa cell layer and active caspase-3 expression in ovarian follicles of Tropidurus hispidus and T. semitaeniatus (Squamata, Tropiduridae): immunohistochemical approach Hellen da Silva Santos1, Vanúzia Gonçalves Menezes2, Eliza Maria Xavier Freire3, Maria Helena Tavares de Matos2, Leonardo Barros Ribeiro1 Universidade Federal do Vale do São Francisco, Campus Ciências Agrárias, BR 407, Km 12, Lote 543, Projeto de Irrigação Nilo Coelho – S/N, C1, Núcleo de Ecologia Molecular, Laboratório de Morfofisiologia, CEP 56.300-000, Petrolina, PE, Brazil. 2 Universidade Federal do Vale do São Francisco, Campus Ciências Agrárias, BR 407, Km 12, Lote 543, Projeto de Irrigação Nilo Coelho – S/N, C1, Laboratório de Biologia Celular, Citologia e Histologia, CEP 56.300-000, Petrolina, PE, Brazil. 3 Universidade Federal do Rio Grande do Norte, Campus Universitário Lagoa Nova, Centro de Biociências, Departamento de Botânica e Zoologia, Laboratório de Herpetologia, CEP 59072-970, Natal, RN, Brazil. 1

Recibido: 02 Junio 2020 Revisado: 20 Agosto 2020 Aceptado: 25 Agosto 2020 Editor Asociado:

J. Goldberg

doi: 10.31017/CdH.2020.(2020-051)

ABSTRACT The greatest threats to terrestrial reptiles are urban development and habitat modification. In this sense, a better understanding of folliculogenesis in these animals would be important to knowledge of reproductive biology. The aim of this study was to analyze the correlation between the thickness of the granulosa cell layer and the expression of the active caspase-3 protein in the previtellogenic and vitellogenic follicles of T. hispidus and T. semitaeniatus. Ovaries were used for histological (morphology and morphometry: thickness of granulosa layer) and immunohistochemical (active caspase-3 expression) analyses. The previtellogenic follicles of T. hispidus and T. semitaeniatus showed a thicker granulosa layer, with pyriform and small cells. The vitellogenic follicles had a monolayer of cuboid cells, and a thicker thecal layer. The thickness of the granulosa layer was significantly higher in the previtellogenic compared to the vitellogenic phase for both species. However, no differences were observed between the species. Active caspase-3 was observed in the pyriform and intermediate cells in previtellogenesis of T. hispidus and T. semitaeniatus. Nevertheless, no immunostaining was observed in the vitellogenic phase in both species. In conclusion, this study shows that the thickness of the granulosa cell layer is higher in the previtellogenic follicles compared to the vitellogenic follicles in the two Tropidurus species. Pyriform and intermediate cells from previtellogenic follicles show high expression of the protein, indicating that remodeling of the epithelium is associated with apoptosis. Finally, our results provide a scientific basis for assisted reproductive techniques and conservation actions to the reptiles in the future. Key words: Apoptosis; Epithelium; Folliculogenesis; Lizards; Pyriform cells. RESUMEN Las mayores amenazas para los reptiles terrestres son el desarrollo urbano y la modificación del hábitat. En este sentido, una mejor comprensión de la foliculogénesis en estos animales sería importante para el conocimiento de la biología reproductiva. El objetivo de este estudio fue analizar la correlación entre el grosor de la capa de células de la granulosa y la expresión de la proteína caspase-3 activa en los folículos previtelogénicos y vitelogénicos de T. hispidus y T. semitaeniatus. Los ovarios se usaron para análisis histológicos (morfología y morfometría: grosor de la capa de la granulosa) e inmunohistoquímicos (expresión activa de caspase-3). Los folículos previtelogénicos de T. hispidus y T. semitaeniatus mostraron una capa de granulosa más gruesa, con células piriformes y pequeñas. Los folículos vitelogénicos tenían una monocapa de células cuboides y una capa tecal más gruesa. El grosor de la capa de granulosa fue significativamente mayor en la fase previtelogénica en comparación con la fase vitelogénica para ambas especies. Sin embargo, no se observaron diferencias entre las especies. Se observó caspase-3 activa en las células piriformes e intermedias en previtelogénesis de T. hispidus y T. semitaeniatus. Sin embargo, no se observó inmunotinción en la fase vitelogénica en ambas

Author for correspondence: leonardo.ribeiro@univasf.edu.br

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H. S. Santos et al. - Active caspase-3 expression in ovarian of lizards especies. En conclusión, este estudio muestra que el grosor de la capa de células de la granulosa es mayor en los folículos previtelogénicos en comparación con los folículos vitelogénicos en las dos especies de Tropidurus. Las células piriformes e intermedias de folículos previtelogénicos muestran una alta expresión de la proteína, lo que indica que la remodelación del epitelio está asociada con la apoptosis. Finalmente, nuestros resultados proporcionan una base científica para técnicas de reproducción asistida y acciones de conservación para los reptiles en el futuro. Palabras clave: Apoptosis; Epitelio; Foliculogénesis; Lagartos; Células piriformes.

Introduction Lizards in the family Tropiduridae, particularly of the genus Tropidurus, are distributed along South America, and widely found in Brazil (Avila-Pires, 1995; Novaes-e-Silva and Araújo, 2008; Vitt et al., 2008), especially in the Caatinga biome (Ribeiro and Freire, 2011). Among the tropidurid lizards, Tropidurus hispidus (Spix, 1825) and Tropidurus semitaeniatus (Spix, 1825) feed on arthropods, small vertebrates, and plant material (Ribeiro and Freire, 2011; Guedes et al., 2017; Pergentino et al., 2017), and serve as prey for invertebrates, such as spiders (Vieira et al., 2012), and for vertebrates as snakes and other lizards (Silva et al., 2013; Mikalauskas et al., 2017). The temporal pattern of reproduction in Squamata in tropical regions is often associated with limiting environmental conditions, such as rainfall (Van Sluys et al., 2002; Ávila et al., 2008; Santos et al., 2015), decreasing or ceasing the reproductive activities during the dry season (Fitch, 1982; Ribeiro et al., 2012). The greatest threats to terrestrial reptiles are thought to be agriculture, logging and harvesting followed by urban development and habitat modification (Böhm et al., 2013). The development and implementation of genome banking strategies may be the only mechanism to prevent loss of genetic diversity and extinction in many reptile species in the future. Therefore, the acceleration of the biodiversity crisis is generating an imperative to develop assisted reproductive techniques to the reptiles (Clulow and Clulow, 2016). In this sense, a better understanding of folliculogenesis in these animals would be important to both the knowledge of reproductive biology and to provide a scientific basis for conservation actions (Ramírez-Bautista et al., 2000; Young et al., 2014). The different phases of folliculogenesis (previtellogenic, vitellogenic, post-ovulatory or luteal phase, and follicular atresia) have already been characterized in some species of squamate reptiles 240

such as Hemidactylus mabouia (Moreau de Jonnès, 1818) (Moodley and Van Wyk, 2007), Sceloporus grammicus Wiegmann, 1828 (Lozano et al., 2014), and T. hispidus and T. semitaeniatus (Santos et al., 2015). The morphological changes in the granulosa and thecal layer, and in the ooplasm observed in the ovarian follicles during folliculogenesis were associated with vitellus deposition in lizards H. mabouia (Moodley and Van Wyk, 2007), T. hispidus and T. semitaeniatus (Santos et al., 2015). At the end of previtellogenesis, the follicular epithelium undergoes remodeling and the intermediate and pyriform cells regress via apoptosis (Motta et al., 1996). Apoptosis is the main mechanism for the elimination of unnecessary cells during development and homeostasis in normal tissue (Liu et al., 2017), and is mediated by a class of cysteine proteases called caspases (McIlwain et al., 2013). Caspase-3 is a major executioner caspase that is cleaved at an aspartate residue to form the active caspase-3 enzyme (O’Donovan et al., 2003). Active caspase-3 degrades multiple cellular proteins and is responsible for morphological changes (cell size reduction, cytoplasm condensation, membrane blebbing) and DNA fragmentation in cells during apoptosis (Hussein, 2005; McIlwain et al., 2013). Recently, Tammaro et al. (2017) have demonstrated that the proform caspase-3 protein is present in previtellogenic follicle cells in the lizard Podarcis siculus (Rafinesque-Schmaltz, 1810). Their data indicated that the enzyme produced is maintained in the inactive proform until the end of the nurse function, and thereafter, activation occurs with consequent cell regression. However, there are no reports correlating intermediate and pyriform cell regression via apoptosis and the expression of active caspase-3 in T. hispidus and T. semitaeniatus. Therefore, the aim of this study was to examine whether there is a correlation between histological (thickness of the granulosa cell layer) and functional

Cuad. herpetol. 34 (2): 239-246 (2020) attributes (apoptosis, i.e. expression of the active caspase-3 protein) in the ovarian follicles of the lizards T. hispidus and T. semitaeniatus during the previtellogenic and vitellogenic phases. Materials and methods Source of ovarian tissue Lizards from T. hispidus and T. semitaeniatus species were collected from the Ecological Station of Seridó (ESEC Seridó), Serra Negra do Norte municipality, state of Rio Grande do Norte, between October 2006 and May 2008. The specimens were dissected and their ovaries were removed and fixed in Bouin’s solution for 4-6 h. Thereafter, histological and immunohistochemical analyses were performed at the Cell Biology/Cytology and Histology Laboratory of the Agrarian Sciences Campus of the Universidade Federal do Vale do São Francisco, Petrolina, state of Pernambuco. Histological and morphometric analyses A total of 30 pairs of ovaries (15 pairs for each species) were dehydrated using increasing concentrations of ethanol (Dinâmica, São Paulo, Brazil), clarified in xylene (Dinâmica) and embedded in paraffin (Dinâmica). The ovarian tissue was cut into 7 μm sections, and every section was mounted on glass slides and stained with hematoxylin and eosin (Vetec, São Paulo, Brazil). The slides were evaluated by light microscopy (Nikon, Tokyo, Japan; 400x magnification) and the images were obtained by using the Scope photo® software. For morphological analysis, structures such as the granulosa and thecal layer cells, the vitelline membrane and the vitelline reservoir in the ooplasma were observed. The arrangement of these structures allowed us to determine the phases of folliculogenesis in these lizards (Santos et al., 2015). Only the follicles that showed intact granulosa cell layer and theca cells were analyzed. Thereafter, morphological analysis was performed using 20 follicles for each species (10 follicles for the previtellogenic phase and 10 for the vitellogenic phase). The thickness of the granulosa cell layer was measured by using the Image-Pro Plus® software. The follicles used for morphological and morphometric analyses were further used for immunohistochemistry assay. Immunohistochemistry Immunohistochemistry was performed according to

previous studies (Barberino et al., 2017) with some modifications. Sections (5 μm thick) from each block were cut using a microtome (EasyPath, São Paulo, Brazil) and mounted in Starfrost glass slides (Knittel, Braunschweig, Germany). The slides were incubated in citrate buffer (Dinâmica) at 95°C in a deckloaking chamber (Biocare, Concord, USA) for 40 min to retrieve antigenicity, and endogenous peroxidase activity was prevented by incubation with 3% H2O2 (Dinâmica) and methyl ethanol (QEEL, São Paulo, Brazil) for 10 min. Non-specific binding sites were blocked using 1% normal goat serum (Biocare) and diluted in phosphate-buffered saline (PBS; Sigma Aldrich Chemical Co., St. Louis, MO, USA). Subsequently, the sections were incubated in a humidified chamber for 90 min at room temperature with polyclonal anti-activated caspase-3 (pro apoptotic protein; 1:50; Santa Cruz Biotechnology). Thereafter, the sections were incubated for 30 min with MACH4 Universal HRP-polymer (Biocare). Protein localization was demonstrated with diaminobenzidine (DAB; Biocare), and the sections were counterstained with haematoxylin (Vetec) for 1 min. Negative control (reaction control) underwent all steps except the primary antibody incubation. Images were acquired and files were saved in tagged-image file format (TIFF). Thereafter, the images were converted in RGB color model (it combines three primary colors, red, green, and blue, in various ways to create other colors; Liu et al., 2006) by using the Adobe Photoshop® software (CC 2017 v18.0). Next, the RGB images were analyzed by using Image J software, and color separation was performed by automatically thresholding red-, green-, and bluefiltered gray-scale values of the image. This technique was applied to separate and differentially analyze DAB (brown)-stained antigen-positive cells/areas from hematoxylin (blue)-counterstained cells/areas (Ruifrok, 1997). The selected areas were then analyzed (number of pixels) by using Image-Pro Plus®. Statistical analysis Data from the thickness of the granulosa cell layer (µm) in the phases of folliculogenesis were submitted to ANOVA and t-test for both intra- and interspecific comparisons. Spearman’s correlation coefficient was used to verify the relationship between the thickness of the granulosa cell layer and active caspase-3 expression (pixels). The differences were considered to be statistically significant when P < 0.05.

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H. S. Santos et al. - Active caspase-3 expression in ovarian of lizards Results Morphological and morphometrical analysis of ovarian follicles The ovarian follicles of T. hispidus and T. semitaeniatus were composed of an oocyte, granulosa and theca cells. The previtellogenic phase showed a thicker granulosa layer, which was characterized by the presence of pyriform cells (Fig. 1A) and intermediate cells. Small cells next to the vitelline membrane can also be observed (Fig. 1A). The granulosa layer is thinner in the vitellogenic phase, which showed a single layer of cuboid cells, contrasting with a thicker thecal layer (Fig. 1B). The thickness of the granulosa cell layer was significantly higher in the pre-vitellogenic phase compared to the vitellogenic phase for both T. hispidus and T. semitaeniatus (P < 0.05, Table 1). However, no differences (P > 0.05) were observed between the species in both phases (pre-vitellogenic and vitellogenic). Expression of active caspase-3 in the ovary Immunohistochemistry analysis demonstrated the presence of active caspase-3 in the cytoplasm of pyriform cells (Fig. 2A, C and E) and intermediate cells (Fig. 2A, 3A, B and C) in follicles of the previtellogenic phase of T. hispidus and T. semitaeniatus. The intensity of immunostaining was 82.37 and 83.35 pixels for T. hispidus and for T. semitaeniatus, respectively. Nevertheless, no immunostaining was observed in any follicle in the vitellogenic phase in

both species (Fig. 2B, D and F). As the pyriform cells regressed, the intensity of active caspase-3 expression in the granulosa layer also decreased as a result of a gradual reduction of this protein. This finding could be observed in Figure 3B and C, which highlight the presence of the remaining intermediate cells of late previtellogenesis epithelium. However, although not statisticallyÂ significant (P = 0.05),Â correlation between the thickness of granulosa layer and the intensity of protein expression (in pixels) was inversely proportional (T. hispidus: r = -0.3952, P = 0.2582; T. semitaeniatus: r = -0,6833, P = 0.290). The negative control is shown in figure 3D. Discussion This study showed that the thickness of the granulosa cell layer is higher in the pre-vitellogenic phase compared to the vitellogenic phase for both T. hispidus and T. semitaeniatus. Moreover, to our knowledge, this is the first study that demonstrates the expression of active caspase-3 protein in lizards. The protein was localized in previtellogenic follicular epithelia of the ovarian follicles of T. hispidus and T. semitaeniatus. Four different phases of folliculogenesis have already been characterized for T. hispidus and T. semitaeniatus: previtellogenic, vitellogenic, postovulatory or luteal phase, and follicular atresia (Santos et al., 2015). In this study, our purpose was to focus attention on issues related to the previtellogenic and vitellogenic follicles. At the beginning of

Figure 1. Ovarian follicle morphology in Tropidurus semitaeniatus: Polymorphic and multilayered epithelium with pyriform (PyC) and small cells (SC) in previtellogenic phase (A); the epithelium is composed by a single layer of small cuboid cells (SC) in the vitellogenic phase (B). T: theca layer, YM: yolk membrane, Oop: ooplasm. Scale bar: 40 Âľm.

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Cuad. herpetol. 34 (2): 239-246 (2020) Table 1. Thickness of the granulosa cell layer (mean ± SD) of ovarian follicles of Tropidurus hispidus and Tropidurus semitaeniatus. Follicular phase

Thickness of the granulosa cell layer (µm) Tropidurus hispidus

Tropidurus semitaeniatus

Previtellogenic

44.02 ± 5.40A

35.77 ± 8.98A

Vitellogenic

16.65 ± 7.85B

19.43 ± 5.21B

(A, B) Different letters in the same column indicate significant differences (P < 0.05).

the previtellogenic phase, the small cells from the granulosa layer start to differentiate, originating the intermediate cells and, following a further differentiation, into pyriform cells (Maurizii et al., 1997; Maurizii et al., 2000). In this phase, these pyriform cells, also called nurse cells, are responsible for the nutrition of the oocyte by sending it mRNA and organelles. Moreover, the vitellogenin, produced in the liver and carried via the circulation to the ovary, traverses the granulosa pyriform cells through an extracellular route (Klosterman, 1987), reaching the oocyte for future nutrition of the embryo to be developed (Santos et al., 2015). By the end of previtellogenesis, pyriform cells transfer most of their cytoplasm and organelles to the growing oocyte, undergo an apoptotic process comprising chromatin clumping and internucleosomal fragmentation and regress (De Caro et al., 1998). Therefore, in this study, regression of pyriform and intermediate cells could explain the lowest thickness of the granulosa cell layer in the vitellogenic phase compared to the previtellogenic phase observed for both species (T. hispidus and T. semitaeniatus). Similar result was demonstrated for the oviparous lizard H. mabouia (Moodley and Van Wyk, 2007). To confirm the hypothesis that apoptosis was associated with regression of the pyriform and intermediate cells, we further evaluated active caspase-3 expression. Caspase-3 activation is necessary for initiation of apoptosis and regulation of processes such as membrane blebbing and internucleosomal DNA fragmentation (Hussein, 2005; McIlwain et al., 2013). In this study, active caspase-3 was immunolocalized only in the granulosa cells of the previtellogenic follicles of T. hispidus and T. semitaeniatus. A previous study has also shown that the proform caspase-3 protein is present in previtellogenic follicular epithelia in the lizard P. siculus (Tammaro et al., 2017). Moreover, these authors reported that mRNA

for caspase-3 is produced during the stem phase and stocked in the cell cytoplasm of small cells until differentiation in the pyriform nurse cells begins. These cells translate messengers but the enzyme produced is maintained in the inactive proform until the end of the nurse function. When the follicle reaches a diameter of about 1500 μm, it starts preparing for vitellogenesis and the epithelium becomes thinner in order to facilitate the uptake of vitellogenin by the oocyte (Motta et al., 1996). At this time, the proform caspase-3 is activated with consequent pyriform cell regression (Tammaro et al., 2017). These pyriform cells acquire the morphology typical of an apoptotic cell with chromatin being sent to the margin and condensed, plus membrane blebbings (Motta et al., 1996). In agreement with these findings, we showed that pyriform cells undergo apoptosis at the end of previtellogenesis, which can be confirmed by the high intensity of active caspase-3 expression in these cells. Moreover, as the pyriform and intermediate cells regress with the progress of folliculogenesis, we did not observe expression of active caspase-3 in the vitellogenic follicles, thus, resulting in a follicular epithelium formed by a monolayer of small follicle cells, as previously reported in the lizard P. siculus (Motta et al., 1995). The different fate of the cellular constituents could be a fundamental event that sustains the differentiation of both epithelium and oocyte in the lizards T. hispidus and T. semitaeniatus. It is important to note that most research on lizard female reproduction has focused on the morphology of ovarian follicles (Klosterman, 1987; Motta et al., 1995; Maurizii et al., 2000; Lozano et al., 2014; Santos et al., 2015), whereas we have compared morphological and functional attributes (using a specific marker for apoptosis) in the follicles. As lizards, such as T. hispidus and T. semitaeniatus, provide valuable models for studies in ecology and evolution and offer a useful comparison for studies on other vertebrates (Hare and Cree, 2010), understanding their reproductive biology is the key to effectively use of genome storage for reptile conservation. Collectively, our data shows that the thickness of the granulosa cell layer is higher in the previtellogenic follicles compared to the vitellogenic follicles for both T. hispidus and T. semitaeniatus. Moreover, pyriform and intermediate cells from previtellogenic follicles show high expression of the active caspase-3 protein, indicating that the remodeling of the epithelium is associated with apoptosis, which could be the result of a functional adaptation in these spe243

H. S. Santos et al. - Active caspase-3 expression in ovarian of lizards

Figure 2. Active caspase-3 localization in follicular epithelial cells of lizards. Pyriform (PyC) and intermediate cells (IC) of previtellogenic follicles of Tropidurus hispidus are intensely labeled (A). Vitellogenic epithelium of Tropidurus semitaeniatus showing small cells (SC) without immunostaining (B). Note that theca cells are unlabeled in both phases of folliculogenesis (A and B). The same follicles (previtellogenic and vitellogenic follicles) after color separation to highlight DAB (brown)-stained antigen-positive cells/areas (C and D). Images were converted in a gray scale by using threshold toolÂ to quantify the intensity (pixels) of the active caspase-3 expression (E and F). Arrows indicate positivity for active caspase-3 (A and C). T: Theca layer; Oop: Ooplasma. Scale bar: 40 Âľm.

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Figure 3. Immunolocalization of active caspase-3 in follicular epithelial cells of Tropidurus hispidus in the previtellogenic phase (A), highlighting that with the progression of pyriform cells regression, the intensity of protein expression reduced (B and C). Negative control (D). Arrows indicate greater positivity for active caspase-3 in intermediate cells. IC: Intermediate cells; SC: Small cells; T: Theca layer; Oop: Ooplasma. Scale bar: 40 µm.

cies. Finally, our results provide a scientific basis for assisted reproductive techniques and conservation actions to the reptiles in the future. Acknowledgements We thank the Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis (IBAMA) for the specimen collection licenses (collection permit 206/2006 and Process 02001.004294/03-15). HSS holds a scholarship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and MHTM is supported by a grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Literature cited

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H. S. Santos et al. - Active caspase-3 expression in ovarian of lizards Motta, C.M.; Scanderberg, M.C.; Filosa, S. & Andreuccetti, P. 1995. Role of pyriform cells during the growth of oocytes in the lizard Podarcis sicula. Journal of Experimental Zoology 273: 247-256. Motta, C.M.; Filosa, S. & Andreuccetti, P. 1996. Regression of the epithelium in late previtellogenic follicles of Podarcis sicula: a case of apoptosis. Journal of Experimental Zoology 276: 233-241. Novaes-e-Silva, V. & Araújo, A.F.B. 2008. Ecologia dos lagartos brasileiros. Technical Books, Rio de Janeiro. O’Donovan, N.; Crown, J.; Stunell, H.; Hill, A.D.; McDermott, E. & O’Higgins, N. 2003. Caspase 3 in breast cancer. Clinical Cancer Research 9: 738-742. Pergentino, H.E.S.; Nicola, P.A.; Pereira, L.C.M.; Novelli, I.A. & Ribeiro, L.B. 2017. A new case of predation on a lizard by Tropidurus hispidus (Squamata, Tropiduridae), including a list of saurophagy events with lizards from this genus as predators in Brazil. Herpetology Notes 10: 225-228. Ramírez-Bautista, A.; Balderas-Valdivia, C. & Vitt L.J. 2000. Reproductive ecology of the whiptail lizard Cnemidophorus lineatissimus (Squamata: Teiidae) in a tropical dry forest. Copeia 2000: 712-722. Ribeiro, L.B. & Freire, E.M.X. 2011.Trophic ecology and foraging behavior of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata, Tropiduridae) in a caatinga area of northeastern Brazil. Iheringia, Série Zoologia 101: 225-232. Ribeiro, L.B.; Silva, N.B. & Freire, E.M.X. 2012. Reproductive and fat body cycles of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata, Tropiduridae) in a caatinga area of northeastern Brazil. Revista Chilena de Historia Natural 85: 307-320. Ruifrok, A.C. 1997. Quantification of immunohistochemical staining by color translation and automated thresholding.

Analytical and Quantitative Cytology and Histology 19: 107-113. Santos, H.S.; Santos, J.M.S.; Matos, M.H.T.; Silva, N.B.; Freire, E.M.X. & Ribeiro, L.B. 2015. Ovarian follicular cycle of Tropidurus hispidus and Tropidurus semitaeniatus (Squamata: Tropiduridae) in a semiarid region of Brazil. Zoologia: an international journal for zoology 32: 86-92. Silva, E.A.P.; Santos, T.D.; Leite, G.N. & Ribeiro, L.B. 2013. Tropidurus hispidus (Squamata: Tropiduridae) and Leptodactylus cf. fuscus (Anura: Leptodactylidae) as prey of the teiid lizards Salvator merianae and Ameiva ameiva. Herpetology Notes 6: 51-53. Tammaro, S.; Simoniello, P.; Ristoratore, F.; Coppola, U.; Scudiero, R. & Motta, C.M. 2017. Expression of caspase 3 in ovarian follicle cells of the lizard Podarcis sicula. Cell Tissue Research 367: 397-404. Van Sluys, M.; Mendes, H.M.A.; Assis, V.B. & Kiefer, M.C. 2002. Reproduction of Tropidurus montanus Rodrigues, 1987 (Tropiduridae), a lizard from a seasonal habitat of southeastern Brazil, and a comparison with other Tropidurus species. Herpetological Journal 12: 89-97. Vieira, W.L.S.; Gonçalves, M.B.R. & Nóbrega, R.P. 2012. Predation on Tropidurus hispidus (Squamata: Tropiduridae) by Lasiodora klugi (Aranea: Theraphosidae) in the semiarid caatinga region of northeastern Brazil. Biota Neotropica 12: 263-265. Vitt, L.J.; Magnusson, W.E.; Ávila-Pires, T.C. & Lima, A.P. 2008. Guia de lagartos da Reserva Adolpho Ducke, Amazônia Central. Áttema Design Editorial, Manaus. Young, C.; Curtis, M.; Ravida, N.; Mazotti, F. & Durrant, B. 2014. Development of a sperm cryopreservation protocol for the Argentine black and white tegu (Tupinambis merianae). Reproduction, Fertility and Development 26: 168-169. © 2020 por los autores, licencia otorgada a la Asociación Herpetológica Argentina. Este artículo es de acceso abierto y distribuido bajo los términos y condiciones de una licencia Atribución-No Comercial 2.5 Argentina de Creative Commons. Para ver una copia de esta licencia, visite http://creativecommons.org/licenses/by-nc/2.5/ar/

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Nota

Records of predation on Ophiodes striatus (Spix, 1824) (Squamata: Diploglossidae) by Oxyrhopus petolarius (Linnaeus, 1758) (Squamata: Dipsadidae) in the northern Atlantic Forest, Brazil Marcos Jorge Matias Dubeux1,2,3, Ubiratan Gonçalves2,3, Tamí Mott2,3 Departamento de Zoologia, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, 1235, Cidade Universitária, CEP 50670-901, Recife, Pernambuco, Brazil. 2 Instituto de Ciências Biológicas e da Saúde, Universidade Federal de Alagoas, Campus A.C. Simão, Av. Lourival Melo Mota, s/n, Tabuleiro do Martins, CEP 57072-970, Maceió, Alagoas, Brazil. 3 Museu de História Natural, Universidade Federal de Alagoas, Av. Amazonas, s/n, Prado, CEP 57010-060, Maceió, Alagoas, Brazil. 1

Recibida: 1 8

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Revisada: 2 1

Mayo

2020

Aceptada: 1 6

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2020

E ditor As o ci a d o : J. G ol db e rg doi: 10.31017/CdH.2020.(2020-009)

ABSTRACT Information on basic aspects of the natural history of many snake species based on naturalistic observations is still scarce. Here we report Oxyrhopus petolarius, a medium-sized false coral snake with terrestrial habits, feeding on Ophiodes striatus, a medium-sized lizard with cylindrical and elongated body, with vestigial posterior limbs and absence of anterior ones. The snake was registered ingesting an individual of O. striatus and upon inspecting of its stomach contents, the presence of two other individuals of O. striatus in different stages of digestion was found. Key Words: Diet; Fossorials; Lizard; Predator-prey relationships; Snake.

Encounters with snakes in the natural environment are fortuitous, and consequently, ecological observations, such as reproductive, foraging and predation events are rare (Mushinsky, 1987; Sazima, 1989). Information on basic aspects of snakes natural history based on naturalistic observations is still scarce, and current knowledge of the diet composition of species is mostly based on dissection of digestive tract of collected individuals and/or punctual records (e.g. Prudente et al., 1998; Bernarde et al., 2000; Bovo and Sueiro, 2012; Dorigo et al., 2014). Reports describing feeding events seen occasionally become essential for understanding the species’ dietary patterns and assess how this can vary between different regions (Greene, 1984). Oxyrhopus petolarius (Linnaeus, 1758) is a medium-sized Neotropical snake (Uetz et al., 2020). This false coral is terrestrial and predominantly nocturnal (Lynch, 2009; McCrainie, 2011). Its diet consists of amphibians, lizards, birds and their eggs, bats, small terrestrial mammals and even other snakes (Rodríguez-França and Amorim, 2012; Ga-

iarsa et al., 2013; Nogueira et al., 2013; Caldeira et al., 2014; Marín-Martínez et al., 2017; Botero et al., 2019). Ophiodes striatus (Spix, 1824) is a mediumsized lizard known as glass snake. It has a cylindrical and elongated body, with vestigial posterior limbs and anterior ones completely absent (Cunha, 1961). They are mostly fossorials and semi-fossorials, but can occasionally be found on the surface (Vitt and Caldwell, 2013). This species is currently found in the east of South America (Costa and Bérnils, 2018; Uetz et al., 2020). Here we report the first record of Ophiodes striatus predation by Oxyhropus petolarius. On December 21, 2019, at 07:55 PM a female of O. petolarius (MUFAL 15968; snout-vent length [SVL]= 265 mm; tail length [TL]= 82 mm; head width [HW]= 6mm; head length [HL]= 9 mm; weight with content = 8.9 g; weight without content= 6.9 g; Fig. 1A–D) was seen on the ground in a flooded pasture during an anuran survey in the municipality of Quebrangulo, state of Alagoas, Brazil (-9.259450° S, -36.440944° W; WGS 84; 537 m a.s.l.). The individual was captured manually by UG and

Author for correspondence: marcosdubeux.bio@gmail.com

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M.J.M. Dubeux et al. - Predation of Ophiodes striatus by Oxyrhopus petolarius

Figure 1. Predation of Ophiodes striatus by Oxyrhopus petolarius in the northern Atlantic Forest. A = Ingestion process; B = Relative position of the three individuals of O. striatus (stomach contents) in the digestive system of O. petolarius; C = Photo in dorsal view of individuals outside the stomach. Lateral, dorsal, and ventral views of the head of O. petolarius (D) and O. striatus (E). Scale bar: B â&#x20AC;&#x201C; C= 100 mm, D â&#x20AC;&#x201C; E= 50 mm.

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Cuad. herpetol. 34 (2): 247-250 (2020) only then he realized that the snake was ingesting an individual of the lizard Ophiodes striatus (MUFAL 15968 [stomach contents]; SVL= 58 mm; TL= 74 mm; HW= 6 mm; HL= 4 mm; weight= 0.9 g; Fig. 1A, B[iii], C[iii] and E). The snake was then placed back on the ground where it was photographed and concluded the ingestion of its prey (Fig. 1A). The individual was collected (SISBio/ICMBIO 32920-1) and taken to the Laboratório de Biologia Integrativa (LABI) of Universidade Federal de Alagoas (UFAL). After euthanasia, it was fixed in 10% formalin and preserved in 70% alcohol. Upon inspecting the stomach contents, the presence of two other individuals of O. striatus in different stages of digestion was found (weight= 0.4 g each; Fig. 1B[i–ii] and C[i–ii]). All specimens were incorporated into the Coleção Herpetológica do Museu de História Natural da Universidade Federal de Alagoas (MHN-UFAL). Punctual records of Oxyrhropus petolarius feeding events are relatively common and show a wide range of taxonomic groups in its dietary items (see below). Lizards predominate among the dietary items already registered for this species (46% [n= 13]; Gaiarsa et al., 2013; Nogueira et al., 2013; Marín-Martínez et al., 2017; Botero et al., 2019; present study). Most these species already registered as prey for O. petolarius generally have aerial, arboreal or semi-arboreal habitats (60% [n= 17]), such as: small non-flying mammals and bats (32% [n= 9 ; Rodríguez-França and Amorim, 2012; Gaiarsa et al., 2013; Caldeira et al., 2014), birds and their eggs (21% [n= 6]; Gaiarsa et al., 2013) and arboreal or semiarboreal lizards (7% [n= 2]; Nogueira et al., 2013; Botero et al., 2019). However, there were no predation record of fossorial or semi-fossorial species such as the lizards Ophiodes in the Oxyrhopus’ diet. As far as we know, predation records of Ophiodes striatus are only known for the snake Philodryas patagoniensis (two records in the state of Rio Grande do Sul, Brazil; Entiauspe-Neto et al., 2018; Quintela and Loebmann, 2019). For the Ophiodes genus predation records are known by the bird Guira guira for O. fragilis (Koski et al., 2019). Predator-prey relationships are important elements for attaining a better understanding of a species’ natural history and may shed light what factors are limiting for species distribution and community composition (Greene, 1984). Acknowledgements The authors thank the Museu de História Natural da

Universidade Federal de Alagoas for allowing us to access the material; researchers A. Melo, I. Martins, P. Costa, M. Ramos, L. Queiroz and R. Oliveira for the support in the field trips. MJMD thanks Fundação de Amparo a Ciência e Tecnologia do Estado de Pernambuco - FACEPE (PBPG-1117-2.04/19) and TM thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq (309904/2015-3 and 312291/2018-3) for financial support. We thank an anonymous referee for constructive comments. Literature cited

Bernarde, P.S; Moura-Leite, J.D.; Machado, R.A. & Kokobum, M.N.C. 2000. Diet of the colubrid snake, Thamnodynastes strigatus (Günther, 1858) from Paraná State, Brazil, with field notes on anuran predation. Revista Brasileira de Biologia 60: 695-699. Botero, V.S.; Martínez, M.M.; Guarín, D.V. & Chavez, H.E.R. 2019. Boyacá spiny rat, Proechimys chrysaeolus (Mammalia: Echimyidae), a new prey item of the banded calico snake, Oxyrhopus petolarius (Reptilia: Dipsadidae). Herpetology Notes 12: 651-653. Bovo, R.P. & Sueiro, L.R. 2012. Records of predation on Itapotihyla langsdorffii (Anura: Hylidae) by Chironius bicarinatus (Serpentes: Colubridae) with notes on foraging substrate. Herpetology Notes 5: 291-292. Caldeira, H.; Borges, D. & Feio, R.A. 2014. New prey record for the Banded Calico Snake Oxyrhopus petolarius (Serpentes: Dipsadidae). Herpetology Notes 7: 115-118. Costa, H.C. & Bérnils, R.S. 2018. Répteis do Brasil e suas Unidades Federativas: Lista de espécies. Herpetologia Brasileira 7: 11-57. Cunha, O.R. 1961. Lacertílios da Amazônia. Boletim do Museu Paraense Emílio Goeldi 39: 1-189. Dorigo, T.A.; Vrcibradic, D.; Borges-Junior, V.N.T. & Rocha, C.B.D. 2014. New records of anuran predation by snakes of the genus Thamnodynastes Wagler, 1830 (Colubridae: Dipsadinae) in the Atlantic rainforest of southeastern Brazil. Herpetology Notes 7: 261-264. Entiauspe-Neto, O.M.; Quintela, F.M.; Pino, S.R. & Loebmann, D. 2018. Ophiodes striatus (Brazilian Glass Lizard). Predation. Herpetological Review 49: 331. Gaiarsa, M.P.; Alencar, L.R.V. & Martins, M. 2013. Natural history of Pseudoboine snakes. Papéis Avulsos de Zoologia 53: 261-283. Greene, H.W. 1984. Feeding and the Evolution of Snakes. BioScience 34: 41-42. Koski, D.A.; Carvalho, D.M.; Koski, A.P.V. & ClementeCarvalho, R.B.G. 2017. Ophiodes fragilis (Cobra-de-vidro; Fragile Worm Lizard). Predation. Herpetological Review 48: 654-655. Lynch, J.D. 2009. Snakes of the genus Oxyrhopus (Colubridae: Squamata) in Colombia: taxonomy and geographic variation. Papéis Avulsos de Zoologia 49: 319-337. Marín-Martínez, M.; Rojas-Morales, J.A. & Díaz-Ayala, R.F. 2017. A Middle American Ameiva, Holcosus festivus (Teiidae), as prey of the Banded Calico Snake, Oxyrhopus petolarius (Dipsadidae). IRCF Reptiles & Amphibians 24:

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M.J.M. Dubeux et al. - Predation of Ophiodes striatus by Oxyrhopus petolarius 55-57. McCrainie, J.R. 2011. Snakes of Honduras. Systematics, Distribution, and Conservation. Society for the Study of Amphibians and Reptiles, New York. Mushinsky, H.R. 1987. Foraging ecology: 302-334. In: Seigel, R.A. Collins, J.T. & Novak, S.S. (eds.), Snakes: Ecology and Evolutionary Biology. MacMillan Publishing Company, New York. Nogueira, C.H.; Figueiredo-de-Andrade, C.A. & Freitas, N. 2013. Death of a juvenile snake Oxyrhopus petolarius (Linnaeus, 1758) after eating an adult house gecko Hemidactylus mabouia (Moreau de Jonnés, 1818). Herpetology Notes 6: 39-43. Prudente, A.L.C.; Moura-Leite, J.C. & Morato, S.A.A. 1998. Alimentação das espécies de Siphlophis Fitzinger (Serpentes, Colubridae, Xenodontinae, Pseudoboini). Revista Brasileira de Zoologia 15: 375-383.

Quintela, F.M. & Loebmann, D. 2019. Diet, sexual dimorphism and reproduction of sympatric racers Philodryas aestiva and Philodryas patagoniensis from the coastal Brazilian Pampa. Anais da Academia Brasileira de Ciências 91: 1-12. Rodrígues-França, F.G. & Amorim, R. 2012. First record of predation on the bat Carollia perspicillata by the False Coral Snake Oxyrhopus petolarius in the Atlantic Rainforest. Biotemas 25: 307-309. Sazima, I. 1989. Comportamento Alimentar da Jararaca, Bothrops jararaca: Encontros provocados na natureza. Ciência e Cultura 41: 500-505. Uetz, P.; Freed, P. & Hošek, J. (eds.) 2019. The Reptile Database. Available at: http://www.reptile-database.org. Last accessed on 13 February 2020. Vitt, L.J. & Caldwell, J.P. 2013. Herpetology: An introductory biology of amphibians and reptiles. Academic Press, San Diego.

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Cuad. herpetol. 34 (2): 251-255 (2020)

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Diet of Dermatonotus muelleri (Anura: Microhylidae) in a semideciduous forest in western Brazil Juan Fernando Cuestas Carrillo1, Caroline Galvão2, Luciano Alves dos Anjos3 , Diego José Santana2 Departamento de Ecologia, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Cidade Universitária, CEP 79002-970, Campo Grande, MS, Brasil. 2 Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Cidade Universitária, CEP 79002-970, Campo Grande, MS, Brasil. 3 Faculdade de Engenharia de Ilha Solteira, Departamento de Biologia e Zootecnia, Universidade Estadual Paulista “Júlio de Mesquita Filho” - UNESP, CEP 15385-000, Ilha Solteira, SP, Brasil. 1

Recibida: 0 3 D i c i e m b r e 2 0 1 9 Revisada: 0 9

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2020

Aceptada: 0 2

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2020

E ditor As o ci a d o : J. G ol db e rg doi: 10.31017/CdH.2020.(2019-057)

ABSTRACT Anurans are important predators and preys in neotropical food webs linking different trophic levels. A small portion of them are specialist predator what is related with mouth size and morphology. Herein, we report the diet of Dermatonotus muelleri (Microhylidae) from a semideciduous forest in Western Brazil. We collected a total of 63 adults of D. muelleri (females and males) from the Selvíria municipality, Mato Grosso do Sul State, Brazil. We did not find differences between male and female diet composition. The most frequent preys found were isopterans (63.34%) and hymenopterans (26.67%). All hymenopterans identified belong to the Formicidae family. Our results defined Dermatonotus muelleri as an ant-specialist predator and agree with previous studies about the diets of neotropical Microhylid frogs like Chiasmocleis albopunctata, C. bassleri, C. capixaba, C. hudsoni, C. jimi, C. leucosticta, C. shudikarensis, C. ventrimaculata, Ctenophryne geayi, Elachistocleis bicolor, E. ovalis, E. pearsei, and E. panamensis. Key Words: Trophic ecology; ant-specialist; Microhylid.

Anurans are fundamental in trophic networks (Stănescu et al., 2014), as they consume several arthropods and efficiently control insect populations (McCormick and Polis, 1982; Wells, 2007). Besides, adults, larvae and eggs are preyed on by both vertebrates and invertebrates such as birds (Poulin et al., 2001), mammals (Lawrence et al., 2018), snakes (Carrillo, 2017), other anurans (Ceron et al., 2018), fishes (Hecnar and M’Closkey, 1997), spiders (Menin et al., 2005a), water bugs (Toledo, 2005), diving beetle (Santos-Silva and Ferrari, 2012), ants (Lingnau and Di-Bernardo, 2006) and wasps (Warkentin, 2000). Due to their intermediate positions in trophic networks, frogs are an important link between arthropods and large sized vertebrate predators, allowing nutrients to dislocate between trophic levels (Beard et al., 2002). Although most anurans really behave as generalist predators, some lineages are considered specialists which is strongly related with mouth morphology and size (Toft, 1981). Microhylids and dendrobatids, for example, are classified as ant-specialists since they feed mainly on ants and

termites (Parmelee, 1999; Darst et al., 2004). Among the neotropical microhylids, Dermatonotus muelleri (Boettger, 1885) is a burrowing species with nocturnal habits, which builds subterranean chambers as refugees where it remains during the dry season in estivation, only emerging in the rainy season for explosive reproduction (Nomura et al., 2009; Nomura and Rossa-Feres, 2011). Dermatonotus muelleri is endemic to the South American Diagonal of open formations, including ecosystems as the Cerrado, Caatinga, Chaco and Pantanal characterized with savanna like vegetation and a seasonal climate (Duellman, 1999). Its distribution includes eastern Bolivia, Paraguay, Northern Argentina and several Brazilian states with open formations (Frost, 2020). Given that more studies about anuran natural history and ecology are needed (Silvano and Segala, 2005), diet studies are fundamental for understanding life history, trophic networks and their ecological implications (Hirai and Matsui, 1999), such as nutrient flow and parasite lifecycles (Beard et al., 2002; Campião et al., 2015). Herein, we report the diet of a population of Dermatonotus muelleri from

Author for correspondence: jfcuestas@gmail.com

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J. Carrillo et al. - Dermatonotus muelleri diet a semi-deciduous forest in Mato Grosso do Sul State, Western Brazil. On 26 of November 2015, we collected 63 adults of Dermatonotus muelleri (28 females and 35 males) from a riparian forest of the Véstia stream at the Fazenda de Ensino, Pesquisa e Extensão da Universidade Estadual Paulista, Campus de Ilha Solteira, located in the Selvíria municipality (20° 23’ 44.00” S; 51° 23’ 40.09” W; DATUM = WGS84), Mato Grosso do Sul State, Brazil. The region presents a tropical weather, with a rainy summer and a dry winter, average annual temperature of 24.5° C and average relative humidity of 64.8% (Moura et al., 2011; Alvares et al., 2014). Vegetation is considered as a remnant of transitional forest between Cerrado and Seasonal Semi-deciduous forest. Cerrado areas varies from dense grassland with shrubs and trees to woodland with a canopy of 12–15 m high, while Semi-deciduous forest presents canopy of 15-18 m high with emergent trees up to 25 m (GromboneGuaratini and Rodrigues, 2002; Bridgewater et al., 2004). We killed the specimens through overdose of liquid lidocaine, fixed them in formaldehyde 10% and preserved them in ethanol 70%. We separated stomachs for posterior diet analysis by ventral dissection. All individuals are housed at Coleção Zoológica of the Universidade Federal de Mato Grosso do Sul (ZUFMS-AMP 10788-10850). For diet analysis, we determined the prey species to their Order using a stereomicroscope. We measured every prey item’s width (w) and length (l) to estimate the ellipsoid volume per prey using Griffiths and Mylotte (1987) formula: V=(4π/3) (w/2)2(l/2). To determine the importance of each prey item for D. muelleri, we used Pinkas et al. (1971) importance index using occurrence percentage (F%), numeric percentage (N%) and volumetric percentage as follow: IRI= F% x (N%+V%). To test whether the diet of the sexes is similar or different, we performed a permutational analysis of variance (PERMANOVA) using the frequency of occurrence of food items in the R program, version 3.2 (R Core Team 2017), with the packages “vegan” (Oksanen et al., 2019). However, the diet did not differ between males and females (p= 0.117; F= 2.04). After analyzing 63 stomachs, we found 33 empty stomachs (52.38%) and 30 stomachs with at least one prey item (47.62%). 24.32% of the prey found were at a high level of decomposition, making their proper identification impossible. We identified 252

2,630 prey items (Table 1), divided in two Insecta orders (Isoptera and Hymenoptera) and one mite order (Trombidiformes). Additionally, it is relevant to mention that, all Hymenopterans identify in D. muelleri diet belong to the Formicidae family. Isoptera was the most frequent item in 19 stomachs (63.34%), corresponding to 98.75% of the total prey ingested and to 39.03% of the total prey volume. The second most important item was Hymenoptera (Formicidae), found in 8 stomachs (26.67%), representing 0.87% of the total prey ingested and 1.01% of the total prey volume. Overall, the most important item, based on important relative index (IRI), was Isoptera followed by Hymenoptera (Formicidae) and Trombidiformes (Table 1). Undetermined items where present in the 30% of the analysed stomach and represented the 59.95% of the total volume of ingested prey. The diet of Dermatonotus muelleri was composed of termites, ants and mite. This kind of diet is classified as ant specialist by Toft (1980). Our results agree with the diet reported for fossorial Microhylid species with explosive reproduction, such as Chiasmocleis albopunctata (Boettger, 1885), C. bassleri Dunn, 1949, C. capixaba Cruz, Caramaschi, and Izecksohn, 1997, C. hudsoni Parker, 1940, C. jimi Caramaschi and Cruz, 2001, C. leucosticta (Boulenger, 1888), C. shudikarensis Dunn, 1949, C. ventrimaculata (Andersson, 1945), Ctenophryne geayi Mocquard, 1904, Elachistocleis bicolor (GuérinMéneville, 1838), E. ovalis (Schneider, 1799), E. panamensis (Dunn, Trapido, and Evans, 1948), E. pearsei (Ruthven, 1914), Hamptophryne alios (Wild, 1995), H. boliviana (Parker, 1927), Kaloula pulchra Gray, 1831, Microhyla fissipes Boulenger, 1884 and M. heymonsi Vogt, 1911 (Berry, 1965; Duellman, 1978; Schluter and Salas, 1991; Parmelee, 1999; Caramaschi and Cruz, 2001; Solé et al., 2002; Van Sluys et al., 2006; Berazategui et al., 2007; López et al., 2007; Araújo et al., 2009; Norval et al., 2014; Blanco-Torres et al., 2015; Lopes et al., 2017; da Silva et al., 2019). The most important alimentary item was Isoptera, which was also found for others species of microhylids like Elachistocleis panamensis (BlancoTorres et al., 2015). These colonial insects fly during the first half of the rainy season, when large numbers of alates actively search for primary reproduction (Pinheiro et al., 2002; Nomura, 2005; Bignell et al., 2010). On the other hand, D. muelleri is a fossorial species whose explosive reproduction only occurs at the beginning of the rainy season (Nomura et al.,

Cuad. herpetol. 34 (2): 251-255 (2020) Table 1. Diet of Dermatonotus muelleri from Selvíria municipality, Mato Grosso do Sul State, Brazil. Absolute and relative volume (V and V%), number of individuals (N and N%), absolute and relative frequency (F and F%) and important relative index (IRI) per prey item. Prey item

V (mm3)

IRI

0.39

<0.01

0.04

2.70

0.11

259.19

1.01

0.87

21.62

40.64

10014.49

39.03

2597

98.75

51.35

7075.00

15381.92

59.95

0.34

24.32

1466.25

ARTHROPODA Arachnida Trombidiformes Insecta Hymenoptera (Form†) Isoptera UNDETERMINED † Form=Formicidae

2009, Nomura and Rossa-Feres, 2011). Dermatonotus muelleri and isopterans share peak reproductive activities, resulting in high abundance of this food item available for to this frog species. Another important alimentary item was Hymenoptera (Formicidae), with high abundance in leaf litter in neotropical environments (BarberenaArias and Aide, 2002). Although it is not the main food item, Formicidae is an important item in the diet of microhylids, including D. muelleri and other species such as Elachistocleis bicolor, E. pearsi and E. panamensis (Berazategui et al., 2007; López et al., 2007; Blanco-Torres et al., 2015). Similar to our results, arachnids like spiders and mites have been reported with low importance for Chiasmocleis hudsoni, C. shudikarensis, Elachistocleis bicolor and E. pearsi (Berazategui et al., 2007; Blanco-Torres et al., 2015; da Silva et al., 2019). Diet of anurans can changes depending on prey availability, which in turn depends on the season (Menin et al., 2005b). However, D. muelleri proved to be a specialist species with fossorial habits, which is always active during the beginning of the rainy season with explosive reproduction, avoiding prey availability changes. Dermatonotus muelleri morphology indicates clear specialization for Isoptera, presenting a small head, small mouth opening and no teeth (Trueb and Grans, 1983; Isacch and Barg, 2002). Furthermore, the species presents specific behavior to reach Isoptera and can change from sit and wait to active predation according to the spatial distribution of its resources (Nomura and Rossa-Feres, 2011). Finally, as we expected, D. muelleri presented a specialist diet, mainly based on Isopterans and Hymenopterans from the Formicidae family. Our results agree with previous reports for the species and suits the known morphology and

behavior of microhylids. Acknowledgements We are grateful to Hannah Doerrier for English review. To the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for JFCC’s scholarship (Finance Code 001), and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for CG’s scholarship (PIBIC 2016/2017). DJS thanks CNPq for his research fellowship (311492/2017-7). Literature cited

Alvares, C.A.; Stape, J.L.; Sentelhas, P.C.; Gonçalves, J.L.M. & Sparovek, G. 2014. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711-728. Araújo, M.S.; Bolnick, D.I.; Martinelli, L.A.; Giaretta, A.A. & Reis, S.F. 2009. Individual-level diet variation in four species of Brazilian frogs. Journal of Animal Ecology 78: 848-856. Barberena-Arias, M.F. & Aide, T.M. 2002. Variation in Species and Trophic Composition of Insect Communities in Puerto Rico. Biotropica 34: 357-367. Beard, K.H.; Vogt, K.A. & Kulmatiski, A. 2002. Top-down effects of a terrestrial frog on forest nutrient dynamics. Oecologia 133: 583-593. Berazategui, M.; Camargo, A. & Maneyro, A. 2007. Environmental and Seasonal Variation in the Diet of Elachistocleis bicolor (Guérin-Méneville 1838) (Anura: Microhylidae) from Northern Uruguay. Zoological Science 24: 225-231. Berry, P.Y. 1965. The diet of some Singapore Anura (Amphibia). Journal of Zoology 144: 163-167. Bignell, D.E.; Roisin, Y. & Lo, N. 2010. Biology of Termites: A modern Synthesis. Springer. Dordrecht. Blanco-Torres, A.; Duré, M. & Bonilla, M.A. 2015. Observaciones sobre la dieta de Elachistocleis pearsei y Elachistocleis panamensis en dos áreas intervenidas de tierras bajas del norte de Colombia. Revista Mexicana de Biodiversidad 86: 538-540. Bridgewater, S.; Ratter, J.A. & Ribeiro, J.P. 2004. Biogeographic patterns, b-diversity and dominance in the Cerrado biome of Brazil. Biodiversity and Conservation 13: 2295-2318.

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J. Carrillo et al. - Dermatonotus muelleri diet Campião, K.M.; Ribas, A.C.A.; Morais, D.H.; Da Silva, R.J. & Tavares, L.E.R. 2015. How Many Parasites Species a Frog Might Have? Determinants of Parasite Diversity in South American Anurans. PLoS ONE 10: e0140577. doi:10.1371/ journal.pone.0140577. Caramaschi, U. & Cruz, C.A.G. 2001. A new species of Chiasmocleis Méhelÿ, 1904 from Brazilian Amazonia. Boletim do Museu Nacional do Rio de Janeiro, Nova Série, Zoologia 469: 1-8. Carrillo, J.F.C. 2017. Predation of Thamnodynastes chaquensis (Serpentes, Colubridae) upon Elachistocleis matogrosso (Anura, Microhylidae) in the Brazilian Pantanal. Herpetology Notes 10: 355-357. Ceron, K.; Moroti, M.T.; Benício, R.A.; Balboa, Z.P.; Marçola, Y.; Pereira, L.B. & Santana, D.J. 2018. Diet and first report of batracophagy in Leptodactylus podicipinus (Anura: Leptodactylidae). Neotropical Biodiversity 4: 69-73. Darst, C.R.; Menéndez-Guerrero, P.A.; Coloma, L.A. & Cannatella, D.C. 2004. Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): a comparative analysis. The American Naturalist 165: 56-69. da Silva, I.B.; dos Santos, T.F.; Frazão, L.; Marques-Souza, S.; da Silva, L.A.; Menin, M. 2019. The diet of Chiasmocleis hudsoni and C. shudikarensis (Anura, Microhylidae) of terra firme forests in the Brazilian Amazonia. Herpetology Notes 12: 655-659. Duellman, W.E. 1978. The biology of an equatorial herpetofauna in Amazonian Ecuador. University of Kansas Museum of Natural History, Miscellaneous Publications 65: 1-352. Duellman, W.E. 1999. Patterns of distribution of amphibians: a global perspective. The Johns Hopkins University Press. Baltimore. Frost, D.R. 2020. Amphibian Species of the World: An Online Reference. Version 6.1. Accessible at: https:// amphibiansoftheworld.amnh.org/index.php. Last access: 20 January 2020. Griffiths, R.A. & Mylotte, V.J. 1987. Microhabitat selection and feeding relations of smooth and warty newts, Triturus vulgaris and T. cristatus, at an upland pond in mid‐Wales. Ecography 10: 1-7. Grombone-Guaratini, M.T. & Rodrigues, R.R. 2002. Seed bank and seed rain in a seasonal semi-deciduous forest in southeastern Brazil. Journal of Tropical Ecology 18: 759-774. Hecnar, S.J. & M’Closkey, R.T. 1997. The effects of predatory fish on amphibian species richness and distribution. Biological Conservation 79: 123-131. Hirai, T. & Matsui, M. 1999. Feeding habits of the pond frog, Rana nigromaculata, inhabiting rice fields in Kyoto, Japan. Copeia 1999: 940-947. Isacch, J.P. & Barg, M. 2002. Are bufonid toads specialized antfeeders? A case test from the Argentinean ﬂooding Pampa. Journal of Natural History 36: 2005-2012. Lawrence, J.P.; Mahony, M. & Noonan, B.P. 2018. Differential responses of avian and mammalian predators to phenotypic variation in Australian Brood Frogs. PLoS ONE 13: e0195446. https://doi.org/10.1371/journal.pone.0195446 Lingnau, R. & Di-Bernardo, M. 2006. Predation on foam nests of two anurans by Solenopsis sp. (Hymenoptera: Formicidae) and Liophis miliaris (Serpentes: Colubridae). Biociências 14: 223-224.

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Lopes, M.S.; Bovendorp, R.S.; de Moraes, G.J.; Percequillo, A.R. & Bertoluci, J. 2017 Diversity of ants and mites in the diet of the Brazilian frog Chiasmocleis leucosticta (Anura: Microhylidae). Biota Neotropica 17: e20170323. López, J.A.; Ghirardi, R.; Scarabotti, P.A. & Medrano, M.C. 2007. Feeding ecology of Elachistocleis bicolor in a riparian locality of the middle Paraná River. The Herpetological Journal 17: 48-53. McCormick, S. & Polis, G.A. 1982. Arthropods that prey on vertebrates. Biological Reviews 57: 29-58. Menin, M.; Rodrigues, D.J. & Azevedo, C.S. 2005a. Predation on amphibians by spiders (Arachnida, Aranae) in the Neotropical region. Phyllomedusa 4: 39-47. Menin, M.; Rossa-Feres, D.C. & Giaretta, A.A. 2005b. Resource use and coexistence of two syntopic hylid frogs (Anura, Hylidae). Revista Brasileira de Zoologia 22: 61-72. Moura, R.V.; Hernandez, F.B.T.; Leite, M.A.; Franco, R.A.M.; Feitosa, D.G. & Machado, L.F. 2011. Qualidade da água para uso em irrigação na microbacia do Córrego do cinturão verde, município de ilha solteira. Revista Brasileira de Agricultura Irrigada 5: 68-74. Nomura, F. 2005. Reproductive ecology, foraging and burrow behavior of Dermatonotus muelleri (Anura, Microhylidae). Biota Neotropica 5: 209-210. Nomura, F. & Rossa-Feres, D.C. 2011. The frog Dermatonotus muelleri (Boettger 1885) (Anura Microhylidae) shifts its search tactics in response to two different prey distributions. Ethology, Ecology and Evolution 23: 318-328. Nomura, F.; Rossa-Feres, D.C. & Langeani, F. 2009. Burrowing behavior of Dermatonotus muelleri (Anura, Microhylidae) with reference to the origin of the burrowing behavior of Anura. Journal of Ethology 27: 195-201. Norval, G., Huang, S.C.; Mao, J.J.; Goldberg, S.R. & Yang, Y.J. 2014. Notes on the diets of five amphibian species from southwestern Taiwan. Alytes 30: 69-77. Oksanen, F.; Blanchet F.G; Friendly, M; Kindt, R; Legendre, P; McGlinn D; Minchin, P.R; O’Hara R.B.; Simpson, G.L.; Solymos, P.L.; Stevens, M.H.H.; Szoecs, E. & Wagner, H. 2019. Vegan. Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan. Parmelee, J.R. 1999. Trophic ecology of a tropical anuran assemblage. Scientific Papers of Natural History Museum, The University of Kansas 11: 1-59. Pinheiro F.; Diniz, I. R.; Coelho, D. & Bandeira, M.P.S. 2002. Seasonal pattern of insect abundance in the Brazilian Cerrado. Austral Ecology 27: 132-136. Pinkas, L.; Oliphant, M.S. & Iverson, I.L.K. 1971. Food habits of albacore, Bluefin tuna and bonito in Californian waters. California Department of Fish and Game: Fish Bulletin 152: 1-105. Poulin, B.; Lefebvre, G.; Ibáñez, R.; Jaramillo, C.; Hernandez, C. & Rand, A.S. 2001. Avian predation upon lizards and frogs in a neotropical forest understory. Journal of Tropical Ecology 17: 21-40. Santos-Silva, C.R. & Ferrari, S.F. 2012. Predation on Dendropsophus soaresi (Anura: Hylidae) by a diving beetle (Coleoptera: Dytiscidae) in Raso da Catarina, north-eastern Brazil. Herpetology Notes 5: 11-12. Schlüter, A. & Salas, A.W. 1991. Reproduction, tadpoles, and ecological aspects of three syntopic microhylid species

Cuad. herpetol. 34 (2): 251-255 (2020) from Peru (Amphibia: Microhylidae). Stuttgarter Beiträge zur Naturkunde 458: 1-17. Silvano, D. L., & Segala, M.V. 2005. Conservation of Brazilian amphibians. Conservation Biology 19: 653-658. Solé, M.; Kketterl, J.; Di Bernardo, M. & Kwet, A. 2002. Ants and termites are the diet of the microhylid frog Elachistocleis ovalis (Schneider, 1799) at an Araucaria forest in Rio Grande do Sul, Brazil. The Herpetological Bulletin 79: 14-17. Stănescu, F.; Marangoni, F. & Reinko, I.I. 2014. Predation of Dermatonotus muelleri (Boettger 1885) by Lepidobatrachus llanensis Reig and Cei 1963. Herpetology Notes 7: 683-684. Toft, C.A. 1980. Feeding ecology of thirteen syntopic species of anurans in a seasonal tropical environment. Oecologia 45: 131-141. Toft, C.A. 1981. Feeding ecology of Panamanian litter anurans: patterns in diet and foraging mode. Journal of Herpetology 15: 139-144.

Toledo, L.F. 2005. Predation of juvenile and adult anurans by invertebrates: current knowledge and perspectives. Herpetological Review 36: 395-400. Trueb, L. & Gans, C. 1983. Feeding specialization of the Mexican burrowing toad, Rhinophrynus dorsalis (Anura: Rhinophrynidae). Journal of Zoology 199: 189-208. Van Sluys, M.; Schittini, G.M., Marra, R.V.; Azevedo, A.R.M.; Vicente, J.J. &Vrcibradic, D. 2006. Body size, diet and endoparasites of the microhylid frog Chiasmocleis capixaba in an Atlantic Forest area of southern Bahia state, Brazil. Brazilian Journal of Biology 66: 167-173. Warkentin, K.M. 2000. Wasp predation and wasp-induced hatching of red-eyed treefrog eggs. Animal Behaviour 60: 503-510. Wells, K. D. 2007. The ecology and behavior of amphibians. The University of Chicago Press, Chicago, Illinois, USA.

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Primer registro de cifoescoliosis en Sceloporus formosus (Squamata: Phrynosomatidae) en Veracruz, México Jorge Luis Castillo-Juárez1, Víctor Vásquez-Cruz2, Laura Pamela Taval-Velázquez3 Universidad Veracruzana, Facultad de Ciencias Biológicas y Agropecuarias, camino viejo Peñuela-Amatlán de los Reyes S/N. Mpio. de Amatlán de los Reyes, C.P. 94950, Veracruz, México. 2 PIMVS Herpetario Palancoatl, Avenida 19 No. 5525. Colonia Nueva Esperanza, Córdoba, Veracruz, C.P. 94540, México. 3 Fortín de las Flores, Veracruz, México. 1

Recibida: 2 9 No v i e m b r e 2 0 1 9 Revisada: 2 0

Enero

2020

Aceptada: 2 3

Marzo

2020

E d itor As o c i a d o : C . B or te i ro doi: 10.31017/CdH.2020.(2019-056)

ABSTRACT First record of kyphoscoliosis in Sceloporus formosus (Squamata: Phrynosomatidae) in Veracruz, México. In June 2019, we found a female with malformations in the spine and tail in a remnant of cloud forest, apparently not associated the use of agrochemicals, observing that despite a severe malformation the individual did not present abnormal locomotion. Key Words: Abnormalities; Malformations; Northern emerald spiny lizard.

Una malformación puede ser definida como aquella desviación del intervalo normal de variación anatómica (Johnson et al., 2001). Algunas malformaciones relacionadas con la espina dorsal son la cifosis, la lordosis y la escoliosis (Barrio-Garín et al., 2011). Las malformaciones pueden ser ocasionadas por varios factores entre ellos genéticos, congénitos y nutricionales (Rothschild et al., 2012). Entre los reptiles se han reportado con mayor frecuencia casos de cifosis y escoliosis en tortugas, serpientes y cocodrilos, siendo más esporádicas en saurios (PérezDelgadillo et al., 2015; Ramírez-Jaramillo, 2018). La cifoescoliosis es una condición donde se presenta en un mismo individuo la cifosis, una curvatura de convexidad dorsal de la columna vertebral, y escoliosis o, desviación lateral en la columna vertebral (Ramírez-Jaramillo et al., 2018). En este trabajo, presentamos el primer registro de cifoescoliosis en la lagartija Sceloporus fomosus observado en México, Veracruz, Calcahualco, Localidad Excola (19°08’06.73” N; 97°07’34.74” O; WGS84 a 1926 m s.n.m.). El 6 de junio del 2019, alrededor de las 1:20 p.m. observamos una hembra subadulta de Sceloporus formosus la cual exhibió una curvatura vertical de la columna (cifosis) iniciando a la altura de las extremidades anteriores hasta la cintura pélvica (Fig. 1A) y la parte anterior de la columna estaba curvado hacia la izquierda y el posterior estaba curvado hacia la derecha (esco-

liosis; Fig. 1B). Además, su cola tenía cuatro curvas laterales alternas cerca de la base (escoliosis). Las malformaciones parecían tener poco efecto en su locomoción. El individuo fue liberado en el sitio de captura. Debido a que no contábamos con permisos de colecta, depositamos una fotografía en la colección digital de la Natural History Museum of Los Angeles County (LACM PC 2491, Fig.1A) En el género Sceloporus son pocos los estudios que han registrado malformaciones referentes a la espina dorsal, en estado silvestre solo se han observado en cuatro especies. Mitchell y Georgel (2005) capturaron una hembra juvenil de S. undulatus en el Parque Histórico Nacional Colonial, al sur de Virginia el cual presentó cifoescoliosis. Durante el tiempo que la mantuvieron en cautividad no presentó limitaciones obvias en la movilidad, crecimiento o captura de presas. Chávez-Cisneros y Lazcano (2012) colectaron una hembra de S. marmoratus con cifoescoliosis en el área natural protegida Cerro de La Silla en el municipio de Juárez, Nuevo León, México. En la Mesa del Huarache, Calvillo, Aguascalientes, México, Pérez-Delgadillo et al. (2015) recolectaron dos hembras adultas de S. torquatus que presentaron cifosis, y mencionan que ambos especímenes no presentaron problemas para desplazarse al momento del encuentro. Valdez-Villavicencio et al. (2016) colectaron un macho subadulto de S. vandenburgianus en Sierra San Pedro Mártir, Municipio de Ensenada,

Autor para correspondencia: victorbiolvc@gmail.com

257

J. Castillo-Juárez et al. - Cifoescoliosis en Sceloporus agrícola es casi nula, así como, la posibilidad de trauma térmico como puede ocurrir en otros saurios durante la incubación no correspondería, ya que S. formosus es una especie vivípara (Canseco-Márquez y Gutiérrez-Mayén, 2010), y la descendencia estaría sujeta a la termorregulación de la hembra grávida (Pianka y Vitt, 2006). Por estas razones, nuestra hipótesis sobre las posibles causas se inclina por la ocurrencia de otros factores congénitos no determinados, como por ejemplo nutricionales tóxicos de tipo dietético o por disfunciones metabólicas de la hembra progenitora. Agradecimientos A dos revisores anónimos por sus comentarios que ayudaron a mejorar el manuscrito. Literatura citada

Canseco-Márquez, L. & Gutiérrez-Mayén, M.G. 2010. Anfibios y reptiles del Valle de Tehuacán-Cuicatlán. Comisión Nacional para el conocimiento y uso de la biodiversidad, México. Chávez-Cisneros, J.A. & Lazcano, D. 2012. Sceloporus marmoratus (Northern Rose-bellied Lizard). Kyphosis and scoliosis. Herpetological Review 43: 140. Barrio-Garín, I.; Sanz-Azkue, I.; Gosa, A. & Bandrés, A. 2011.

Figura 1. Una hembra subadulta de Sceloporus formosus con cifoescoliosis (LACM PC 2491). Vista lateral de la columna con cifosis (A) y vista dorsal de las curvaturas de la columna con escoliosis (B).

Baja California, México, que exhibió cifoescoliosis, mencionando los autores un aparente escaso efecto en la movilidad. Nuestra observación ocurrió durante un estudio a largo plazo de la herpetofauna en diferentes zonas del municipio de Calcahualco, Veracruz. Este fue el único caso de la presencia de malformaciones en un total de 58 individuos de S. formosus observados (Castillo-Juárez datos no publicados). Si bien sería necesaria una investigación muy detallada para determinar la causa de dicha malformación, la inducción por agroquímicos es poco probable ya que el hallazgo ocurrió en un remanente de bosque mesófilo de montaña (Fig. 2) en el cual la actividad 258

Figura 2. Remanente de Bosque Mesófilo de Montaña en la localidad Excola, Municipio de Calcahualco, Veracruz, México.

Cuad. herpetol. 34 (2): 257-259 (2020) Un caso de cifosis en Podarcis pityusensis (Boscá, 1883), lagartija introducida en el peñón de Gaztelugatxe (Bizkaia). Munibe (Ciencias Naturales) 59: 103-109. Jhonson, P.T.; Lunde, K.B.; Hagth, R.W.; Bowerman, J. & Blaustein, A.R. 2001. Ribeiroia ondatrae (Trematoda: Dignae) infection indices sever limb malformations in western toad (Bufo boreas). Canadian Journal of Zoology 79: 370-379. Mitchell, J.C.; & Georgel, C.T. 2005. Natural History Notes. Sceloporus undulatus undulatus (Eastern fence lizard). Kyphosis and scoliosis. Herpetological Review 36: 183. Pérez-Delgadillo, A.G.; Quintero-Díaz, G.E.; CarbajalMárquez, R.A.; & García-Balderas, C.M. 2015. Primer reporte de cifosis en Sceloporus torquatus (Squamata:

Phrynosomatidae) en el estado de Aguascalientes, México. Revista Mexicana de Biodiversidad 86: 272-274. Pianka, E.R. & Vitt, L.J. 2006. Lizards: windows to the evolution of diversity. Berkeley: University of California Press. Ramírez-Jaramillo, S.M. 2018. Primer reporte de cifoescoliosis en Stenocercus guentheri (Iguania: Tropiduridae), Andes Norte de Ecuador. Cuadernos de herpetología 32 (1): 55-57 Rothschild, B.M.; Schultze, H.P. & Pellegrini, R. 2012. Herpetological osteopathology: Annotated bibliography of Amphibians and Reptiles. Springer Science. New York. Valdez-Villavicencio, J.H.; Hollingsworth, B.D. & GalinaTessaro, P. 2016. Sceloporus vandenburgianus (Cope, 1896). Nature Notes. Kyphosis and scoliosis. Mesoamerican Herpetology 3: 488-490.

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Nota

First record of the rare snake Cercophis auratus (Schlegel, 1837) (Serpentes: Colubridae: Dipsadinae) in a relictual forest enclave at Caatinga Castiele Holanda Bezerra1,2, Bruno Ferreira Guilhon1,3, Antônio Rafael Lima Ramos1,3, Diva Maria Borges-Nojosa1,2,3 Núcleo Regional de Ofiologia, Departamento de Biologia, bloco 905. Av. Humberto Monte, Universidade Federal do Ceará, Pici, 60440-900, Fortaleza, Ceará, Brasil. 2 Programa de Pós-graduação em Ecologia e Recursos Naturais, Departamento de Biologia, bloco 902. Av. Humberto Monte, Universidade Federal do Ceará, Pici, 60440-900Fortaleza, Ceará, Brasil. 3 Programa de Sistemática, Uso e Conservação da Biodiversidade, Departamento de Biologia, bloco 902. Av. Humberto Monte, Universidade Federal do Ceará, Pici, 60440-900, Fortaleza, Ceará, Brasil. 1

Recibida: 1 5

Mayo

2020

Revisada: 2 9

Mayo

2020

Aceptada: 0 3

Junio

2020

E d i t o r A s o c i a d o : P. P a s s o s doi: 10.31017/CdH.2020.(2020-031)

ABSTRACT Cercophis auratus is a rare snake with known disjunct distribution between coastal Atlantic Forest to eastern Amazonia and Guiana Shield. Here we provide a new record of this species from a relictual highland of rainforest inside the xeric Caatinga ecoregion. This new record fill a gap of 1700 kilometers between southern (Barra do Choça – BA) and northern (Augusto Corrêa – PA) in the distribution of C. auratus (Schlegel, 1837), and bring insights about the past connective bridge between Amazonia and Atlantic forests. Key Words: Relictual rainforest; Northeastern Brazil; Gaps; Distribution.

The monotypic snake Cercophis auratus (Schlegel, 1837) was described from Paramaribo, Suriname on the basis of a single specimen. Fifty years later, Peracca (1897) described Uromacerina ricardinii (= C. auratus, see below) based on individual from São Paulo State, Brazil. Since then, several studies expand specie’s range to the states of Rio Grande do Sul, Santa Catarina, Paraná, Rio de Janeiro, Espírito Santo, and Bahia along the Atlantic coast of Brazil (Hoge, 1957; Lema, 1973; Müller and Ritter, 1978; Zamprogno, 1997; Argôlo, 2001). In addition, Cunha and Nascimento (1982) reported on two specimens of C. auratus to Cacoal Farm, municipality Augusto Corrêa, Pará State, eastern Amazon Forest, highlighting a disjunct distribution of the species among Amazonia and Atlantic rainforest. Recently, Hoogmoed et al. (2019) synonymized U. ricardinii with Cercophis auratus (Schlegel, 1837), updating its morphological variation and geographic distribution. Cercophis auratus is an arboreal and diurnal species, anurophagic and with seasonal reproduction (Morato and Bernils, 1989; Marques, 2000). The lack of knowledge about this snake in museum collections results in the almost totality of knowledge being restricted to external morphology and distribution data.

In the course of revision of the herpetological collection of Universidade Federal do Ceará, Brazil, we identified two specimens of Cercophis auratus previously considered with uncertain identifications (CHUFC 2169, 2609; Fig. 1). The color pattern and general external morphology data from the specimens falls within the spectrum of variation as reported by Hoogmoed et al. (2019) to C. auratus, see Table 1. Both specimens are from municipality of Pacoti (04°13’30”S; 38°55’24”W; 736 m above sea level; asl hereafter), state of Ceará, Brazil (Fig. 2). The Pacoti Municipality makes part of the Maciço de Baturité, a relictual moist forest enclave rounded by xeric Caatinga (Figueiredo and Barbosa, 1990). These new records of C. auratus extends the species range in 1200 km airline to the north from the municipality Barra do Choça (14°57’32”S; 40°32’56”W; 850 m a.s.l) in the Bahia State (Argolo, 2001), and 936 km airline to the southeast from Cacoal Farm, municipality Augusto Corrêa (01°01’18”S; 46°38’06”W; 20 m a.s.l) in the Pará State, (Cunha and Nascimento, 1982). There are moist forest enclaves known to occurs in Pernambuco, Paraíba and Ceará States along their highlands regions at northeastern portion of Brazil, and being each of them composed by mixed

Author for correspondence: castieleholanda@gmail.com

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C.H. Bezerra et al. - New record of Cercophis auratus to Caatinga

Figure 1. General view of Cercophis auratus based on the specimens from municipality of Pacoti, state of Ceará, Brazil. Dorsal view of body (A) of the individual female (CHUFC 2609), and lateral view of body (B) and dorsal (C) and lateral views (D) of head of the individual female (CHUFC 2169).

biota from Caatinga, Amazonia and Atlantic forest (Figueiredo and Barbosa, 1990; Borges-Nojosa and Caramaschi, 2003; Rodal et al., 2008; Batalha-Filho et al., 2013). Such forest relics represent putative past connections between Amazonia and Atlantic forest (Haffer, 1969; Vanzolini and Williams, 1970). These rainforest ecoregions are currently separated by known South American Dry Diagonal composed by Caatinga, Cerrado and Chaco (Ab’Saber, 1977), and

has been considered as a natural barrier to migration of rainforest species. Many evidences support the past contact between Atlantic and Amazonia rainforest (Rodal et al., 2008; Batalha-Filho et al., 2013), suggesting wetter periods in Pleistocen that granted the expansion of moist forest in area actually covered by open vegetation (Auler et al., 2004). There are many taxa with disjunct distribution along Amazonia and relictual forests on the Caatin-

Table 1. Sex, meristic and morphometric data of the two specimens of Cercophis auratus from municipality Pacoti, Ceará State, Brazil, and the range variation in the character found in this species according Hoogmoed et al., 2019. The exemplar CHUFC 2609 has a crushed head. SVL: Snout-vent-length.

Voucher number

Range variation

CHUFC 2169

CHUFC 2609

F or M

Dorsals

15/15/11

15/15/11 or 15/13/11

Ventrals

143

141

135 - 150

Subcaudals

155

153

144 - 171

Preocular

Postocular

2 or 3

Sex

262

Cuad. herpetol. 34 (2): 261-264 (2020) Supralabials

7-9

8 - 11

1 (divided)

Temporals

1+2+3

1 + 2 + 2 or 3

Anal

Divided

18 + 2

18 + 2 – 23 + 2

SVL (mm)

455

307

max. 508

Tail length (mm)

380

253

max. 412

Total length (mm)

835

560

max. 905

Tail/Total length (%)

42 - 54

Tail/SVL (%)

65 - 97

Grey-brown

Grey

Bronze, brown, grey or grey-brown

Infralabials Loreal

Maxillary teeth

Color

ga (e.g. Caecilia tentaculata, Borges-Nojosa et al., 2017), between relictual forests and Atlantic forest (e.g. Stenolepis ridleyi, Enyalius bibronii, Strobilurus torquatus, Euryoryzomys russatus, Borges and Caramaschi, 2003; Gurguel-Filho et al., 2015) or in the three rainforest types (e.g. Anolis fuscoauratus, Kentropix calcarata, Lachesis muta, Drymoluber dichrous; Nogueira et al., 2019; Borges and Caramaschi, 2003).

Therefore, the new records for Cercophis auratus, a species previously known along Atlantic forest with two disparate records on Amazonia, augment the disjunct pattern between both rainforest biomes, reinforcing putative past connections between Amazonia and Atlantic forest (Rodal et al., 2008; Batalha-Filho et al., 2013). Acknowledgments We thank Antonio Jorge Suzart Argôlo for help in the specimens identification. Literature cited

Figure 2. Distribution of Cercophis auratus. Star represent the type-locality and the new records of the species are marked by a triangle. The dots represent previously known records to C. auratus based on Hoogmoed et al. (2019) and Nogueira et al. (2019).

Ab’Saber, A.N. 1977. Os domínios morfoclimáticos da América do Sul. Primeira aproximação. Geomorfologia 53: 1-23. Argôlo, A.J.S. 2001. Uromacerina ricardinii (Liana Snake). Herpetological Review 32: 196-197. Auler, A.S.; Wang, A.; Edwards, R.L.; Cheng, H.; Cristalli, P.S.; Smart, M.L. & Richards, D.A. 2004. Quaternary ecological and geomorphic changes associated with rainfall events in presently semi-arid northeastern Brazil. Journal of Quaternary Sciences 19: 693-701. Batalha-Filho, H.; Fjeldsa, J.; Fabre, P.H. & Miyaki, C.Y. 2013. Connections between the Atlantic and Amazonian forest avifaunas represent distinct historical events. Journal of Ornithology 154: 41-50. Borges-Nojosa, D.M. & Caramaschi, U. 2003. Composição e análise comparativa da diversidade e das afinidades biogeográficas dos lagartos e anfisbenídeos (Squamata) dos brejos nordestinos: 489-540. In: Leal, I.R.; Tabarelli, M. & Silva, J.M.C (eds), Ecologia e Conservação da Caatinga. Editora UFPE, Recife. Borges-Nojosa, D.M.; Castro, D.P.; Lima, D.C.; Bezerra, C.H.; Maciel, A.O. & Harris, D.J. 2017. Expanding the known range of Caecilia tentaculata (Amphibia: Gymnophiona) to relict mountain forests in northeastern Brazil: linking Atlantic forests to the Amazon? Salamandra 53: 429-434. Cunha, O.R. & Nascimento, F.P. 1982. Ofídios da Amazônia: XVI – A espécie Uromacerina ricardinii (Peracca, 1897) na

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C.H. Bezerra et al. - New record of Cercophis auratus to Caatinga Amazônia Oriental (leste do Pará) (Ophidia: Colubridae). Boletim do Museo Paraense Emílio Goeldi 113: 1-9. Figueiredo, M.A. & Barbosa, M.A. 1990. A vegetação e flora na serra de Baturité. Coleção Mossoroense 747(B). Gurgel-Filho, N.M.; Feijó, A. & Langguth, A. 2015. Pequenos mamíferos do Ceará (marsupiais, morcegos e roedores sigmodontíneos) com discussão taxonômica de algumas espécies. Revista Nordestina de Biologia 23: 3-150. Haffer, J. 1969. Speciation in Amazonian Forest Birds. Science 165: 131-137. Hoge, A.R. 1959. Étude sur Uromacerina ricardinii (Peracca) (Serpentes). Memorias do Instituto Butantan 27: 77-82. Hoogmoed, M.S.; Fernandes, R.; Kucharzewski, C.; Moura-Leite, J.C.; Bérnils, R.S.; Entiauspe-Neto, O.M. & Santos, F.P.R. 2019. Synonymization of Uromacer Ricardinii Peracca, 1897 with Dendrophis aurata Schlegel, 1837 (Reptilia: Squamata: Colubridae: Dipsadinae), a rare South American snake with a disjunct distribution. South American Journal of Herpetology 14: 88-102. Lema, T. 1973. Ocorrência de Uromacerina ricardinii (Peracca, 1897) no Rio Grande do Sul e contribuição ao conhecimento desta rara espécie (Ophidia, Colubridae). Iheringia Série Zoologia 44: 64-73. Marques, O.A.V. 2000. Natural History Notes: Uromacerina ricardinii (Vine Snake). Predation and Prey. Herpetological Review 31: 180-181. Morato, S.A.A. & Bérnils, R.S. 1989. Dados sobre reprodução

de Uromacerina ricardinii (Peracca, 1897) (Serpentes: Colubridae) do Estado do Paraná-Brasil. Acta Biologica Leopoldensia 11: 273-278. Müller, P. & Ritter, C. 1978. Erstnachweis von Uromacerina ricardinii (Peracca, 1897) für den Staat von Santa Catarina (Brasilien) (Reptilia: Serpentes: Colubridae). Salamandra 14: 44. Nogueira, C.C.; Argôlo, A.J.S.; Arzamendia, V.; Azevedo, J.A.B.; Barbo, F.E. et al. 2019. Atlas of Brazilian Snakes: Verified Point-Locality Maps to Mitigate the Wallacean Shortfall in a Megadiverse Snake Fauna. South American Journal of Herpetology 14: 1-274. Peracca, M.G. 1897. Intorno ad una nuova specie di ofidio di S. Paulo (Brasile) riferibile al gen. Uromacer D. & B. Bolletino dei Musei di Zoologia ed Anatomia Comparata della R. Universita di Torino 12: 1-2. Rodal, M.J.N.; Barbosa, M.R.V. & Thomas, W.W. 2008. Do the seasonal forests in northeastern Brazil represent a single floristic unit? Brazilian Journal of Biololgy 68: 467-475. Vanzolini, P.E. & Williams, E.E. 1970. South American anoles: the geographic differentiation and evolution of the Anolis chrysolepis species group (Sauria: Iguanidae). Arquivos de Zoologia (São Paulo) 19: 125-298. Zamprogno, C. 1997. Uromacerina ricardinii (Cobra-cipó, Sao Paulo Sharp Snake). Brazil: Espírito Santo. Herpetological Review 28: 211.

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Defensive behaviors in two Proceratophrys species (Anura: Odontophrynidae) from central Brazilian Cerrado Afonso Santiago de Oliveira Meneses1,3, Bruno Alessandro Augusto Peña Corrêa2,3 Laboratório de Herpetologia, Departamento de Zoologia, Museu Paraense Emílio Goeldi. CEP 66040-170, Belém, Pará, Brazil. 2 Laboratório de Anatomia Comparativa de Vertebrados, Instituto de Biologia, Universidade de Brasília. Caixa Postal 04357. CEP 70910-900, Brasília, DF, Brazil. 3 Laboratório de Fauna e Unidades de Conservação, Departamento de Engenharia Florestal, Faculdade de Tecnologia, Universidade de Brasília. Caixa Postal 04357. CEP 70919-970 Brasília, DF, Brazil. 1

Recibida: 0 6

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Aceptada: 2 0

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E d itor As o c i a d o : C . B or te i ro doi: 10.31017/CdH.2020.(2020-039)

ABSTRACT Anurans present a wide array of defensive displays, which are exhibited in different phases of predation. There are several records of defensive behaviors for the genus Proceratophrys, most of them in species from the Atlantic Forest. Besides, few is known about such displays in Cerrado species. Herein, we report new defensive behaviors for P. goyana and P. vielliardi, of the P. cristiceps group. Both species presented immobility, body inflation and production of secretions. The stiff-legged behavior was commonly reported for the Atlantic Forest species of Proceratophrys, along with contraction. To date, body inflation, digging, and distress calls were only recorded in the P. cristiceps group. Our observations on defensive behaviors, account for the still poorly know natural history of the genus Proceratophrys. Key Words: Brazil; Neotropical region; Proceratophrys goyana; Proceratophrys vielliardi; South America.

Anurans can display various defensive strategies (Toledo et al., 2011), including a wide range of features, such as morphological, behavioral, and physiological traits to avoid predation (Duellman and Trueb, 1994). About 12 antipredator mechanisms were quoted for anurans, with 28 variations (Ferreira et al., 2019). These features are displayed in different phases of predation (Edmunds, 1974; Ferreira et al., 2019), and defensive behaviors are related to predator’s strategies for locating and subjugating anuran prey (Greenbaum, 2004). The genus Proceratophrys Miranda-Ribeiro, 1920 is composed of 41 species distributed across eastern and southern Brazil, with records also in Argentina and Paraguay (Frost, 2020). Of those species, 11 have been registered in the Brazilian Cerrado ecoregion, from where eight of them are considered endemisms: P. bagnoi, P. branti, P. cururu, P. dibernardoi, P. moratoi, P. strussmannae, P. rotundipalpebra, and P. vielliardi (Valdujo et al., 2012; Brandão et al., 2013; Martins and Giaretta, 2013). In the Distrito Federal region, within central

Brazilian Cerrado two species were recorded, P. goyana, and P. vielliardi (Brandão et al., 2012; Brandão and Araújo, 2001), both of them belonging to the P. cristiceps group (Giaretta et al., 2000). Proceratophrys goyana (Miranda-Ribeiro, 1937) has a wide distribution in the central portion of Brazil (Teixeira Jr et al., 2012; Martins and Giaretta 2013). It is associated with lotic waters both in forested and open physiognomies (Santoro and Brandão, 2014; Carvalho et al., 2020). Proceratophrys vielliardi Martins and Giaretta, 2011 has a narrow distribution in the central portion of the Cerrado (Martins and Giaretta, 2011; Brandão et al., 2012). This species is associated with seasonal rocky brooks and streams at high altitudes in open physiognomies (Martins and Giaretta, 2011; Brandão et al., 2012), such as “campo limpo” and “campo sujo” (sensu Ribeiro and Walter, 2008). Various defensive behaviors have been already reported for Proceratophrys, most of them correspond to species of the Atlantic Rain Forest ecoregion (Sazima, 1978; Weygoldt, 1986; Toledo and Zina, 2004; Costa et al., 2009; Moura et al., 2010; Toledo

Author for correspondence: afonso.santiago06@gmail.com

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Meneses and Corrêa - Defense Behaviors in two Proceratophrys species et al., 2011; Lourenço-de-Moraes and Lourençode-Moraes, 2012; Peixoto et al., 2013; Mângia and Garda, 2015; Ferreira et al., 2019; Table 1). Herein, we report the first records of defensive behaviors for two Cerrado species, P. goyana, and P. vielliardi. The individuals were found at Fazenda Água Limpa (15°58’31.5”S, 47°56’56.1”W, 1175 m a.s.l), and at APA do Cafuringa (15°33’13.6’’S, 47°51’59.8’’W, 769 m a.s.l.), Brasília, Distrito Federal, Brazil. None of the individuals were collected. On 16 August 2018, at 19:01 h, at APA do Cafuringa we found a male of P. goyana vocalizing in the leaflitter at the margins of a stream. When first spotted, it displayed crouching down behavior and remained immobile (Fig. 1A). When startled by our close presence, it jumped, inflated the body, and remained in this posture for some seconds, while also discharging secretions (Fig. 1B). Afterwards, it attempted to flee from us with small jumps into the leaflitter. On 25 October 2018, at 21:03 h, at Fazenda Água Limpa we found an individual of P. vielliardi vocalizing at the margins of a creek. When spotted, it stopped vocalizing and remained immobile. While manipulated, the specimen inflated the body, mostly the abdomen (puffing up behavior), and remained motionless for some seconds (Fig. 2A). After this, and once put on the floor, the frog attempted to flee back to the creek with fast and erratic jumps. We also

found a second individual of the same species on 03 November 2018, at 22:23 h, at the same locality, vocalizing at the margins of a creek. It also presented immobility when first spotted, followed by puffing up the body (again, mostly the abdomen) when startled, and remained motionless for a few seconds while the body was inflated. After that, it elevated the posterior part of the body, while lowering its head and discharging secretions (Fig. 2B). Immobility and fleeing are the most common defensive behaviors amongst anurans (Toledo et al., 2011). These behaviors combined with the cryptic coloration of the genus Proceratophrys (Toledo and Haddad, 2009), can be very effective in avoiding predation by visually-oriented predators (Marchisin and Anderson, 1978; Cooper et al., 2008). Along with immobility, crouching down may also aid in escaping from this kind of predators (Marchisin and Anderson, 1978; Toledo et al., 2011). Puffing up the body consists of filling the lungs with air (Toledo et al., 2011), to prevent subjugation by a potential predator (Toledo et al., 2011; Ferreira et al., 2019). Besides, it may also be displayed before a subjugation attempt, even in the ground, water, or vegetation (Toledo et al., 2011; Mângia and Garda, 2015), like was observed in the individuals we studied. Discharging noxious secretions is also another common defensive behavior in anurans when threatened,

Figure 1. Defensive displays of Proceratophrys goyana, crouching down (A) and puffing up the body, while discharging skin secretions (B) (Photos by ASOM).

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Figure 2. Defensive displays of Proceratophrys vielliardi, puffing up the body (A) and puffing up while discharging secretions (B) (Photos by ASOM).

and would avoid subjugation (Toledo et al., 2011; Ferreira et al., 2019). Production of secretions may happen synergistically with other behaviors, such as immobility, crouching down, and puffing up the body (Toledo et al., 2011). Stretching limbs was commonly reported as a defensive behavior for the Atlantic Rain Forest species of Proceratophrys (Weygoldt, 1896; Sazima,

1978; Toledo and Zina, 2004; Costa et al., 2009; Moura et al., 2010; Toledo et al., 2011; Peixoto et al., 2013; Ferreira et al., 2019). There are no records of the stiff-legged behavior in the P. cristiceps group, and other behaviors displayed by Proceratophrys (e.g. body inflation, digging, and distress calls) were to date only documented in this group (Toledo et al., 2011; Mângia and Garda, 2015; this work; Table

Table 1. Defensive displays recorded in the genus Proceratophrys.

Species

Defensive displays

Association

Reference

Proceratophrys appendiculata Stretching limbs

Atlantic Rain Forest Sazima, 1978

Proceratophrys avelinoi

Contraction

Atlantic Rain Forest Lourenço-de-Moraes and Lourenço-deMoraes, 2012

Proceratophrys boiei

Stretching limbs

Atlantic Rain Forest Toledo and Zina, 2004; Costa et al., 2009

Proceratophrys cristiceps

Puffing up the body, mouth gaping, Caatinga distress calls, fleeing

Mângia and Garda, 2015

Proceratophrys cururu

Digging

Toledo et al., 2011

Proceratophrys goyana

Puffing up the body, crouching Cerrado/Caatinga down, discharge of secretions, fleeing

Cerrado

This work

Proceratophrys melanopogon Stretching limbs

Atlantic Rain Forest Moura et al., 2010

Proceratophrys moehringi

Stretching limbs

Atlantic Rain Forest Weygoldt, 1986

Proceratophrys moratoi

Digging

Cerrado

Proceratophrys paviotti

Gland exposure posture

Atlantic Rain Forest Ferreira et al., 2019

Proceratophrys renalis

Stretching limbs

Atlantic Rain Forest Peixoto et al., 2013

Proceratophrys schirchi

Stretching limbs

Atlantic Rain Forest Ferreira et al., 2019

Proceratophrys vielliardi

Puffing up the body, discharge of Cerrado secretions, fleeing

Toledo et al., 2011

This work

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Meneses and Corrêa - Defense Behaviors in two Proceratophrys species 1). Except for P. concavitympanum, which presents distribution in transitional areas between Cerrado and Amazon Rain Forest (Ávila et al., 2012; Teixeira Jr et al., 2012), all the species of this group are associated with seasonally dry open physiognomies in Cerrado and Caatinga biomes (Brandão et al., 2013; Giaretta et al., 2000; Teixeira Jr et al., 2012). Since stretching limbs is a defensive behavior commonly presented in leaflitter anurans (Mângia and Santana, 2013), the absence of records of this display in the P. cristiceps group is possibly due to its association with open phytophysiognomies (Loebmann and Haddad, 2010; Brandão et al., 2012; Santoro and Brandão, 2014), where the leaflitter is scarce (Ribeiro and Walter, 2008). However, the stiff-legged behavior has already been recorded in a species that inhabit open physiognomies (e.g. Pleurodema bibroni, Kolenc et al., 2009, as death feigning), perhaps due to evolutionary constraints. Although not yet recorded, it is possible that the P. cristiceps species group also presents the stiff-legged behavior. Members of Odontophrynidae, other than Proceratophrys, present similar defensive behaviors. Puffing up the body, crouching down and production of secretions have been recorded in several species of Odontophrynus (Borteiro et al., 2018), but stretching limbs was only seen in O. americanus (Maffei and Ubaid, 2016; Borteiro et al., 2018). There are other records of the stiff-legged behavior within Odontophrynidae in species inhabiting the leaflitter, Proceratophrys spp. (Weygoldt, 1896; Sazima, 1978; Toledo and Zina, 2004; Costa et al., 2009; Moura et al., 2010; Toledo et al., 2011; Peixoto et al., 2013; Ferreira et al., 2019), and Macrogenioglottus alipioi, a species that also presents body inflation and tilting (Mira-Mendes et al., 2016). The natural history of species of the genus Proceratophrys, for instance regarding defensive and reproductive behaviors, is poorly known (Mângia and Garda, 2015; Carvalho et al., 2020). The increasing knowledge of its defensive displays would allow to study the evolution of these behavioral features in Odontophrynidae. Acknowledgements We are grateful to Nathalie Citeli for comments on the earlier version of the manuscript. We also thank Fazenda Água Limpa for support during fieldwork. The manuscript was also improved by suggestions made by Cuadernos de Herpetología reviewers.

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Ribeiro, 1920) (Anura, Odontophrynidae). Herpetology Notes 6: 479-430. Ribeiro, J.F. & Walter B.M.T. 2008. As principais fitofisionomias do bioma Cerrado: 151-212. In: Sano, S.M. & Almeida S.P. (eds.), Cerrado: Ambiente e Flora. Embrapa press, Brasília. Santoro, G.R.C.C. & Brandão, R.A. 2014. Reproductive modes, habitat use, and richness of anurans from Chapada dos Veadeiros, central Brazil. North-Western Journal of Zoology 10: 365-373. Sazima, I. 1978. Convergent defensive behaviour of two leaflitter frogs of southeastern Brazil. Biotropica 10: 158. Teixeira Jr, M., Amaro, R.C., Recoder, R.S., Dal Vechio, F., Rodrigues, M.T. 2012. A new dwarf species of Proceratophrys Miranda-Ribeiro, 1920 (Anura, Cycloramphidae) from the highlands of Chapada Diamantina, Bahia, Brazil. Zootaxa 3551: 25-42. Toledo, L.F. & Zina, J.P. 2004. Proceratophrys boiei (Smooth Horned Toad). Defensive behavior. Herpetological Review 35: 375. Toledo, L.F. & Haddad, C.F.B. 2009. Colors and some morphological traits as defensive mechanisms in anurans. International Journal of Zoology 2009: 1-12. Toledo, L.F.; Sazima, I. & Haddad, C.F.B. 2011. Behavioural defences of anurans: an overview. Ethology, Ecology & Evolution 23: 1-25. Wells, K.D. 2007. The ecology and behaviour of amphibians. The University of Chicago Press, Chicago. Weygoldt, P. 1986. Beobachtungen zur Ökologie und Biologie von Fröschen an einem neotropischen Bergbach. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere 113: 429-454.

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Cytogenetic analysis of Rhinella jimi (Stevaux, 2002) (Anura, Bufonidae) from northeastern Brazil Marcelo João da Silva1, Maria Rita dos Santos Cândido1, Flávia Manoela Galvão Cipriano1, Ana Paula de Araújo Vieira1, Tamaris Gimenez Pinheiro1, Edson Lourenço da Silva2 Universidade Federal do Piauí, campus Senador Helvídio Nunes de Barros, Rua Cícero Duarte, 905 - Junco, Picos - PI, CEP: 64607-670, Brasil. 2 Instituto Federal do Piauí, campus Picos, Avenida Pedro Marques de Medeiros, s/n - Pantanal, Picos- PI, CEP: 64606- 115, Brasil. 1

Recibida: 1 1 D i c i e m b r e 2 0 1 9 Revisada: 2 9

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Aceptada: 1 0

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E d it or As o c i a d o : D. B a l d o doi: 10.31017/CdH.2020.(2019-065)

ABSTRACT In this work we analyzed the karyotype of Rhinella jimi (Stevaux, 2002) (Anura, Bufonidae) from Picos (Piauí) in Northeastern Brazil. The chromosomes were examined using classical cytogenetic approaches (Giemsa, C-banding, and Ag-NOR staining). This species has 2n = 22 chromosomes, all metacentric or submetacentric. Heterochromatic segments were visualized at the centromeric region and the nucleolus organizer regions (NOR) were restricted to terminal regions of the short arms in pair 7. There was no evidence of heteromorphic sex chromosomes. The chromosomal analysis of R. jimi allowed us to identify a karyotype that is similar to many other species of Rhinella, in which the diploid number remains unchanged and without evidences of structural rearrangements. Key Words: Amphibians; Cytogenetic markers; C-banding; Karyotype evolution; Nucleolar organizing region.

Rhinella Fitzinger, 1826 is a genus that comprises 92 valid species of frogs and that is distributed from Lower Rio Grande Valley region of southern Texas (USA) and southern Sonora (Mexico) south, through tropical Mexico and to southern South America; one species in particular (Rhinella marina) is widely introduced (Antilles, Hawaii, Fiji, Philippines, Taiwan, Ryukyu Is. (Japan), New Guinea, Australia, and many Pacific islands) (Frost, 2020). All Rhinella species were previously grouped in the polyphyletic genus Bufo Laurenti, 1768, and currently are arranged in several species groups (i.e., R. crucifer, R. festae, R. granulosa, R. margaritifera, R. marina, R. spinulosa, and R. veraguensis) Pramuk, 2006; Chaparro et al., 2007; Moravec et al., 2014). However, there are species that have not been assigned to none of the existing groups, thus showing a taxonomic confusion in the group (Chaparro et al., 2007). Chromosomal data of Rhinella were reported as a relatively conserved karyotype, composed by a diploid number of 2n= 22 and NF= 44, such as in R. achalensis (Cei, 1972), R. achavali (Maneyro, Arrieta, and de Sá, 2004), R. arenarum (Hensel, 1867), R.

crucifer (Wied-Neuwied, 1821), R. diptycha (Cope, 1862), R. fernandezae (Gallardo, 1957), R. granulosa (Spix, 1824), R. henseli (Lutz, 1934), R. hoogmoedi Caramaschi and Pombal, 2006, R. icterica (Spix, 1824), R. jimi (Stevaux, 2002), R. margaritifera (Laurenti, 1768), R. marina (Linnaeus, 1758), R. ornata (Spix, 1824), R. proboscidea (Spix, 1824), R. pygmaea (Myers and Carvalho, 1952), and R. rubescens (Lutz, 1925) (Kasahara et al., 1996; Baldissera et al., 1999; Azevedo et al., 2003; Amaro-Ghilardi et al., 2008; Baraquet et al., 2011; Kolenc et al., 2013; Bruschi et al., 2019). Rhinella jimi (R. marina group) is mainly distributed in northeastern Brazil, however, it occurs from the state of Pará (Municipality of Bujaru) and Maranhão to Piauí, to the state of Espírito Santo, at altitudes of 15 to 500 m (Frost, 2020). Thus, in this work, we cytogenetically analyzed a population of R. jimi from northeastern Brazil by conventional staining, to better understand chromosomal characteristics and contribute to understanding the evolution of chromosomes in this widely distributed anuran species. All the individuals used were collected in the

Author for correspondence: ed.loren@ifpi.edu.br

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M. J. Silva et al. - Cytogenetic analysis of Rhinella jimi field under a governmental license issued by the Chico Mendes Institute for Biodiversity Conservation (ICMBio) number 47710-1/2015. Cytogenetic analyzes were performed on 10 specimens of Rhinella jimi (6 males and 4 females) collected in Picos (6° 54’ 22.9”; S 41° 33’ 49.8” W) in the Brazilian state of Piauí. Cellular suspensions were obtained from bone marrow using an in vitro colchicine 1% treatment for four hours according to Bertollo et al. (1978). Metaphase spreads were stained with 10% Giemsa in order to determine the standard karyotype of the sampled animals. The active NOR sites were detected by Ag-NOR staining according to Howell and Black (1980) and C-banding was carried out as described by Sumner (1972). Metaphases were photographed with a Nikon Eclipse microscope coupled to Thiachron camera and processed using the AMscope 3.7® software. The chromosomes were ordered in decreasing according to Levan et al. (1964), with modifications of Guerra et al. (1986). While few Rhinella species have been analyzed cytogenetically, the karyotypic macrostructure and the diploid number of 2n= 22 was observed in all populations studied so far. Here, we found the same characteristic for a new population of R. jimi from Northeastern Brazil (Fig. 1 A and B), suggesting that this chromosome number is common to the genus and has been maintained over time in all analyzed groups, such as the R. crucifer, R. granulosa and R. marina groups (see Kasahara et al., 1996; Baldissera et al., 1999; Baraquet et al., 2011; Amaro-Ghilardi et al., 2008; Kolenc et al., 2013; Bruschi et al., 2019). The conserved aspect of Rhinella species kar-

yotype is not restrict to the chromosome number aspects. In all Rhinella species analyzed so far, a highly conserved chromosomal morphology composed by biarmed chromosomes of metacentric and subcentric types were yet observed (Bruschi et al., 2019). However, some subtle differences such as the proportion between metacentric and submetacentric pairs have been reported (Amaro-Ghilardi et al., 2008; Baraquet et al., 2011). Nevertheless, the application of different criteria for chromosome classification may have interfered in such differences, rather than any actual variation between species in their chromosomal assemblies, and a thorough revision is needed. Heterochromatic blocks were detected in the centromeric regions of chromosomes (Fig. 2, A and B) and no secondary constrictions were evident. Regarding nucleolar organizing regions, only one pair corresponding to the short arm of pair 7 was observed (Fig. 1, C). Regarding the pattern of constitutive heterochromatin distribution in the R. jimi, the karyotype shows positive marks at the centromeric region of all chromosomes, corroborating previous results observed for some Rhinella species (e.g., Kasahara et al., 1996; Amaro-Guilardi et al., 2008; Bruschi et al., 2019). In our analysis, the NOR located in the short arm of chromosomal pair 7 in R. jimi are coincident with the NORs found for the species in others of the Rhinella marina group: R. icterica, R. rubescens and R. diptycha by Kasahara et al. (1996) and Amaro-Ghilardi et al. (2008), differing from these only in the location occupied on the chromosome.

Figure 1. Karyotypes of Rhinella jimi based on Giemsa staining: A, male metaphase and B, female metaphase; C, stained by the AgNOR method, showing the pair 7.

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Figure 2. Karyotypes of Rhinella jimi based on C-banding: A, male metaphase and B, female metaphase.

In conclusion, the chromosomal analysis of Rhinella jimi in this work allowed us to identify a karyotype very close to that observed in other Rhinella species, and in particular in the R. marina group, in which the diploid number remains unchanged and without evidence of structural rearrangements. Further studies considering more resolutive cytogenetic techniques are needed to test for the occurrence of hidden variation in the conserved karyotypes of Rhinella. Acknowledgements The authors are grateful to Instituto Federal de Educação, Ciência e Tecnologia do Piauí (IFPI), campus Picos (PROAGRUPAR-INFRA 033/2014) for logistic and financial support and to the anonymous reviewers for suggestions to our manuscript. Literature cited

Amaro-Ghilardi, R.C.; Silva, M.J.J.; Rodrigues, M.T. & Yonenaga-Yassuda Y. 2008. Chromosomal studies in four species of genus Chaunus (Bufonidae, Anura): localization of telomeric and ribosomal sequences after fluorescence in situ hybridization (FISH). Genetica, 134: 159-168. Azevedo, M.F.C.; Foresti, F.; Ramos, P.R.R. & Jim, J. 2003. Comparative cytogenetic studies of Bufo ictericus, B. paracnemis (Amphibia, Anura) and an intermediate form in sympatry. Genetics and Molecular Biology 26: 289-294. Baldissera, F.A.; Batistic, R.F. & Haddad, C.F.B. 1999. Cytotaxonomic considerations with the description of two new NOR locations for South American toads, genus Bufo (Anura: Bufonidae). Amphibia-Reptilia 20: 413-420. Baraquet, M.; Valetti, J.A.; Salas, N. & Martino, A. 2011. Redescription of the karyotypes of five species of the

family Bufonidae (Amphibia: Anura) from central area of Argentina. Biologia 66: 543-547. Bertollo, L.A.C.; Takahashi, C.S. & Moreira-Filho, O. 1978. Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erythrinidae). Brazilian Journal of Genetics 1: 103-120. Bruschi, D.P.; Sousa, D.Y.; Soares, A.; Carvalho, K.A.; Busin, C.S.; Ficanha, N.C.; Lima, A.P.; Andrade, G.V. & Recco-Pimentel, S.M. 2019. Comparative cytogenetics of nine populations of the Rhinella genus (Anura, Bufonidae) with a highlight on their conservative karyotype. Genetics and Molecular Biology 42: 445-451. Chaparro, J.C.; Pramuk, J.B. & Gluesenkamp, A.G. 2007. A new species of arboreal Rhinella (Anura: Bufonidae) from cloud forest of Southeastern Peru. Hepertologica 63: 203-212. Frost, D.R. 2020. Amphibian Species of the World: An Online Reference. American Museum of Natural History, New York, USA. Electronic Database. Available in: <http://research. amnh.org/herpetology/amphibia/index.html> Accessed in: March 28, 2020. Guerra, M.S. 1986. Reviewing the Chromosome Nomenclature of Levan et al. Revista Brasileira de Genética 9: 741-743. Howell, W.M. & Black, D.A. 1980. Controlled silver staining of the nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36: 1014-1015. Kasahara, S.; Silva, A.P.Z. & Haddad, C.F.B. 1996. Chromosome banding in three species of Brazilian toads (AmphibiaBufonidae). Brazilian Journal of Genetics 19: 237-242. Kolenc, F.; Borteiro, C.; Cotichelli, L.; Baldo, D.; Debat, C. M. & Candioti, F. V. 2013. The Tadpole and karyotype of Rhinella achavali (Anura: Bufonidae). Journal of Herpetology 47: 599-606. Levan, A.; Fredga, K. & Sandeberg, A. A. 1964. Nomenclature for centromeric position on chromosomes. Hereditas 52: 201-220. Moravec, J.; Lehr, E.; Cusi, J.C.; Córdova, J.H. & Gvodík, V. 2014. A new species of the Rhinella margaritifera species group (Anura, Bufonidae) from the montane forest of the Selva Central, Peru. ZooKeys 371: 35-56.

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Sumner, A. T. 1972. A simple technique for demonstrating centromeric heterochromatin. Experimental Cell Research 74: 304-306.

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Nota

Estudo dos hábitos alimentares das serpentes Sibynomorphus neuwiedi e Sibynomorphus mikanii (Squamata, Dipsadidae) de Minas Gerais, Brasil Vinícius José Pilate1,2, Fabiano Matos Vieira3, Bernadete Maria de Sousa1,4 Programa de Pós-graduação em Ecologia Aplicada ao Manejo e Conservação de Recursos Naturais, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Rua José Lourenço Kelmer, s/nº, Campus Universitário, São Pedro, Juiz de Fora, MG, 36036-900, Brasil. 2 Instituto Federal de Educação, Ciência e Tecnologia do Sudeste de Minas Gerais – Campus Juiz de Fora, Rua Bernardo Mascarenhas, 1.283, Fábrica, Juiz de Fora, MG, 36080-001, Brasil. 3 Programa de Pós-graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Avenida Brasil, 4.365, Manguinhos, Rio de Janeiro, RJ, 21040-900, Brasil. 4 Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora, Rua José Lourenço Kelmer, s/nº, Campus Universitário, São Pedro, Juiz de Fora, MG, 36036-900, Brasil. 1

Recibida: 0 2 D i c i e m b r e 2 0 1 9 Revisada: 1 9 D i c i e m b r e 2 0 1 9 Aceptada: 0 7

Julio

2020

E d itor As o c i a d o : M . C abre r a doi: 10.31017/CdH.2020.(2019-055)

ABSTRACT Study of the eating habits of snakes Sibynomorphus neuwiedi and Sibynomorphus mikanii (Squamata, Dipsadidae) from Minas Gerais, Brazil. Sibynomorphus neuwiedi (Ihering, 1911) and Sibynomorphus mikanii (Schlegel, 1837) are small sized snakes, nocturnal, non-venomous, snail eaters and commonly known as sleepy snakes. Studies about biology and ecology of both species are scarce. The goal of the present study was to analyze eating habits of the snakes S. neuwiedi and S. mikanii from Minas Gerais, Brazil, examining specimens in the Herpetological Collection of the UFJF - Reptiles. The 39 specimens of S. neuwiedi and 49 of S. mikanii analyzed where necropsied, sexed, and their gastrointestinal tract and digestive contents inspected in search of preys. The snakes showed similar diets: mollusks from species of the Family Veronicellidae, being registered the prey-species Sarasinula linguaeformis (Semper, 1885) in S. neuwiedi and Latipes erinaceus (Colosi, 1921) and Sarasinula sp. in S. mikanii. Key Words: Sleepy Snake; Diet; Malacophagy.

A alimentação é um importante aspecto da história natural de uma serpente, podendo influenciar seu período de atividade, seu comportamento e seu uso de habitat (Toft, 1985; Oliveira et al., 2001). Assim, uma das maneiras de compreender os processos que atuam no ecossistema onde esse animal está inserido é através do estudo sobre sua ecologia alimentar (Carreira Vidal, 2002). A diversidade de possibilidades na dieta das serpentes se deve em parte à utilização de diferentes habitats e evidencia o desenvolvimento de variadas especializações alimentares, que implicam especializações comportamentais e morfológicas associadas à detecção, subjugação, imobilização, captura, manuseio e ingestão das presas (Greene, 1983). As serpentes apresentam as maiores adaptações para a malacofagia – hábito alimentar especializado em moluscos – entre os répteis, havendo

aproximadamente 200 espécies de serpentes que predam gastrópodes terrestres e aquáticos, algumas destas altamente especialistas, como várias espécies das famílias Colubridae e Dipsadidae, onde alguns tipos de moluscos são os itens predominantes de suas dietas (Ferreira e Salomão, 2004). No Brasil há 17 espécies da família Dipsadidae, inofensivas aos seres humanos, sendo cinco destas do gênero Sibynomorphus Fitzinger, 1843, conhecidas popularmente como cobras “dormideiras”, entre as quais Sibynomorphus neuwiedi (Ihering, 1911) e Sibynomorphus mikanii (Schlegel, 1837), serpentes de pequeno porte, noturnas e úteis ao ser humano ao predar pragas agrícolas (Ferreira et al., 1986; Peters et al., 1986; Marques et al., 2001; Freitas, 2003; Ferreira e Salomão, 2004). Assim como muitas outras espécies de serpentes não peçonhentas, pouco se conhece sobre seus aspectos biológicos e ecológicos,

Autor para correspondencia: viniciuspilate@gmail.com

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V. Pilate et al. - Dieta de serpentes Sibynomorphus sendo o estudo destes aspectos necessários para embasar estratégias de conservação (Gibbons et al., 2000). O objetivo deste estudo foi analisar os hábitos alimentares das serpentes S. neuwiedi e S. mikanii de Minas Gerais, Brasil. O estudo foi desenvolvido no Laboratório de Herpetologia – Répteis da Universidade Federal de Juiz de Fora (UFJF) – MG. Foram analisadas 88 serpentes da Coleção Herpetológica da UFJF – Répteis (CHUFJF-Répteis), provenientes da Zona da Mata e do Campo das Vertentes de Minas Gerais, sendo 39 espécimes de S. neuwiedi e 49 de S. mikanii. As serpentes foram necropsiadas através de uma abertura na linha mediana ventral da cloaca até a garganta. O esôfago, o estômago, os intestinos delgado e grosso, e os conteúdos do tubo digestório foram examinados em placas de Petri contendo água sob microscópio estereoscópico em busca de presas. Após a triagem, os animais eviscerados foram conservados em etanol 70º e devolvidos à CHUFJF-Répteis. Os moluscos encontrados nos tubos digestórios das serpentes foram enviados para o Laboratório de Malacologia do Instituto Oswaldo Cruz (IOC) da Fundação Oswaldo Cruz (Fiocruz) – RJ, onde foram dissecados e examinados em placas de Petri contendo água sob microscópio estereoscópico, para a identificação, com base na morfologia do sistema reprodutor. Após a identificação, os moluscos foram novamente conservados em etanol 70º GL, etiquetados e depositados na Coleção de Moluscos / IOC / Fiocruz (CMIOC). Sobre os itens da dieta, foi aplicado o método qualitativo de Frequência de Ocorrência (FO%), definido pelo número de estômagos com determinado item dividido pelo número total de estômagos com conteúdo estomacal, e o método quantitativo de Abundância Numérica (N%), definido pelo valor de abundância de um item dividido pelo número total de itens alimentares. Nas 88 serpentes analisadas, foram encontrados 11 moluscos terrestres, sendo dez da Família Veronicellidae (Soleolifera) (um não pôde ser identificado por tratar-se de um indivíduo muito jovem), nos estômagos de nove destas serpentes: seis em S. neuwiedi (em quatro serpentes, duas com um molusco e duas com dois moluscos) e cinco em S. mikanii (em cinco serpentes, um por serpente), o que reforça os estudos de outros autores que registraram moluscos da família Veronicellidae nos estômagos de S. neuwiedi e S. mikanii (Ferreira et al., 276

1986; Marques e Sazima, 2004; Palmuti et al., 2009; Maia-Carneiro et al., 2012). Por não possuírem glifo (dente inoculador de veneno) (Ferreira et al., 1986) e nem o hábito de constrição, as serpentes do gênero Sibynomorphus se alimentam de presas que não oferecem retaliação: moluscos gastrópodes (Marques et al., 2001). A Família Veronicellidae é um grupo de 23 gêneros com aproximadamente 100 espécies amplamente distribuídas de gastrópodes pulmonados estritamente terrestres, herbívoros, noturnos, sinantrópicos, destituídos de concha e reconhecíveis por sua morfologia externa (Thomé, 1975). Tal grupo possui importância agrícola, médica e veterinária, uma vez que inclui espécies pragas prejudiciais a diversas culturas e outras que podem atuar como hospedeiros intermediários de nematoides parasitos de humanos e canídeos silvestres (Pereira e Gonçalves, 1949). Nem sempre é comum encontrar itens alimentares nos conteúdos digestórios de serpentes, já que pelo fato destas muitas vezes serem mantidas em laboratório em terrários por algum tempo (entre horas a semanas) antes de serem eutanasiadas e fixadas, há um intervalo suficiente para que as presas presentes nos estômagos das serpentes no ato de captura destas sejam digeridas, o que explicaria o número baixo de moluscos encontrados e de espécimes de serpentes contendo conteúdo alimentar (aproximadamente 10% das serpentes analisadas). Como os moluscos são invertebrados que contém o corpo rico em água, e as espécies de serpentes deste estudo são especialistas em predar moluscos terrestres sem concha (lesmas), também não foi possível encontrar resíduos das presas nos conteúdos intestinais das serpentes. Dois espécimes foram identificados como pertencentes à espécie Latipes erinaceus (Colosi, 1921) (Soleolifera, Veronicellidae), seis como Sarasinula linguaeformis (Semper, 1885) (Soleolifera, Veronicellidae) e dois como Sarasinula sp., não podendo ser determinadas as espécies, em um caso por tratar-se de espécime muito jovem e no outro por estruturas do sistema reprodutor utilizadas no diagnóstico estarem deterioradas. Os seis moluscos da espécie S. linguaeformis foram encontrados nos estômagos de S. neuwiedi, apresentando Frequência de Ocorrência (FO%) de 100% e Abundância Numérica (N%) de 100%. Com relação aos moluscos encontrados nos estômagos de S. mikanii, tanto o táxon L. erinaceus quanto o táxon Sarasinula sp. apresentaram FO% de 40% e N% de 40%, enquanto o táxon não identificado apresentou

Cuad. herpetol. 34 (2): 275-278 (2020) FO% de 20% e N% de 20%. Entre os moluscos da Família Veronicellidae utilizados como itens da dieta de S. neuwiedi, já haviam sido registrados na literatura os táxons Sarasinula sp., Belocaulus sp., Belocaulus angustipes (Heynemann, 1885), Phyllocaulis soleiformis (d’Orbigny, 1835) e Potamojanuarius lamellatus (Semper, 1885) (Palmuti et al., 2009; Maia-Carneiro et al., 2012). Também há registros de predação por essa serpente de gastrópodes terrestres com concha do gênero Bradybaena Beck, 1837 (Stylommatophora, Bradybaenidae) e límnicos do gênero Biomphalaria Preston, 1910 (Basommatophora, Planorbidae) (Ferreira et al., 1986; Ferreira e Salomão, 2004). Diferenças cranianas entre S. neuwiedi e S. mikanii foram relacionadas à alimentação (Ferreira et al., 1986; 1988; Santos et al., 2017). Em S. neuwiedi, em que também é registrado o consumo de caramujos, o mecanismo de retirada destes de suas conchas foi associado às características dos ossos cranianos (Ferreira et al., 1986; 1988). Em S. mikanii, as adaptações foram relacionadas à alimentação baseada apenas em lesmas, como dentes mandibulares maiores − adaptação às presas serem escorregadias (Peters, 1960; Ferreira et al., 1986, 1988). Entretanto, tomando por base os dados deste estudo somados às informações da bibliografia relacionada, conclui-se que predações por essas serpentes de moluscos com concha, ou mesmo de artrópodes – quilópodes e pequenos insetos −, são ocasionais. Ferreira et al. (1986) verificaram que S. neuwiedi apresentou nítida atividade noturna, fato que é relacionado ao constante forrageio, já que o conteúdo calórico de seu alimento – moluscos − é muito baixo (Arnold, 1993), gerando a necessidade de a serpente precisar ingerir um maior número de presas, o que explica o registro neste estudo de duas serpentes da espécie S. neuwiedi contendo dois moluscos no estômago, cada. Não é incomum encontrar várias presas nos estômagos de S. neuwiedi e S. mikanii (Barbo et al., 2011). Viera e Marques (2017) estudaram o horário de atividade de S. mikanii, tendo encontrado resultado comum ao registrado por outros autores: atividade predominantemente no período noturno. Ambas as espécies são especialistas em lesmas Veronicellidae (Marques et al., 2001; Agudo-Padrón, 2012), cuja atividade é predominantemente noturna (Junqueira et al., 2004), o que torna síncrona a atividade predador-presa. Foi verificada também neste estudo diferença

sazonal no número de presas nos conteúdos estomacais em ambas as serpentes analisadas: em S. neuwiedi houve maior proporção de presas nos conteúdos estomacais de serpentes coletadas na estação seca (67%) em relação às presas das serpentes coletadas na estação úmida (33%). Em S. mikanii houve maior proporção de presas nos conteúdos estomacais de serpentes coletadas na estação úmida (80%) em relação às presas das serpentes coletadas na estação seca (20%), o que é explicado pela maior necessidade calórica ligada às atividades de reprodução (Bozinovic e Rosenmann, 1988). Embora a estação úmida não tenha se correlacionado a um maior número de veronicelídeos também em S. neuwiedi, as espécies S. neuwiedi e S. mikanii apresentam atividade estimulada durante períodos mais úmidos (sob ou após chuvas) para busca de moluscos, e em momentos de seca é possível que permaneçam em repouso, já que o conteúdo calórico de seu alimento é baixo e rapidamente digerido, não sendo vantajoso realizar atividades de alimentação em períodos com pequena probabilidade de encontro das presas (Barbo et al., 2011; Agudo-Padrón, 2012). Tendo em vista que os dados de dieta dessas serpentes disponíveis na literatura resultaram de observações ocasionais na natureza, em cativeiro e de necropsia de poucos espécimes de coleções, foi necessário neste estudo analisar um grande número de conteúdos estomacais para determinar o alimento usual das espécies, já que para estabelecer os itens de dietas é desejável o exame de grande número de indivíduos (Marques e Puorto, 1994). Agradecimentos Agradecemos ao Instituto Federal de Educação, Ciência e Tecnologia do Sudeste de Minas Gerais (IF Sudeste MG) pelo apoio à qualificação, ao Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) pela Bolsa de Produtividade em Pesquisa (PQ) e às pesquisadoras Dra. S. Thiengo e Dra. S. Gomes pelas identificações dos moluscos. Literatura citada

Agudo-Padrón, A.I. 2012. Brazilian snail-eating snakes (Reptilia, Serpentes, Dipsadidae) and their alimentary preferences by terrestrial molluscs (Gastropoda, Gymnophila & Pulmonata): a preliminary overview. Biological Evidence 2: 2-3. Arnold, S.J. 1993. Foraging theory and prey-size-predator-size relations in snakes. 87-115. In: Seigel, R.A. & Collins, J.T. (eds.), Snakes: Ecology and Behavior. McGraw-Hill. New York.

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V. Pilate et al. - Dieta de serpentes Sibynomorphus Barbo, F.E.; Marques, O.A.V. & Sawaya, R.J. 2011. Diversity, natural history, and distribution of snakes in the municipality of São Paulo. South American Journal of Herpetology 6: 135160. Bozinovic, F. & Rosenmann, M. 1988. Energetics and food requirements of the female snake Philodryas chamissonis during the breeding season. Oecologia 75: 282-284. Carreira Vidal, S. 2002. Alimentación de los ofidios de Uruguay. Asociación Herpetológica Española. Monografías de Herpetología, 6. Barcelona. Ferreira, I.L.L. & Salomão, M.G. 2004. Reptilian predators of terrestrial gastropods. 427-481. In: Barker, G.M. (ed.), Natural Enemies of Terrestrial Molluscs. CABI Publishing. Wallingford. Ferreira, I.L.L.; Salomão, M.G. & Puorto, G. 1988. Mecanismo de tomada de alimento por serpentes tropicais moluscófagas (Sibynomorphus neuwiedi e Sibynomorphus mikanii). Adaptações morfológicas do esqueleto cefálico. Boletim de Fisiologia Animal 12: 81-88. Ferreira, I.L.L.; Salomão, M.G. & Sawaya, P. 1986. Biologia de Sibynomorphus (Colubridae – Dipsadinae) – reprodução e hábitos alimentares. Revista Brasileira de Biologia 46: 793-799. Freitas, M.A. 2003. Serpentes Brasileiras. Editora Malha-de-Sapo Publicações e Consultoria Ambiental. Bahia. Gibbons, J.W.; Scott, D.E.; Ryan, T.J.; Buhlmann, K.A.; Tuberville, T.D.; Metts, B.S.; Greene, J.L.; Mills, T.; Leiden, Y.; Poppy, S. & Winne, C.T. 2000. The global decline of reptiles, déjà vu amphibians. Bioscience 50: 653-666. Greene, H.W. 1983. Dietary correlates of the origin and radiation of snakes. American Zoologist 23: 431-441. Junqueira, F.O.; Prezoto, F.; Bessa, E.C.A. & D’ávila, S. 2004. Horário de atividade e etograma básico de Sarasinula linguaeformis Semper, 1885 (Mollusca, Veronicellidae), em condições de laboratório. Revista Brasileira de Zoociências 6: 237-247. Maia-Carneiro, T.; Dorigo, T.A.; Gomes, S.R.; Santos, S.B. & Rocha, C.F.D. 2012. Sibynomorphus neuwiedi (Ihering, 1911) (Serpentes; Dipsadidae) and Potamojanuarius lamellatus (Semper, 1885) (Gastropoda; Veronicellidae): a trophic relationship revealed. Biotemas 25: 211-213.

Marques, O.A.V.; Eterovic, A. & Sazima, I. 2001. Serpentes da Mata Atlântica. Guia ilustrado para a Serra do Mar. Holos. Ribeirão Preto. Marques, O.A.V. & Puorto, G. 1994. Dieta e comportamento alimentar de Erythrolamprus aesculapii, uma serpente ofiófaga. Revista Brasileira de Biologia 54: 253-259. Marques, O.A.V. & Sazima, I. 2004. História natural dos répteis da Estação Ecológica Juréia-Itatins. 257-277. In: Marques, O.A.V. & Duleba, W. (eds.), Estação Ecológica Juréia-Itatins: Ambiente Físico, Flora e Fauna. Holos. Ribeirão Preto. Oliveira, R.B.; Di-Bernardo, M.; Pontes, G.M.F.; Maciel, A.P. & Krause, L. 2001. Dieta e comportamento alimentar da cobra-nariguda, Lystrophis dorbignyi (Duméril, Bibron & Duméril, 1854), no litoral norte do Rio Grande do Sul, Brasil. Cuadernos de Herpetología 14: 117-122. Palmuti, C.F.S.; Cassimiro, J. & Bertoluci, J. 2009. Food habits of snakes from the RPPN Feliciano Miguel Abdala, an Atlantic Forest fragment of southeastern Brazil. Biota Neotropica 9: 263-269. Pereira, H.F. & Gonçalves, L.I. 1949. Caramujos, caracóis e lesmas nocivos e meios de combate. O Biológico 15: 65-73. Peters, J.A. 1960. The snakes of the subfamily Dispsadinae. Miscellaneous Publications of the Museum of Zoology 114: 1-224. Peters, J.A.; Orejas-Miranda, B.; Donoso-Barros, R. & Vanzolini, P.E. 1986. Catalogue of the Neotropical Squamata. Part I: snakes. Part II: Lizards and Amphisbaenians. Revised edition. Smithsonian Institution Press. Washington. Santos, M.M.; Silva, F.M.; Hingst-Zaher, E.; Machado, F.A.; Zaher, H.E.D. & Prudente, A.L.C. 2017. Cranial adaptations for feeding on snails in species of Sibynomorphus (Dipsadidae: Dipsadinae). Zoology 120: 24-30. Thomé, J.W. 1975. Os gêneros da família Veronicellidae nas Américas (Mollusca; Gastropoda). Iheringia, Série Zoologia 48: 3-56. Toft, C.A. 1985. Resource partitioning in amphibians and reptiles. Copeia 1985: 1-21. Viera, N.F.T. & Marques, O.A.V. 2017. Daily activity of neotropical dipsadid snakes. South American Journal of Herpetology 12: 128-135.

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Dietary composition and feeding strategy of Leptodactylus fuscus (Anura: Leptodactylidae) from a suburban area of the Caribbean Region of Colombia Luis F. Montes1,2, Oscar F. Hernández1, Jill L. Martínez1, Jose A. Jarava1, Jorge A. Díaz3,4 Facultad de Educación y Ciencias, Universidad de Sucre, Cra 28 # 5-267 Barrio Puerta Roja- Sincelejo (Sucre), Colombia. 2 Programa de Pós-Graduação em Ecologia e Evolução, Instituto de Ciências Ambientais, Químicas e Farmacêuticas, Universidade Federal de São Paulo, Rua Prof. Artur Riedel, Jd. Eldorado, 09972-270, Diadema, São Paulo, Brazil. 3 Grupo de Investigación en Zoología y Ecología, Universidad de Sucre, Sincelejo, Colombia. 4 Programa de Pós-Graduação em Ecologia e Conservação, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Avenida Costa e Silva, Campo Grande, 79070-900, Mato Grosso do Sul, Brazil. 1

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E d i t o r A s o c i a d o : P. P e l t z e r doi: 10.31017/CdH.2020.(2020-012)

ABSTRACT The use of trophic resources by anurans may be influenced by sexual dimorphism, ontogenetic variation and resources available in the environment. However, most studies on anuran feeding behavior lack of environmental prey availability data. In this study, the dietary composition and the feeding strategy of Leptodactylus fuscus were evaluated considering the availability of potential prey in a sub-urban area of the Colombian Caribbean Region. Additionally, differences in diet composition between adult and juvenile’ frogs were assessed. Prey items were obtained through forced regurgitation technique and prey availability was assessed using pitfall traps. The importance of each prey category and prey selectivity were evaluated through a relative importance index and a food selection index, respectively. Twenty-four stomachs were analyzed, being Hymenoptera the most important prey category and the most abundant resource in the environment. The population of L. fuscus showed a low prey selectivity and prey size was associated with frog’s body size. However, there was no variation in numeric and volumetric dietary composition related to ontogeny. Considering the relationship between the diet and prey availability, our results evidenced L. fuscus exhibits a generalist and opportunistic feeding behavior, which highlight the importance of including information on prey availability to better understand the anurans dietary behavior. Key Words: Anurans; Diet; Prey Availability; Prey Selectivity.

The use of trophic resource by anurans is an important aspect related to their natural history and represents basic information associated with their role in community dynamics and ecosystem functioning (Cortés-Gomez et al., 2015). Traditionally, it has been recognized that anurans feed on a continuum of two strategies that range from active to passive search for prey (Simon and Toft, 1991). Anuran feeding strategies can be influenced by several factors, such as specific nutrient requirements, energy costs associated with foraging, risk of predation and prey availability (Berazategui et al., 2007). Thus, prey availability is a key aspect in order to understand anurans feeding behavior, but this topic is usually neglected in amphibian dietary studies (de Oliveira

et al., 2019). Anurans diet can also show sexual and ontogenetic variations regarding composition, size and quantity of prey (Rodrigues et al., 2004; Maragno and Souza, 2011). In this sense, females can eat more prey than males, adults can eat larger prey than juveniles and larger individuals can eat prey with larger sizes than small individuals (Sugai et al., 2012; Junqueira et al., 2016). In general, animals that cannot chew like frogs are limited to the consumption of prey that fits in the mouth and, consequently, ontogenetic changes allow larger individuals to eat larger prey (Lima and Moreira, 1993). Leptodactylus fuscus is a terrestrial and nocturnal frog, with wide distribution in the Neotropical

Author for correspondence: lfmontesbenitez@gmail.com

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L. Montes et al. - Diet and feeding strategy of Leptodactylus fuscus region, generally associated to grasslands, savannahs, swampy areas, degraded forest and urban areas (Reynolds et al., 2004; Frost, 2020). There are several studies on diet composition of L. fuscus, which indicate a generalist and opportunist feeding behavior, but none of them considers prey availability (Sugai et al., 2012; Junqueira et al., 2016; Santana et al., 2019). Thus, in the present study, the diet composition and the feeding strategy of Leptodactylus fuscus in a suburban area of the Colombian Caribbean region were evaluated, taking into account the availability of prey. In addition, differences in diet composition between adults and juvenile frogs, as well as the association of maximum prey size and body size of frogs were evaluated. This study was carried out in the Sincelejo municipality, department of Sucre, Colombia (9° 18’ 58.1”N, 75° 23’ 17.3”W; 213 m a.s.l). Three field trips were conducted between August and October 2016, corresponding to the rainy season. The frogs were collected during night, between 19:00 and 23:00 hs using the technique of systematic survey by visual encounters (Crump and Scott, 2001). The snout-vent length (SVL) of each frog was measured using a Vernier caliper (0.01 mm accuracy) and the stomach contents were removed through forced regurgitation technique; stomach contents were preserved in 70% ethanol (Rivas et al., 1996). Frogs were classified in adults and juveniles taking into account body size characteristics (Heyer, 1978). An analysis of sexual variation of diet was not considered because it was not possible to determine the sex of all individuals in the field. In order to evaluate the availability of potential prey, five pitfall traps were installed separated 10m from each other, in a transect of 50m in the same area where frogs were collected (Campbell and Christman, 1982). These pitfall traps consisted of plastic cups of 250 ml and 10 cm diameter with ethanol and were active between 18:00 and 6:00 hours on the night of sampling. All arthropods collected in the pitfall traps were considered potential prey and were preserved in 70% ethanol. Stomach contents were identified at the level of order using taxonomic keys (McGavin, 2000). To determine the volume of different prey categories, photographs of each prey item were taken using an assembly with metric reference and then, the images were scanned through tps2DIG program. The length (L) and width (W) of each prey item were measured and the volume was calculated using the ellipsoid formula: V = 4/3 π (length / 2) (width / 2)2, 280

according to Dunham (1983). The importance of each prey category in the population diet was calculated using the Index of Relative Importance (IRI) of Pinkas et al. (1971), according to the following equation: IRI = (N + V) * F; where N, V and F represents the numerical, volumetric and the frequency of occurrence percentages of each prey category in the diet, respectively. Additionally, a hierarchical classification of prey categories was made using the ranking index (RI) of Montori (1991). Chao 1 and ACE estimators were calculated to know if the number of stomachs analyzed represents a sufficient sample to characterize the diet of L. fuscus, using stomachs as sample units and abundance data of prey categories in Estimates version 9.1.0 (Colwell, 2013). To determine the association between prey size and frogs body size a regression analysis was performed, with the volume of the largest prey in each frog as a dependent variable and the SVL as independent variable. In order to evaluate prey selectivity the Jacobs selectivity index was calculated for the two most important prey types (Jacobs, 1974). To evaluate if volumetric and numeric composition of prey differs between adults and juveniles one-way ANOSIM tests were performed (Clarke, 1993). In this sense, Euclidean distance and Bray Curtis index were used for volumetric and numeric composition tests respectively, through the software PAST version 3.24 (Hammer et al. 2001). Twenty-four specimens were captured, of which seven were juveniles and 17 adults (six juveniles and 13 adults had stomach contents). Mean SVL of juveniles was 33 mm (SD=1.63mm, range=31-36mm) and mean SVL of adults was 45mm (SD=4.23mm, range=41-57mm). A total of 92 prey items were retrieved from stomach contents, belonging to 12 categories and 10 orders (Table 1). Chao 1 and ACE estimated 16.45 and 14.67 prey categories respectively, which are values relatively close to the observed number of prey categories for L. fuscus in the present study. Hymenoptera and Acariformes showed the highest value of IRI in the diet of L. fuscus and were classified, according to the ranking index, as fundamental and secondary prey respectively (Table 1). On the other hand, Scolopendromorpha, Coleoptera and Haplotaxida were classified as accessory prey types, and Gastropoda, Diptera, Hemiptera, Blattodea and Polydesmida were accidental prey in the diet (Table 1). Adults and juveniles did not differ regarding volumetric composition (R= -0.054, p= 0.63) neither

Cuad. herpetol. 34 (2): 279-283 (2020) Table 1. Diet of Leptodactylus fuscus. N: total number of items; % N: numeric percentage; %F: frequency of occurrence percentage; %V: volumetric percentage; IRI: index of relative importance; RI: ranking index.

Class

Prey category

IRI

Hymenoptera

16.3

33.33

0.08

546.14

100

Coleoptera

10.87

12.5

5.92

209.87

38.43

Diptera

3.26

12.5

2.97

77.89

14.26

Hemiptera

2.17

8.33

3.31

45.7

8.37

Blattodea

1.09

4.17

0.78

7.78

1.42

Arachnida

Acariformes

21.74

16.67

0.06

363.32

66.52

Chilopoda

Scolopendromorpha

1.09

4.17

54.64

232.2

42.52

Diplopoda

Polydesmida

1.09

4.17

0.16

5.2

0.95

Mollusca

Gastropoda

7.61

16.67

0.51

135.31

24.78

Clitellata

Haplotaxida

7.61

4.17

30.97

160.74

29.43

Eggs

23.91

4.17

0.12

100.14

18.34

Larvae

3.26

4.17

0.49

15.63

2.86

Insecta

Other categories

numeric composition of prey (R= 0.044, p= 0.22). In addition, the volume of the largest prey was positively and significantly related with frogs SVL (R2 = 0.54, p <0.001). Likewise, Scolopendromorpha and Haplotaxida were found only in the stomachs of the largest individuals. A total of 2643 arthropods were collected through pitfall traps and were identified 10 potential prey categories, being Hymenoptera the most abundant, followed by Collembola and Acariformes (Fig. 1). Among the 10 potential prey categories, six were retrieved from the stomachs of L. fuscus (Fig. 1) and according to Jacobs’ Index, the two most important prey in the diet were consumed opportunistically

Figure 1. Numerical proportion of different prey categories in the environment and diet of Leptodactylus fuscus.

(Hymenoptera, J=0.034; Acariformes, J=0.024). The relationship between the diet of L. fuscus and the availability of potential prey was registered here. The low values in the selectivity index and the variety of consumed prey categories suggest a generalist feeding behavior by L. fuscus, similarly to that observed by de Oliveira et al. (2019) in Leptodactylus latrans, where the individuals consumed prey with higher availability in the environment. The generalist feeding behavior of L. fuscus was documented in others studies, but none of that considered the availability of prey (De-Carvalho et al., 2008; Sugai et al., 2012; Santana et al., 2019). On the other hand, the high consumption of small prey in L. fuscus suggests an opportunistic feeding strategy, as had previously been registered in this and other species of the genus Leptodactylus (Rodrigues et al., 2004; López et al., 2005a-b; De-Carvalho et al., 2008; Solé et al., 2009; Sugai et al., 2012), likewise, the consumption of large prey by some individuals may suggest a possible sit and wait feeding strategy (Solé and Rodder, 2009). The high consumption of Hymenoptera and Acari may be associated with the high availability of these prey in the study area. Likewise, the high intake of these prey categories differs from those found in other studies (De-Carvalho et al., 2008; Sugai et al., 2012; Junqueira et al., 2016; Santana et al., 2019), which Coleoptera and Orthoptera were the most important prey. These differences may be associated with the type of environment where frogs live, that determines the diversity of potential prey (Santana et al., 2019). On the other hand, the obser281

L. Montes et al. - Diet and feeding strategy of Leptodactylus fuscus ved association of prey size with body size has been registered in other species of genus Leptodactylus, and can be attributed to the fact that larger individuals can eat large prey (e.g. Lajmanovich, 1994; Maneyro et al., 2004; Rodrigues et al., 2004; Lopez et al., 2005a). Furthermore, the intake of some prey categories by few individuals, may suggest the existence of individual specialization in the population or body size constraints on prey types (Amundsen et al., 1996; Cloyed and Eason, 2017). Likewise, an increase in body size can produce an increase in the variety of prey that could be consumed (Solé and Rodder (2009), which can cause variation in the diet according to ontogeny, being associated with the energy requirements, foraging modes, microhabitat use variation between juveniles and adults and prey availability (Rodrigues et al., 2004; Lima and Magnusson 2000; Sugai et al., 2012). However, in this study, adults and juveniles had similar volumetric and numerical composition of consumed prey, which may be associated with the generalist feeding behavior and the availability of prey in the environment. In conclusion, the diet of the studied population of L. fuscus is composed mainly of arthropods, exhibiting low prey selectivity and a food intake based mainly on the most abundant prey in the environment, showing an opportunist and generalist foraging behavior. These results demonstrate the importance of including resource availability data in feeding studies to achieve a better understanding of the trophic ecology of anurans. Acknowledgments The authors thank the Museo de Zoología de la Universidad de Sucre (MZUSU) for providing equipment and logistical support. To Paula Ojeda for her help to improve the English in the manuscript. To Pedro Álvarez, Pedro Atencia, Jesús Jaraba and Juan Tovar for their contributions during field work and manuscript development. Jorge Díaz thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq scholarship No. 133108/2018-0). Literature cited

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New dietary records and geographic variation in the diet composition of the snake Philodryas nattereri in Brazil Raul Fernandes Dantas Sales1, Juliana Delfino Sousa2, Carolina Maria Cardoso Aires Lisboa3, Paulo Henrique Marinho3, Eliza Maria Xavier Freire1, Marcelo Nogueira de Carvalho Kokubum2,4,5 Laboratório de Herpetologia, Departamento de Botânica e Zoologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, Campus Universitário Lagoa Nova, 59072-970, Natal, RN, Brazil. 2 Laboratório de Herpetologia, Unidade Acadêmica de Ciências Biológicas, Centro de Saúde e Tecnologia Rural, Universidade Federal de Campina Grande, Jatobá, 58708-110, Patos, PB, Brazil. 3 Programa de Pós-graduação em Ecologia, Departamento de Ecologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, 59072-970, Natal, RN, Brazil. 4 Programa de Pós-graduação em Ciências Florestais, Centro de Saúde e Tecnologia Rural, Universidade Federal de Campina Grande, Jatobá, 58708-110, Patos, PB, Brazil. 5 Programa de Pós-graduação em Ecologia e Conservação, Universidade Estadual da Paraíba, 58429-500, Campina Grande, PB, Brazil. 1

Recibida: 1 4

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Aceptada: 2 1

Agosto

2020

Editor Asociado: V. Arzamendia doi: 10.31017/CdH.2020.(2020-015)

ABSTRACT In this study, we report new dietary data about the South American dipsadine snake Philodryas nattereri in the Caatinga ecoregion of northeastern Brazil. Our observations in the wild include predation on a large-sized lizard, an adult bird, venomous toads, a snake, bird chicks inside nests, and a mammal. Besides that, we compared the diet composition of P. nattereri between the Caatinga and the Cerrado ecoregions of Brazil, by pooling our original data with all available literature records. We found a significant difference in the diet of P. nattereri between these two regions: lizards comprise the predominant prey category for P. nattereri in the Caatinga, whereas mammals stand out as the most reported prey in the Cerrado. Our results evidence generalist and opportunistic feeding habits of P. nattereri, one of the most common snake species in Brazil. Key Words: Caatinga; Cerrado; Dipsadinae; Feeding habits; Semi-arboreal habits.

Data on the natural history of snakes are important for studies on evolutionary biology and ecology (Greene, 1997; Martins and Oliveira, 1998). Furthermore, regional life-history data can contribute to an understanding of the patterns of ecological geographic variation of widely distributed snake species (Coelho et al., 2019). Some snakes are known to show geographic variations in morphology (King, 1989; How et al., 1996), habitat use (Shine, 1987), reproductive tactics (Seigel and Ford, 2001), defensive behavior (Sweet, 1985), foraging behavior and diet composition (Arnold, 1977; Luiselli et al., 2005; Coelho et al., 2019). However, detailed knowledge on feeding ecology and behavior of many snakes are still poorly understood, particularly for neotropical species (Guedes et al., 2018).

The Paraguay Green Racer, Philodryas nattereri Steindachner, 1870, is a dipsadine snake widely distributed in the South American dry diagonal, from northeastern (NE) Brazil to Paraguay, occurring in the Caatinga, Cerrado and Pantanal ecoregions (Guedes et al., 2014). It has diurnal activity and is considered a primarily terrestrial snake, but may also perch on trees and shrubs (Mesquita et al., 2011, 2013). In the semiarid Caatinga of NE Brazil, P. nattereri is among the most common and abundant species of local snake assemblages, both in natural and in disturbed environments (Mesquita et al., 2013; Guedes et al., 2014). Like with most of its congeners, its diet can be classified as generalist and includes several small vertebrates such as lizards, birds, mammals and anurans (Vitt and Vangilder,

Author for correspondence: mnckokubum@gmail.com

285

R. F. D. Sales et al. - Diet of Philodryas nattereri 1983; França et al., 2008; Mesquita et al., 2011). Moreover, natural episodes of ophiophagy have also been reported in this species (Mesquita et al., 2011; Guedes, 2017; Coelho-Lima et al., 2019). In this study, our goals were: (1) to report a compilation of predation events recorded by us in the Caatinga of northeastern Brazil involving different vertebrates species, most of them previously not reported as prey of P. nattereri; and (2) to present a literature review of all prey items reported for P. nattereri throughout its geographic distribution in Brazil. The combination of our original data with data from literature allowed us to test for geographic differences in the diet composition of P. nattereri between the Caatinga and the Cerrado, the two largest non-strictly forest ecoregions of Brazil. The predation events described in this study were opportunistically recorded in the states of Rio Grande do Norte (RN) and Pernambuco (PE), between 2017 and 2020. One predation event was recorded by RFDS in João Câmara municipality, RN state (municipality’s central coordinates: 5.5344° S; 35.8131° W), and eight predation events were recorded by JDS in Brejinho Municipality, PE state (municipality’s central coordinates: 7.3473° S; 37.2868° W). We also present a predation event registered by an external collaborator (Cícero Lajes) in Angicos municipality, RN state (municipality’s central coordinates: 5.6582° S; 36.6097° W), who kindly provided the photos and videos, together with the information about the observation. All these sites are in the Caatinga ecoregion of northeastern Brazil, where the climate is semiarid (BSh according to Köppen), hot and dry, with annual precipitation between 500 and 800 mm (Velloso et al., 2002). None of the specimens (predators and prey) were collected, and the records were based on natural observations and photographs/videos. In order to compile the available data about diet composition of P. nattereri, we made an extensive search in the literature in on-line bibliographic databases (Web of Science JSTOR, Scielo, Scopus, and Google Scholar), looking for dietary records of the species using a combination of the keywords “Paraguay Green Racer” or “Philodryas nattereri” plus “diet” or “feeding habits” or “prey”. We also used a “snowball” method, searching for records in the “References” section of found articles. Unpublished predation records from dissertations, theses, and works published in congresses were not considered in the review. We split the records in relation to the 286

ecoregion of Brazil where they were made (Caatinga versus Cerrado). We present data on prey types by the taxonomic level of species when provided by the author. Higher taxonomic levels (e.g. genus, family) were pooled in the “unidentified” subcategory of each defined prey category (amphibians, lizards, snakes, mammals, birds, and vertebrate eggs). We considered in the review only studies where authors provided the number of prey items ingested by P. nattereri. To test for geographic differences in the diet composition between the Caatinga and the Cerrado, we used the Kolmogorov-Smirnov twogroup test, considering the numeric proportions of prey categories (Fialho et al., 2000). The predation episodes are described below in chronological order. The first observation was recorded by JDS on 14 October 2017, at 09:40, in “Sítio Degredo” (7.3164° S; 37.2794° W, 755 m a.s.l.), Brejinho municipality, PE state. The vegetation physiognomy in this site is arboreal caatinga, with some disturbed areas due to cattle and agricultural activities. An adult individual of P. nattereri (sex not determined; total length around 150 cm) was observed on the ground below a tree subduing an adult individual (probably a female; total length around 50 cm) of the Common Green Iguana, Iguana iguana (Linnaeus, 1758). When spotted, the snake was already constricting and adjusting the lizard in the mouth (Fig. 1A). Ingestion process lasted about 20 minutes, and the snake stayed motionless for several minutes in the same place after completing swallowing. The second observation was recorded by JDS on 31 January 2018, at 13:38, in “Sítio Fechado” (7.2992° S; 37.2978° W, 791 m a.s.l.), Brejinho municipality, PE state. Similar to “Sítio Degredo”, the vegetation physiognomy in this site is arboreal caatinga, with some disturbed areas due to cattle and agricultural activities. An adult individual of P. nattereri (sex not determined; total length around 100 cm) was observed on bare soil below a tree subduing an adult individual of the Picui ground-dove, Columbina picui (Temminck, 1813). When spotted, the snake was biting and holding the bird’s neck on its mouth (Fig. 1B) but released the prey and quickly fled after human approximation. The observer checked the bird on the ground and confirmed that it was already dead. The snake would clearly succeed in the predation without the human interference. The third observation was recorded by RFDS on 02 May 2018, at 16:18, in “Maria da Paz” com-

Cuad. herpetol. 34 (2): 285-293 (2020)

Figure 1. Prey items of the snake Philodryas nattereri reported in this study: A) Iguana iguana; B) Columbina picui; C) Rhinella jimi; D) Lygophis dilepis; E) Rhinella granulosa; F) chicks of Columbina picui; G) Galea spixii; H) Coereba flaveola.

munity (5.4570째 S; 35.8905째 W, 195 m a.s.l.), Jo찾o C창mara municipality, RN state. The vegetation physiognomy in this site is shrubby caatinga, with some disturbed areas due to wind farms, cattle and agricultural activities. An adult individual of P. nattereri (sex not determined; total length around 150 cm) was observed on bare soil in the margins

of dense shrubby vegetation ingesting a juvenile individual (total length around 10 cm) of the Cururu toad, Rhinella jimi (Stevaux, 2002). When spotted, the snake was already adjusting the puffed-up toad in the mouth. The toad was swallowed belly up and head first (Fig. 1C), and the ingestion process lasted 15 min; after that, the snake remained motionless for 287

R. F. D. Sales et al. - Diet of Philodryas nattereri about three minutes, and then entered the shrubby vegetation and disappeared from the observer’s sight. The fourth observation was recorded by a group of cyclists on 09 September 2018, at 08:30, in the roadside of the highway BR 304 (5.6894° S; 36.3500° W, 153 m a.s.l.), Angicos municipality, RN state. The vegetation physiognomy in this site is disturbed shrubby caatinga due to cattle and agricultural activities, and the proximity of the highway facilitates anthropogenic disturbance. An adult individual of P. nattereri (sex not determined; total length around 100 cm) was spotted trying to subdue and swallow an adult individual of the Lema’s striped snake, Lygophis dilepis Cope, 1862 (Fig. 1D). Although the L. dilepis was thinner than the P. nattereri, the two snakes had similar sizes, with the predator slightly larger than the prey. The P. nattereri kept a bite on the head region of the L. dilepis, presumably poisoning the prey with the rear fangs. After about five minutes, the two snakes where in the same position, but the observers left the site, so we cannot be sure if the attempted predation was successful or not. The fifth observation was recorded by JDS on 20 March 2019, at 11:40, in “Sítio Fechado” (7.2992° S; 37.2978° W, 791 m a.s.l.), Brejinho municipality, PE state. An adult individual of P. nattereri (sex not determined; total length around 150 cm) was observed on bare rocky soil ingesting a juvenile individual (total length around 5 cm) of the Cururu toad, Rhinella granulosa (Spix, 1824). The observer located the individuals (predator and prey) because the toad emitted distress calls after being captured by the snake. When spotted, the snake was already adjusting the puffed-up toad in the mouth, which was swallowed belly down and head first (Fig. 1E). Ingestion lasted about 3 min, and the snake left the site immediately after swallowing the toad. The sixth observation was recorded by JDS on 22 March 2019, at 11:36, in “Sítio Fechado” (7.2992° S; 37.2978° W, 791 m a.s.l.), Brejinho municipality, PE state. An adult individual of P. nattereri (sex not determined; total length around 150 cm) was observed perched on a tree (Anacardium occidentale L.) attempting to reach a nest of the Sayaca tanager, Tangara sayaca (Linnaeus, 1766). The bird parents mobbed the snake continuously, flying towards it and emitting alarm calls, which made the snake to withdraw approximation to the nest and move to the upper branches of the tree. During the snake’s approach to the nest, two chicks fell to the ground 288

and were immediately assisted by the parents. The predation attempt was thereby unsuccessful. The seventh observation was recorded by JDS on 16 September 2019, at 14:15, in “Sítio Fechado” (7.2992° S; 37.2978° W, 791 m a.s.l.), Brejinho municipality, PE state. An adult individual of P. nattereri (sex not determined; snout-vent length around 180 cm) was observed perched on a tree (Citrus × sinensis Macfad.), moving up to the higher branches. After 15 min, at 14:30, the snake moved down towards a nest of the Picui ground-dove, Columbina picui (Temminck, 1813). The snake stopped right above the nest, when an adult individual of C. picui (probably one of the parents) flew towards it but quickly moved away. The P. nattereri then captured a chick in the nest (Fig. 1F), which was swallowed in just 30 seconds; 22 seconds after ingestion, the snake captured another chick in the nest and swallowed it in 32 seconds. After the predation of the two chicks, the snake came down from the tree; the entire observation lasted 32 min. The eighth observation was recorded by JDS on 16 October 2019, at 10:09, in “Sítio Fechado” (7.2992° S; 37.2978° W, 791 m a.s.l.), Brejinho municipality, PE state. An adult individual of P. nattereri (sex not determined; snout-vent length around 140 cm) was observed on the ground over some dry branches, preying upon a juvenile individual (total length around 8 cm) of the Spix’s cavy, Galea spixii (Wagler, 1831). When spotted, the snake was biting and holding the prey’s neck on its mouth, presumably poisoning it with the rear fangs (Fig. 1G); the juvenile G. spixii was still alive and emitting loud and pitched whistles. An adult individual of G. spixii (presumably the mother) was seen close to the snake, but ran away after the human approximation. The snake kept the juvenile on its mouth for 6 min, but the noise caused by the observer trying to get closer to take pictures disturbed the snake, leading it to release the prey and flee. The mammal was already dead when released by the snake, which would clearly succeed in the predation if there was no human interference. The ninth observation was recorded by JDS on 5 April 2020, at 13:55, in “Sítio Fechado” (7.2992° S; 37.2978° W, 791 m a.s.l.), Brejinho municipality, PE state. An adult individual of P. nattereri (sex and snout-vent length not determined) was observed perched on a guava tree (Psidium guajava L.), at a height of about 2 m, being mobbed by two individuals of the Tropical Wren, Troglodytes mus-

Cuad. herpetol. 34 (2): 285-293 (2020) culus Naumann, 1823. The birds mobbed the snake continuously, flying towards it and emitting alarm calls. A hole in the tree trunk, about 1 m below the location where the snake was, allowed the researcher to confirm the existence of a nest with three chicks. The P. nattereri entered another hole in the tree trunk near the site where it was first seen, then moved down inside the trunk and reached the nest; then snake ingested all three chicks in sequence (duration of ingestion: 32, 48 and 72 seconds). Fourteen minutes after ingestion of the last chick, the snake appeared in the hole entrance where the nest was positioned, but entered the trunk again. The bird parents continued to emit alarm calls during the entire observation, which lasted 72 minutes, when the researcher left the site. The tenth observation was recorded by JDS on

14 May 2020, at 09:32, in “Sítio Fechado” (7.2992° S; 37.2978° W, 791 m a.s.l.), Brejinho municipality, PE state. An adult individual of P. nattereri (sex and snout-vent length not determined) was observed perched on a “mandacaru” cactus (Cereus jamacuru DC.) next to a bird nest preying upon a chick of the Bananaquit, Coereba flaveola (Linnaeus, 1758). When spotted, the snake was moving down the cactus, biting and holding the bird’s head on its mouth (Fig. 1H). Ingestion of the prey was completed in the ground and lasted 55 seconds. We compiled a total of 93 prey items of P. nattereri combining the ones reported in this study with those of the literature; 67 records are from the Caatinga ecoregion (Table 1) and 26 records are from the Cerrado (Table 2). Lizards (N= 38) comprised the predominant prey category for P. nattereri in

Table 1. Summary of prey items of Philodryas nattereri in the Caatinga ecoregion of Brazil based on literature data and new observations.

Prey category

Source

Leptodactylus macrosternum Miranda-Ribeiro, 1926

Mesquita et al., 2011

Rhinella granulosa (Spix, 1824)

This study

Rhinella jimi (Stevaux, 2002)

Guedes et al., 2018; this study

Unidentified

Vitt and Vangilder, 1983

Ameivula ocellifera (Spix, 1825)

Vitt and Vangilder, 1983; Mesquita et al., 2011

Ameiva ameiva (Linnaeus, 1758)

Vitt and Vangilder, 1983; Mesquita et al., 2011

Tropidurus hispidus (Spix, 1825)

Vitt and Vangilder, 1983; Mesquita et al., 2011; Menezes et al., 2013

Brasiliscincus heathi (Schmidt & Inger, 1951)

Vitt and Vangilder, 1983

Phyllopezus pollicaris (Spix, 1825)

Vitt and Vangilder, 1983; Mesquita et al., 2011

Hemidactylus mabouia (Moreau de Jonnès, 1818)

Mesquita et al., 2011

Iguana iguana (Linnaeus, 1758)

This study

Salvator merianae Duméril & Bibron, 1839

Vitt and Vangilder, 1983

Vanzosaura multiscutata (Amaral, 1933)

Vitt and Vangilder, 1983

Unidentified

Mesquita et al., 2011

Leptodeira annulata (Linnaeus, 1758)

Guedes, 2017

Oxybelis aeneus (Wagler, 1824)

Mesquita et al., 2011

Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854

Coelho-Lima et al., 2019

Lygophis dilepis Cope, 1862

This study

Coereba flaveola (Linnaeus, 1758)

This study

Columbina picui (Temminck, 1813)

This study

Tangara sayaca (Linnaeus, 1766)

This study

Troglodytes musculus Naumann, 1823

This study

Unidentified

Vitt and Vangilder, 1983; Mesquita et al., 2011

Amphibians (N= 6)

Lizards (N= 38)

Snakes (N= 4)

Birds (N= 9)

289

R. F. D. Sales et al. - Diet of Philodryas nattereri Mammals (N= 9) Necromys lasiurus (Lund, 1841)

Vitt and Vangilder, 1983; Mesquita et al., 2011

Wiedomys pyrrhorhinos (Wied-Neuwied, 1821)

Mesquita et al., 2011

Galea spixii (Wagler, 1831)

This study

Myotis nigricans (Schinz, 1821)

Mesquita et al., 2011

Monodelphis domestica (Wagner, 1842)

Mesquita et al., 2011

Rattus rattus Linnaeus, 1758

Vitt and Vangilder, 1983

Unidentified

Mesquita et al., 2011

Eggs (N= 1) Unidentified (Squamata) * Unsuccessful attempted predation

the Caatinga (56.7% of reported prey items; Table 1; Fig. 2), followed by mammals (N= 9; 13.4 %), birds (N= 9; 13.4%), anuran amphibians (N= 6; 9.0 %), snakes (N= 4; 6.0%), and vertebrate eggs (N= 1; 1.5 %). In the Cerrado ecoregion, mammals (N= 13) stand out as the most reported prey category (50.0% of reported prey items; Table 2; Fig. 2), followed by lizards (N= 7; 26.9%), anuran amphibians (N= 4; 15.4%), and birds (N= 2; 7.7%). Based on these data, the diet composition of P. nattereri is significantly different between the Caatinga and Cerrado ecoregions (Kolmogorov-Smirnov two-group test, Dmax= 0.351, p < 0.001). In this study, we report ten predation events by the snake Philodryas nattereri in northeastern Brazil, bringing new data about its feeding habits. Our ob-

servations include predation on a large-sized lizard, one adult bird, two venomous toads, one snake, bird chicks, and one mammal. Our field observations, together with previous studies in the Caatinga (Vitt and Vangilder, 1983; Mesquita et al., 2011) and in the Cerrado (França et al., 2008) evidence that P. nattereri is a generalist and opportunistic snake predator in these ecoregions of Brazil. Mesquita et al. (2011) studied the autecology of P. nattereri in a Caatinga site in Ceará state, and argued that this snake may be a keystone species in the Caatinga, taking into consideration its high abundance, ability to forage in different substrates (e.g. ground, rocky outcrops, trees), wide variety of suitable prey, extended reproductive cycle and high fecundity. Thus, like other generalist and widely distributed snakes, P. nattereri

Table 2. Summary of prey items of Philodryas nattereri in the Cerrado ecoregion of Brazil based on literature data.

Prey category

Source

Leptodactylus vastus A. Lutz, 1930

Araújo et al., 2013

Physalaemus cuvieri Fitzinger, 1826

Gambale et al., 2014

Scinax x-signatus (Spix, 1824)

Godinho et al., 2012

Unidentified

França et al., 2008

Hemidactylus mabouia (Moreau de Jonnès, 1818)

Godinho et al., 2012

Tropidurus itambere Rodrigues, 1987

França et al., 2008

Tropidurus torquatus (Wied-Neuwied, 1820)

França et al., 2008

Unidentified

França et al., 2008

Volatinia jacarina (Linnaeus, 1766)

França et al., 2008

Unidentified

França et al., 2008

Amphibians (N= 4)

Lizards (N= 7)

Birds (N= 2)

Mammals (N= 13) Unidentified

290

Cuad. herpetol. 34 (2): 285-293 (2020)

Figure 2. Relative contribution of different prey categories in the diet of Philodryas nattereri in the Caatinga and Cerrado ecoregions of Brazil.

can play an important ecological role in controlling prey populations (Cabral et al., 2019), especially in altered environments where top predators have been locally extinct. In agreement with Mesquita et al. (2011), our observations confirm the semi-arboreal habits of P. nattereri, which was previously thought to be terrestrial (Vitt, 1980; Vanzolini et al. 1980). This snake is able not only to perch on trees, but is also an efficient arboreal forager, feeding on adult birds (FranĂ§a et al., 2008; Mesquita et al., 2011), bird chicks inside nests (this study), arboreal snakes (Mesquita et al., 2011) and bats, presumably in their shelters (Mesquita et al., 2011). Our data also evidence that some flying and/or arboreal prey can be captured by P. nattereri in the ground. Many birds forage in the ground (Sick, 1997), and thus can be ambushed by P. nattereri, such as the dove Columbina picui reported in this study, which was captured by P. nattereri in the ground (Fig. 1B). The predation of the arboreal lizard Iguana iguana in the ground by P. nattereri (Fig. 1A) can be defined as highly opportunistic, since this lizard spends most of the time perched on trees, but can eventually go down to the soil to bask (Sales et al., 2009). Our data also revealed different feeding tactics of P. nattereri depending on the type, size and vitality of prey. This species can use constriction (e.g. largesized lizards, Fig. 1A) and/or poisoning to subdue the preys (e.g. adult birds, Fig. 1B; rodents, Fig.1G), or simply catch and swallow defenseless prey (e.g. bird chicks, Figs. 1D and 1H). Philodryas nattereri is also able to feed on toads of the genus Rhinella (Figs.

1C and 1E), which are stocky, inflate their bodies in defense, and have parotoid macroglands behind the eyes that secrete powerful venom (Jared et al., 2009). Guedes et al. (2018) suggest that this way of ingestion of P. nattereri enables the snakesâ&#x20AC;&#x2122;s postdiastemal teeth to puncture the puffed-up bodies of toads, deflating them and facilitating ingestion. Moreover, this position may prevent the toad from grasping on the substrate, or may reduce the compression of parotoid glands against the palate of the snake, avoiding venom liberation in the oral mucosa (Guedes et al. 2018). Nevertheless, in the predation episode on R. granulosa (Fig. 1E), a smaller Rhinella species, the toad was ingested belly down and did not deflate during swallowing, which indicates that P. nattereri may vary the way of ingestion of toads depending on their sizes. Since toads are nocturnal and P. nattereri is diurnal, it is highly likely that P. nattereri actively searches for them in their shelters. This same hunting strategy is probably adopted by P. nattereri towards bats (Mesquita et al., 2011). Several authors report birds as part of the diet of snakes of the genus Philodryas (Vitt, 1980; Hartmann and Marques, 2005; Leite et al., 2009; Mesquita et al., 2011), but few literature records (e.g. Sazima and Marques, 2007; Sazima, 2015) specify how snakes catch these highly evasive preys. For instance, the Lichtensteinâ&#x20AC;&#x2122;s Green Racer, Philodryas olfersii (Lichtenstein, 1823) chooses profitable hunting spots in trees to ambush birds (Sazima, 2015). The new field observations reported in this study show that P. nattereri can both ambush adult birds and actively search for bird chicks in their nests. Bird chicks are defenseless, and can be quickly swallowed without any resistance. However, if the snake is detected by adult birds, they can promptly perform mobbing to avoid predation of chicks, as in the episode of approximation of P. nattereri to nests of the birds Tangara sayaca and Troglodytes musculus. Mobbing is a type of harassing behavior employed by birds in the presence of potential predators, in which they emit alarm calls, display visual signals (which may attract additional birds to the mobbing group), and may fly towards the potential predator, disturbing it by pecking (Sick, 1997; Sazima and Marques, 2007; Sazima, 2015). In some instances, the mobbing behavior may be successful in discouraging the predator, as in the attempted predation event upon chicks of T. sayaca reported in this study. Many genera of snakes have members that include snakes as part or all of their diet (Greene, 291

R. F. D. Sales et al. - Diet of Philodryas nattereri 1997). Observations both in natural conditions and simulated in the lab confirm that some snakes are even able to ingest other snakes that equal or exceed their own body length (Jackson et al., 2004). In the Caatinga of NE Brazil, a few snakes are known by their ophiophagous feeding habits, such as the Sertão Muçurana snake, Boiruna sertaneja Zaher, 1996, that despite being characterized as a snake specialist (Alencar et al., 2013), also feeds on lizards, mammals and birds (Sales et al., 2019). Our observation of predation of Lygophis dilepis (Fig. 1D) constitutes the fourth record of ophiophagous behavior for P. nattereri (Table 1). As suggested by Coelho-Lima et al. (2019), the consumption of snakes by P. nattereri may be more frequent than previously assumed. The dietary data of P. nattereri yielded from our field observations and literature records revealed geographic variations in diet composition (Fig. 2). Lizards comprised the most reported prey in the Caatinga, whereas mammals are the most reported prey in the Cerrado. These results agree with the geographic variation reported for the Brazilian false coral snake, Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854, in which lizards are massively consumed by Caatinga populations, accounting for ~90% of the diet (Vitt and Valgilder, 1983; Coelho et al., 2019), whereas mammals are the predominant prey in the Cerrado (França et al., 2008), and these prey categories are more equitably consumed in the Atlantic Forest (Alencar et al., 2012). Prey availability is the main discussed cause for geographic variations in diet composition of squamates (e.g. Vitt and Colli, 1994). Thus, given the generalist and opportunistic feeding habits of P. nattereri, the differences in diet composition between Caatinga and Cerrado ecoregions are likely related to prey availability. For small non-flying mammals, for example, in the Cerrado there is a greater species richness and abundance than in the Caatinga (Freitas et al., 2005). However, the low sampling effort on the feeding ecology of P. nattereri in both ecoregions makes it difficult to establish large generalizations and should be considered when interpreting the results presented here. Other evoked causes for geographic variation in diets of snakes, such as presence/absence of potential competitors (Luiselli et al., 2005) and interpopulational differences in behaviors that influence resource utilization (Arnold, 1977), may also be applicable to P. nattereri. Future studies should address these questions to improve knowledge about this abundant and widely distributed snake that plays an important 292

ecological role as a predator in both natural and disturbed environments of Brazil. Acknowledgements We are grateful to Cícero Lajes for kindly provide us the photos and videos, together with the information about the predation events. Raul Sales and Paulo Marinho thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the post-doctoral and PhD (Finance Code 001) scholarships, respectively. Eliza Freire thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the research scholarship (process 142961/2019-1). Literature cited

Alencar, L.R.V., Galdino, C.A.B. & Nascimento, L.B. 2012. Life history aspects of Oxyrhopus trigeminus (Serpentes: Dipsadidae) from two sites in southeastern Brazil. Journal of Herpetology 46: 9-13. Alencar, L.R., Gaiarsa, M.P. & Martins, M. 2013. The evolution of diet and microhabitat use in Pseudoboine snakes. South American Journal of Herpetology 8: 60-67. Araújo, S.C.M., Sousam G.D.L. & Andrade, E.B. 2013. Philodryas nattereri (Paraguay Green Racer). Diet. Herpetological Review 44: 526. Arnold, S.J. 1977. Polymorphism and geographic variation in the feeding behavior of the Garter Snake Thamnophis elegans. Science 197: 676-678. Cabral, S.O., Freitas, I.S., Morlanes, V., Katzenberger, M. & Calabuig, C. 2019. Potential seed dispersers: a new facet of the ecological role of Boa constrictor constrictor Linnaeus 1758. Biota Neotropica 19: e20180626. Coelho, R.D.F., Sales, R.F.D. & Ribeiro, L.B. 2019. Sexual dimorphism, diet, and notes on reproduction in Oxyrhopus trigeminus (Serpentes: Colubridae) in the semiarid Caatinga of northeastern Brazil. Phyllomedusa 18: 89-96. Coelho-Lima, A.D., Oliveira-Filho, J.M. & Passos, D.C. 2019. Philodryas nattereri (Paraguay Green Racer). Diet. Herpetological Review 50: 601. Fialho, R.F., Rocha, C.F.D. & Vrcibradic, D. 2000. Feeding ecology of Tropidurus torquatus: ontogenetic shift in plant consumption and seasonal trends in diet. Journal of Herpetology 34: 325-330. França, F.G.R., Mesquita, D.O., Nogueira, C.C. & Araújo, A.F.B. 2008. Phylogeny and ecology determine morphological structure in a snake assemblage in the central Brazilian Cerrado. Copeia 2008: 23-28. Freitas, R.R., Rocha, P.L.B. & Simões-Lopes, P.C. 2005. Habitat structure and small mammals abundances in one semiarid landscape in the Brazilian Caatinga. Revista Brasileira de Zoologia 22: 119-129. Gambale, P.G., Batista, V.G., Vieira, R.R., Dias, T.M., Morais, A.R. & Bastos, R.P. 2014. Physalaemus cuvieri (Barker Frog). Predation. Herpetological Review 45: 682-683. Godinho, L.B., Moura, M.R., Peixoto, M.A. & Feio, R.N. 2012. Notes on the diet of Philodryas nattereri (Squamata:

Cuad. herpetol. 34 (2): 285-293 (2020) Colubridae) in southeastern Brazil. Salamandra 48: 233-234. Greene, H.W. 1997. Snakes: The Evolution of Mystery in Nature. University of California Press. Berkeley and Los Angeles. Guedes, T.B. 2017. Philodryas nattereri (Paraguay Green Racer). Diet. Herpetological Review 48: 679-680. Guedes, T.B., Nogueira, C. & Marques, O.A.V. 2014. Diversity, natural history, and geographic distribution of snakes in the Caatinga, Northeastern Brazil. Zootaxa 3863: 1-93. Guedes, T.B., Sazima, I. & Marques, O.A.V. 2018. Does swallowing a toad require any specialisation? Feeding behaviour of the dipsadid snake Philodryas nattereri on the bufonid toad Rhinella jimi. Herpetology Notes 11: 825-828. Hartmann, P.A. & Marques, O.A.V. 2005. Diet and habitat use of two sympatric species of Philodryas (Colubridae), in South Brazil. Amphibia-Reptilia 26: 25-31. How, R.A., Schmitt L.H. & Suyanto, A. 1996. Geographical variation in the morphology of four snake species from the Lesser Sunda Islands, eastern Indonesia. Biological Journal of the Linnean Society 59: 439-456. Jackson, K., Kley, N.J. & Brainerd, E.L. 2004. How snakes eat snakes: the biomechanical challenges of ophiophagy for the California kingsnake, Lampropeltis getula californiae (Serpentes: Colubridae). Zoology 107: 191-200. Jared, C., Antoniazzi, M.M., Jordão, A.E.C., Silva, J.R.M.C., Greven H. & Rodrigues, M.T. 2009. Parotoid macroglands in toad (Rhinella jimi): their structure and functioning in passive defence. Toxicon 54: 197-207. King, R.B. 1989. Body size variation among island and mainland snake populations. Herpetologica 45: 84-88. Leite, P.T., Kaefer, I.L. & Cechin, S.Z. 2009. Diet of Philodryas olfersii (Serpentes, Colubridae) during hydroelectric dam flooding in southern Brazil. North-Western Journal of Zoology 5: 53-60. Luiselli, L., Filippi, E. & Capula, M. 2005. Geographic variation in diet composition of the grass snake (Natrix natrix) along the mainland and an island of Italy: the effects of habitat type and interference with potential competitors. The Herpetological Journal 15: 221-230. Martins, M. & Oliveira, M.E. 1998. Natural history of snakes in forests of the Manaus region, Central Amazonia, Brazil. Herpetological Natural History 6: 78-150. Menezes, L.M.N., Reis, P.M.A.G., Souza, K., Urias, I.C., Walker, F.M. & Ribeiro, L.B. 2013. Death of a snake Philodryas nattereri (Squamata: Dipsadidae) after predation on a largesized lizard Tropidurus hispidus (Squamata: Tropiduridae). Herpetology Notes 6: 55-57. Mesquita, P.C.M.D., Borges-Nojosa, D. M., Passos, D.C. & Bezerra, C.H. 2011. Ecology of Philodryas nattereri in

the Brazilian semi-arid region. Herpetological Journal 21: 193-198. Mesquita, P.C.M.D., Passos, D.C., Borges-Nojosa, D.M. & Cechin, S.Z. 2013. Ecologia e história natural das serpentes de uma área de Caatinga no nordeste brasileiro. Papéis Avulsos de Zoologia 53: 99-113. Sales, R.F.D., Lisboa, C.M.C.A. & Freire, E.M.X. 2009. Répteis Squamata de remanescentes florestais do campus da Universidade Federal do Rio Grande do Norte, Natal-RN, Brasil. Cuadernos de Herpetología 23: 77-88. Sales, R.F.D., Lima, M.L.S. & França, B.R.A. 2019. Dead but delicious: an unusual feeding event by the Sertão Muçurana snake (Boiruna sertaneja) on a bird carcass. Herpetology Notes 12: 941-943. Sazima I. 2015. Predation attempts on birds by the snake Philodryas olfersii prevented by mobbing mockingbirds. Herpetology Notes 8: 231-233. Sazima, I. & Marques, O.A.V. 2007. A reliable customer: hunting site fidelity by an actively foraging neotropical colubrid snake. Herpetological Bulletin 99: 36-38. Seigel, R.A. & Ford, N.B. 2001. Phenotypic plasticity in reproductive traits: geographical variation in plasticity in a viviparous snake. Functional Ecology 15: 36-42. Shine, R. 1987. Intraspecific variation in thermoregulation, movements and habitat use by Australian blacksnakes, Pseudechis porphyriacus (Elapidae). Journal of Herpetology 21: 165-177. Sick, H. 1997. Ornitologia Brasileira. Nova Fronteira. Rio de Janeiro, Brazil. Sweet, S.S. 1985. Geographic variation, convergent crypsis and mimicry in Gopher snakes (Pituophis melanoleucus) and Western rattlesnakes (Crotalus viridis). Journal of Herpetology 19: 55-67. Vanzolini, P.E., Ramos-Costa, A. & Vitt, L.J. 1980. Répteis das Caatingas. Academia Brasileira de Ciências. Rio de Janeiro, Brazil. Velloso, A.L., Sampaio, E.V.S.B. & Pareyn, F.G.C. 2002. Ecorregiões: Propostas para o Bioma Caatinga. Instituto de Conservação Ambiental. The Nature Conservancy do Brasil. Recife, Brazil. Vitt, L.J. 1980. Ecological observation on sympatric Philodryas (Colubridae) in northeastern Brazil. Papéis Avulsos de Zoologia 34: 87-98. Vitt, L.J. & Vangilder, L.D. 1983. Ecology of a snake community in Northeastern Brazil. Amphibia-Reptilia 4: 273-296. Vitt, L.J. & Colli, G.R. 1994. Geographical ecology of a neotropical lizard: Ameiva ameiva (Teiidae) in Brazil. Canadian Journal of Zoology 72: 1986-2008. © 2020 por los autores, licencia otorgada a la Asociación Herpetológica Argentina. Este artículo es de acceso abierto y distribuido bajo los términos y condiciones de una licencia Atribución-No Comercial 2.5 Argentina de Creative Commons. Para ver una copia de esta licencia, visite http://creativecommons.org/licenses/by-nc/2.5/ar/

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Cuad. herpetol. 34 (2): 295-298 (2020)

Nota

First record and geographic distribution of Epictia borapeliotes (Vanzolini, 1996) (Squamata: Leptotyphlopidae) in the state of Piauí, northeastern Brazil Sâmia Caroline Melo Araújo1, Francisco Emídio Gomes Rodrigues2, Rudy Camilo Nunes3, Etielle Barroso de Andrade3 Programa de Pós-graduação em Biodiversidade, Ambiente e Saúde, Universidade Estadual do Maranhão, Caxias, Maranhão, Brazil. 2 Cooperativa Educacional e Social de Pedro II (COESP), Pedro II, Piauí, Brazil. 3 Grupo de Pesquisa em Biodiversidade e Biotecnologia do Centro-Norte Piauiense, Instituto Federal de Educação, Ciência e Tecnologia do Piauí, Pedro II, Piauí, Brazil. 1

Recibida: 1 1

Abril

2020

Revisada: 2 5

Abril

2020

Aceptada: 2 2

Junio

2020

E d it or As o c i a d o : D. B a l d o doi: 10.31017/CdH.2020.(2020-017)

ABSTRACT Epictia borapeliotes belongs to the family Leptotyphlopidae, composed of the smallest snakes known in the world. Currently, there are records of this species for the states of Alagoas, Bahia, Ceará, Paraíba, Pernambuco, Rio Grande do Norte, and Sergipe. However, due to its underground habits and small size, little is known about its actual distribution. Herein, we present the first record of E. borapeliotes for the state of Piauí, northeastern Brazil, expanding its geographical distribution about 270 km northwest from Aratuba municipality, state of Ceará, and about 750 km north of the type locality, the Santo Inácio district, Gentio do Ouro municipality, state of Bahia. In addition, we present an updated map of the geographic distribution of this species in northeastern Brazil. Key Words: Snake; Caatinga biome; Brazilian semiarid; fossorial snakes.

The family Leptotyphlopidae, currently represented by 14 genera and about 143 species (Martins et al., 2019; Uetz et al., 2020), is widely distributed in Africa, Central and South America, and West Indies, some few species in North America, Arabia, and Asia, in which occupy several types of environments, such as deserts, forests, savannas, wet areas, and even in anthropized environments (Adalsteinsson et al., 2009). The group of leptopiflopids includes the smallest known snakes in the world, usually measuring less than 30 cm, in which they have a slender body, shiny and smooth scales, and undifferentiated ventral scales (Adalsteinsson et al., 2009). They are fossorial or semifossorial animals that feed on larvae or adults of small social insects; however, information about the diet of these animals is quite scarce (Sampaio et al., 2018; Vanzolini, 1970; Adalsteinsson et al., 2009). In Brazil are recognized 19 species of Leptotyphlopidae distributed in four genera (Epictia, Habrophallos, Siagonodon, Trilepida): Epictia albifrons, E. australis, E. borapeliotes, E. clinorostris, E. munoai, E. striatula, E. tenella, E. vellardi, Habrophallos collaris, Siagonodon acutirostris, S. cupinensis, S. septemstriatus, Trilepida brasiliensis, T. dimidiata,

T. fuliginosa, T. jani, T. koppesi, T. macrolepis, and T. salgueiroi (Costa and Bérnils, 2018; Hoogmoed and Lima, 2018; Martins et al., 2019). Of these, only E. borapeliotes is endemic to the Caatinga biome, also occurring in enclaves of Cerrado and forested areas of the coastal region of the northeastern Brazilian (Guedes et al., 2014; Costa and Bérnils, 2018). This species has wide ecological tolerance, occurring both in hot and dry areas of the Brazilian semiarid as well as in wet areas of the coastal zone (Vanzolini, 1996; Guedes et al., 2014). It can be found at different altitude levels, with records ranging from 0 to 938 m a.s.l (Freitas et al., 2012; Guedes et al., 2014), in addition to being well adapted to anthropic environments (Sampaio et al., 2018; present study). Epictia borapeliotes is currently distributed in seven states of the Northeast region of Brazil, however, due to its small size and fossorial habits, little is known about the real distribution of this species. Herein, we present the first record of E. borapeliotes for the state of Piauí and an updated map of the geographic distribution of the species in northeastern Brazil. A small individual of E. borapeliotes (total length= 81 mm, sex not determined; Fig. 1) was

Author for correspondence: etlandrade@hotmail.com

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S. C. M. Araújo et al. - Distribution map of Epictia borapeliotes

Figure 1. Lateral (A) and dorsal (B) view of the head of Epictia borapeliotes (CBPII 125) recorded in the Pedro II municipality, state of Piauí, northeastern Brazil.

accidentally found in the urban area of the Pedro II municipality, state of Piauí, northeastern Brazil (4°26’2.14” S; 41°27’13.68” W, 600 m a.s.l). Pedro II municipality is located in Serra dos Matões, centralnorthern region of the state of Piauí, and inserted in the Serra da Ibiapaba Environmental Protection Area (Brasil, 1996), presenting transitional vegetation between Caatinga and Cerrado (Barros et al., 2014; Santos et al., 2019). The specimen was found under cashew foliage during the cleaning of a residential yard on July 13, 2019, collected manually and sent dead, fixed in 70% ethanol, to the Biology Laboratory of the Federal Institute of Education, Science and Technology of Piaui – IFPI (Instituto Federal de Educação, Ciência e Tecnologia do Piauí), Campus Pedro II, for identification. The individual was deposited in the Biological Collection of the IFPI, Campus Pedro II (CBPII 125). Species identification was carried out by comparing the diagnostic characteristics proposed by Vanzolini (1996). The species was previously recorded for the Brazilian states of Alagoas, Bahia, Ceará, Paraíba, Pernambuco, Rio Grande do Norte, and Sergipe (e.g., Guedes et al., 2014; Table 1). The states of Paraíba, Ceará, and Bahia are those with the 296

highest number of records of the species (see Table 1). However, to date, no record of this species has been made for the state of Piauí. Thus, the present work records the first occurrence of E. borapeliotes for the state of Piauí (Fig. 2), increasing its geographical distribution about 270 km in a straight line northwest from the Aratuba municipality, state of Ceará (Roberto and Veiga, 2009; Roberto and

Figure 2. Geographic distribution map of Epictia borapeliotes, with a new record (yellow triangle) for the state of Piauí, northeastern Brazil, and data from literature (black dots). For occurrence locations, see Table 1.

Cuad. herpetol. 34 (2): 295-298 (2020) Table 1. Localities of the Northeast region of Brazil with records of Epictia borapeliotes (– = information not available in consulted references).

State Alagoas

Bahia

Municipality

Paraíba

Pernambuco

9°30'14.00''

37°49'48.00''

Vanzolini (1996); Guedes et al. (2014)

Piranhas

9°30'05.00''

37°49'44.00''

Vanzolini (1996); Guedes et al. (2014)

Mucugê

13°09'00.00''

41°24'00.00''

Freitas et al. (2012)

Gentio do Ouro

11°25'47.00''

42°30'16.00''

Vanzolini (1996); Guedes et al. (2014)

Itaetê

12°59'00.00''

40°58'05.00''

Guedes et al. (2014)

Jacobina

11°10'53.00''

40°30'45.00''

Vanzolini (1996); Guedes et al. (2014)

Miguel Calmon

11°25'41.00''

40°35'40.00''

Guedes et al. (2014)

Palmeiras

12°31'00.00''

41°33'00.00''

Magalhães et al. (2015)

Aratuba

4°24'41.00''

39°02'21.00''

Roberto and Veiga (2009); Roberto and Loebmann (2016); Guedes et al. (2014) Ribeiro et al. (2012)

Limoeiro do Norte

5°09'19.00''

38°06'07.00''

Roberto and Loebmann (2016)

Maranguape

3°53'16.00''

38°40'32.00''

Roberto and Loebmann (2016)

Mulungu

4°18'27.00''

38°59'58.00''

Roberto and Loebmann (2016)

Santana do Cariri

7°11'11.00''

39°44'16.00''

Roberto and Loebmann (2016)

Várzea Alegre

6°47'46.00''

39°17'51.00''

Roberto and Loebmann (2016)

Araruna

6°27'13.00''

35°40'49.00''

Arzabe et al. (2005)

Boqueirão

7°28'54.00''

36°08'05.00''

Guedes et al. (2014)

Cacimba de Dentro

6°41'00.00''

35°44'59.00''

Arzabe et al. (2005)

Campina Grande

7°13'44.00''

35°52'51.00''

Guedes et al. (2014)

Conde

7°15'26.42''

34°54'21.98''

Vanzolini (1996)

João Pessoa

7°09'26.92''

34°48'40.80''

Vanzolini (1996); Sampaio et al. (2018)

Junco do Seridó

6°59'39.00''

36°42'50.00''

Vanzolini (1996); Guedes et al. (2014)

São José dos Cordeiros

7°28'15.00''

36°52'51.00''

Brito (2017)

Bezerros

8°14'31.00''

35°45'25.00''

Guedes et al. (2014)

Sertânia

8°04'00.00''

37°16'00.00''

Cordeiro and Hoge (1974); Vanzolini (1996);

Angicos

5°35'45.00''

36°36'01.00''

Guedes et al. (2014)

João Câmara

5°25'38.00''

35°54'38.00''

Calixto and Morato (2017)

5°50'24.00''

35°12'07.00''

Sales et al. (2009)

Rio Grande Natal do Norte Nísia Floresta

Sergipe

Reference

Olho D’Água do Casado

Chapada do Araripe Ceará

Latitude (S) Longitude (W)

6°06'47.67''

35°10'59.25''

Vanzolini (1996)

Serra Negra do Norte

6°39'38.00''

37°23'56.00''

Guedes et al. (2014); Caldas et al. (2016)

Canindé de São Francisco

9°39'52.00''

37°47'05.00''

Guedes et al. (2014); Souza and Bocchiglieri (2018)

Poço Redondo

9°39'44.00''

37°47'05.00''

Guedes et al. (2014); Souza and Bocchiglieri (2018)

Loebmann, 2016; Guedes et al., 2014), and about 750 km in a straight line north of the type locality of the species, the Santo Inácio district, Gentio do Ouro municipality, state of Bahia (Vanzolini, 1996). This new record corresponds to the westernmost known occurrence of the species. This work presents additional information about the geographic distribution of E. borapeliotes in a poorly studied area, reinforcing the need to conduct long-term herpetological surveys in the northern region of the state of Piauí

(Santos et al., 2019). Literature cited

Adalsteinsson, A.S.; Branch, W.R.; Trape, S. & Vitt, L.J. 2009. Molecular phylogeny, classification, and biogeography of snakes of the Family Leptotyphlopidae (Reptilia, Squamata). Zootaxa 2244: 1-50. Arzabe, C.; Skuk, G.; Santana, G.G.; Delfim, F.R.; Lima, Y.C.C. & Abrantes, S.H.F. 2005. Herpetofauna da Área de Curimataú, Paraíba: 259-274. In: Araújo, F.S.; Rodal, M.N.J. & Barbosa, M.R.V. (eds.), Análise das Variações da Biodiversidade do

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S. C. M. Araújo et al. - Distribution map of Epictia borapeliotes Bioma Caatinga. Ministério do Meio Ambiente, Brasília, Brasil. Barros, J.S., Ferreira, R.V., Pedreira, A.J. & Schobbenhaus, C. 2014. Geoparque Sete Cidades-Pedro II (PI): Proposta. Brasília: Serviço Geológico Brasileiro (CPRM), relatório técnico. Secretaria da Agricultura, São Paulo – Brasil. Vol. XXIII, N.° 2 - pp. 13-16. Available in: http://www.cprm.gov. br/publique/Gestao-Territorial/Geoparques-134. Accessed in: 02 April 2020. Brasil. 1996. Decreto de 26 de novembro de 1996. Dispõe sobre a criação da Área de Proteção Ambiental Serra da Ibiapaba, nos Estados do Piauí e Ceará, e dá outras providências. Poder Executivo. Brasília-DF. Brito, J.A.M. 2017. Influência da morfologia na utilização de recursos em uma taxocenose de serpentes em área de Caatinga arbórea no Nordeste do Brasil. Trabalho de Conclusão de Curso, Universidade Federal da Paraíba. Areia, Paraíba. Caldas, F.L.S.; Costa, T.B.; Laranjeiras, D.O.; Mesquita, D.O. & Garda, A.A. 2016. Herpetofauna of protected areas in the Caatinga V: Seridó Ecological Station (Rio Grande do Norte, Brazil). Check List 12: 1929. Calixto, P.O. & Morato, S.A.A. 2017. Herpetofauna recorded by a fauna rescue program in a Caatinga area of João Câmara, Rio Grande do Norte, Brazil. Check List 13: 647-657. Cordeiro, C.L. & Hoge, A.R. 1974. Contribuição ao conhecimento das serpentes do estado de Pernambuco. Memórias do Instituto Butantan 37: 261-290. Costa, H.C & Bérnils, R.S. 2018. Répteis do Brasil e suas Unidades Federativas: Lista de espécies. Herpetologia Brasileira 7: 11-57. Freitas, M.A.; Veríssimo, D. & Uhlig, V. 2012. Squamate Reptiles of the central Chapada Diamantina, with a focus on the municipality of Mucugê, state of Bahia, Brazil. Check List 8: 16-22. Guedes, T.B.; Nogueira, C. & Marques, O.A.V. 2014. Diversity, natural history, and geographic distribution of snakes in the Caatinga, Northeastern Brazil. Zootaxa 3863: 1-93. Hoogmoed, M.S. & Lima, J. 2018. Epictia collaris (Hoogmoed, 1977) (Reptilia: Squamata: Leptotyphlopidae), new record for the herpetofauna of Amapá and Brazil, with additional localities in French Guiana and a distribution map. Boletim do Museu Paraense Emilio Goeldi, Ciencias Naturais 13: 461-465. Magalhães, F.M.; Laranjeiras, D.O.; Costa, T.B.; Juncá, F.A.; Mesquita, D.O.; Röhr, D.L.; Silva, W.P.; Vieira, G.H.C. &

Garda, A. A. 2015. Herpetofauna of protected areas in the Caatinga IV: Chapada Diamantina National Park, Bahia, Brazil. Herpetology Notes 8: 243-261. Martins, A.; Koch, C.; Pinto, R.; Folly, M.; Fouquet, A. & Passos, P. 2019. From the inside out: Discovery of a new genus of threadsnakes based on anatomical and molecular data, with discussion of the leptotyphlopid hemipenial morphology. Journal of Zoological Systematic and Evolutionary Research 57: 840-863. Ribeiro, S.C.; Roberto, I.J.; Sales, D.L.; Ávila, R.W. & Almeida, W.O. 2012. Amphibians and reptiles from the Araripe bioregion, northeastern Brazil. Salamandra 48: 133-146. Roberto, I.J. & Loebmann, D. 2016. Composition, distribution patterns, and conservation priority areas for the herpetofauna of the state of Ceará, northeastern Brazil. Salamandra 52:134-152. Roberto, I.J. & Veiga, S. 2009. Leptotyphlops borapeliotes: Geographic distribution. Herpetological Review 40: 238. Sales, R.F.D.; Lisboa, C.M.C.A & Freire, E.M.X. 2009. Répteis Squamata de remanescentes florestais do campus da Universidade Federal do Rio Grande do Norte, Natal-RN, Brasil. Cuadernos de Herpetología 23: 77-88. Sampaio, I.L.R.; Santos, C.P.; França, R.C.; Pedrosa, I.M.M.C.; Solé, M. & França, F.G.R. 2018. Ecological diversity of a snake assemblage from the Atlantic Forest at the south coast of Paraíba, northeast Brazil. ZooKeys 787: 107-125. Santos, A.J.; Costa, C.A.; Sena, F.P.; Araújo, K.C. & Andrade, E.B. 2019. New record and geographic distribution of Proceratophrys caramaschii Cruz, Nunes, and Juncá, 2012 in the state of Piauí, northeastern Brazil (Anura: Odontophrynidae). Herpetology Notes 12: 675-679. Souza, F.H. & Bocchiglieri, A. 2018. Epictia borapeliotes (Caatinga Threadsnake). Predation. Herpetological Review 49: 752-753. Uetz, P.; Freed, P. & Hošek, J. 2020. The Reptile Database. Available in: http://www.reptile-database.org. Accessed in: 28 May 2020. Vanzolini, P.E. 1970. Climbing habitats of Leptotyphlopidae (Serpentes) and walls’s theory of the evolution of the ophidian eye. Papéis Avulsos do Departamento de Zoologia 23: 13-16. Vanzolini, P.E. 1996. A new (and very old) species of Leptotyphlops from northeastern Brazil (Serpentes, Leptotyphlopidae). Papeis Avulsos de Zoologia 39: 281-291.

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Nota

Are there threatened snakes at the end of the rainbow? Notes on the distribution and morphology of Epicrates cenchria, Rainbow Boa, in the Brazilian Atlantic Forest Albedi Andrade-Junior, Matheus Soares França, Vinícius Sudré, Paulo Passos Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristóvão, Rio de Janeiro, RJ, 20940-040, Brazil.

Recibida: 1 6 S e t i e m b r e 2 0 1 9 Revisada: 2 9

Abril

2020

Aceptada: 1 7

Julio

2020

Editor Asociado: A. Pr udente doi: 10.31017/CdH.2020.(2019-030)

ABSTRACT We report on new voucher specimens of Epicrates cenchria to the meridional limits of its distribution in the Atlantic Forest. We provide data on the meristic, morphometric and hemipenial morphology features for this southernmost population. We review the recent published record of E. cenhria for the locality of Ipiguá, state of São Paulo, Brazil, and reidentify it specimen herein to as E. crassus. Finally, we comment on the niche models available to E. cenchria and other congeners, suggesting outstanding issues that require additional studies. Key Words: Boidae, Conservation, Epicrates spp. distribution, Epicrates cenchria, Southern Atlantic Forest.

The genus Epicrates Wagler, 1830 comprises five species popularly known as Rainbow Boas due to the general iridescence effect of their dorsal scales under sunlight (Fig. 1). It is endemic to the Neotropical region, occurring from Nicaragua to northwestern Argentina (Passos and Fernandes, 2009; Reynolds and Henderson, 2018; Uetz et al. 2019), and all its species feed preferably on small mammals (marsupials and rodents) and birds (Pizzatto et al., 2009). Epicrates cenchria occurs along the Amazonian rainforest with a disjunct set of populations in the Brazilian Atlantic rainforest spreading from Pernambuco to Rio de Janeiro states (Passos and Fernandes, 2009). To date, the occurrence of Epicrates cenchria in the state of Rio de Janeiro, southeastern Brazil, requires voucher specimens. Passos and Fernandes (2009) reported the species to the municipality of Rio das Flores, in the boundary between Rio de Janeiro and Minas Gerais states following Passos (2003), without a detailed explanation justifying this record. In fact, such a record referred to a specimen donated alive to Instituto Vital Brazil (located in the municipality of Niterói, state of Rio de Janeiro, Brazil), that escaped from the captivity on a weekend (Aníbal Melgarejo pers. comm. to P. Passos in July 2002). Since then, no other records of the species in

Rio de Janeiro came to light. In the course of curatorial work of the herpetological collection of Museu Nacional, Universidade Federal do Rio de Janeiro (MNRJ), we found new specimens of Epicrates cenchria from three different localities of Rio de Janeiro that corroborates the presence of this species in the state and represents the southernmost area of its occurrence in the Atlantic Forest domain. Thus, we herein provide details on the localities of occurrence, the distribution of E. cenchria in southeastern Brazil, as well as additional information on meristic, morphometric and hemipenial morphology of this population. The new records are from the municipality of Macaé, RJ-168 Highway, 22°21’20”S; 41°54’52”W (MNRJ 20349), and RJ-106 Highway, 22°18’44”S; 41°43’38”W (MNRJ 20350), both collected on February 26 2011 by Adriano Lima Silveira and team; and Cachoeiras de Macacu, Km 35 of the BR-116 Highway, 22°30’26.64”S; 42°41’16.8”W (MNRJ 27233), collected in August 2018 by Cecília Bueno and team (Appendix 1). The meristic and morphometric data of the individuals is synthesized in Table 1. The hemipenial morphology of the specimen MNRJ 27233 resembles the organs of other specimens from Amazonia and Atlantic Forest, but

Author for correspondence: albedi.junior@gmail.com

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Figure 1. General view in life of a specimen of Epicrates cenchria (MNRJ 9805; male 1250 mm SVL) from Reserva Biológica Santa Lúcia, municipality of Santa Teresa, state of Espírito Santo, Brazil. Photo by B. Pimenta.

differs from these populations (see Passos and Fernandes, 2009) by having the hemipenial body similar in size to the papillate lobes, transversal flounces (=horizontally continuous) more conspicuous on the sulcate face and more numerous on the asulcate face of the organ (Fig. 2). In Brazil, Epicrates cenchria occurs in sympatry with E. assisi in the states of Alagoas, Bahia, Minas Gerais and Pernambuco; with E. crassus in the

states of Bahia, Goiás, Mato Grosso, Minas Gerais, and Tocantins, and with E. maurus in the states of Amapá, Pará and Roraima (Passos and Fernandes, 2009). Beyond the borders of Brazil, E. cenchria also co-occurs with E. maurus in Venezuela, in the states of Táchira, Amazonas and Bolívar (Barrio-Amorós and Díaz de Pascual, 2008). All these regions represent ecotonal areas between rainforest and open formations, riparian forests associated with rivers

Table 1. Meristic and morphometric characters for the three specimens of Epicrates cenchria recorded in the state of Rio de Janeiro, Brazil. We report bilateral counts as “right side/left side”.

Specimen Sex

MNRJ 20349

MNRJ 20350

MNRJ 27233

Male

Snout-vent length (SVL)

1007 mm

1100 mm

1346 mm

Tail length

173 mm

160 mm

213 mm

37/49

38/50

36/46

Ventrals

261

257

261

Subcaudals

Supralabials

13/13

12/12

Infralabials

14/13

13/13

14/14

Dorsals (near the head/midbody)

Number of ocelli (right side of body)

300

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Figure 2. Asulcate (left) and sulcate (right) faces of the hemipenis of Epicrates cenchria (MNRJ 27233) from municipality of Cachoeiras de Macacu, state of Rio de Janeiro, Brazil. Scale bar= 10 mm.

or secondary open areas that replaced original ombrophilous forests (cf. Barrio-Amorós and Díaz de Pascual, 2008; Passos and Fernandes, 2009). Rivera et al. (2011) performed a molecular phylogeny and a detailed niche modeling analysis to the genus Epicrates, broadly corroborating the species boun-

Figure 3. Geographic distribution of Epicrates cenchria, comprising the new and southernmost records within the species’ corology. The symbols are as follows: white circles= specimens examined (cited in Passos and Fernandes, 2009, increased by Appendix 1); black circles= literature data (see Appendix 2); white pentagons= new records with voucher specimens; and white triangle= record without voucher specimen.

daries proposed by Passos and Fernandes (2009). Nonetheless, except for E. alvarezi and E. maurus, the occurrence probability maps for the genus presented some inconsistencies (Rivera et al., 2011:1-6; Figs. 2, 3, 4 [in part] and 6 [in part]). Rivera et al. (2011) did not recover areas of Atlantic Forest as suitable habitats to occurrence of E. cenchria, suggesting that these populations would be geographically isolated and ecologically divergent from other populations of the region. We argue that such models should be revisited considering the past environmental conditions, as well as the current levels of massive deforestation on this biome (Andrade-Junior. et al. in prep.). Despite putative problems with dataset labels or analyses in the course of modeling, our data confirm that E. cenchria distribution in fact occurs in Brazilian Atlantic Forest (see figure 8 of Passos and Fernandes, 2009), including broadly impacted areas in the domain (Fig. 3). More recently, Marques et al. (2019: 217) reported a specimen of Epicrates crassus misidentified as E. cenchria to the locality of Ipiguá, state of São Paulo, Brazil. Thus, the southernmost records of E. cenchria on the Brazilian coast are those from the above-mentioned records of Rio das Flores from the 301

Andrade-Junior et al. - Notes on the distribution and morphology of Epicrates cenchria

Figure 4. Atlantic Forest remnants based on SOS Mata Atlântica foundation 2016-2017, showing in detail the southernmost records for Epicrates cenchria. The symbols are as follows: white circles= specimens examined (cited in Passos and Fernandes, 2009, increased by Appendix 1); black circles= literature data (see Appendix 2); white pentagons= new records with voucher specimens; and white triangle= record without voucher specimen.

Instituto Vital Brazil (lacking voucher specimen) and Cachoeiras de Macacu (voucher MNRJ 27233; Fig. 3). The meridional limits of distribution of E. cenchria in the coastal Brazilian Atlantic Forest follows the pattern of other boid taxa such as Boa constrictor, which southernmost record lies in Ilha Grande, southern of the state of Rio de Janeiro, Brazil (Rocha et al., 2018). Therefore, considering the high levels of deforestation on the Atlantic and Amazonian rainforests (see Escobar, 2019), the conservation status of species restricted to such biomes, as E. cenchria, are deserve attention. Such a threat is especially alarming from the point of view of unique biogeographic patterns associated with threatened areas (see Funk et al., 2002), illustrated by the progressive fragmentation on the southern portions of the Atlantic Forest (Fig. 4). During execution of this study, we faced great political and economic difficulties by lack of political representativeness and research financing in Brazil. More seriously, the new Brazilian environmental legislations revealed unable to exchange of scientific information with other countries by erroneous or 302

malicious interpretations of international biodiversity conventions (Alves et al., 2018). To complicate matters, the Brazilian federal government has dismantled the control apparatus of IBAMA agency, weakening the fight against environmental crimes along the country, in parallel with permissions to exploit fully protected reserves. In the face of so many difficulties, the Atlantic Forest that had been registering a recent drop in deforestation, unfortunately returned to suffer a major impact between 2018-2019 with about 30% deforestation growth (SOS Mata Atlântica Foundation and INPE, 2020). Acknowledgements Paulo Passos is very indebted with Aníbal Melgarejo (in Memoriam) for detailed information with respect to the previous occurrence of Epicrates cenchria in the state of Rio de Janeiro, and Bruno Pimenta by the slides of E. cenchria from the Reserva Santa Lúcia. We thank the anonymous reviewers for the helpful comments on the early version of the manuscript. Albedi Andrade Jr. (88887.371704/2019-00), Viní-

Cuad. herpetol. 34 (2): 299-304 (2020) cius Sudré (88887.201311/2018-00), and Matheus S. França (133011/2020-8) thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and Conselho Nacional de Desenvolvimento Científico e Tecnológico for the scholarship. Financial support for Paulo Passos was provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (processes 306227/2015-0, 439375/2016-9, 302611/20185 and 309560/2018-7) and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (E-26/202.737/2018). Literature cited

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Andrade-Junior et al. - Notes on the distribution and morphology of Epicrates cenchria continental forms of the genus Epicrates (Serpentes, Boidae) integrating phylogenetics and environmental niche models. PLoS ONE 6: e22199. Rocha, C.F.D.; Telles, F.B.S.; Vrcibradic, D. & Nogueira-Costa, P. 2018. The herpetofauna from Ilha Grande (Angra dos Reis, Rio de Janeiro, Brazil): updating species composition, richness, distribution and endemisms. Papéis Avulsos de Zoologia 58: e20185825. Sabaj, M.H. 2019. Standard symbolic codes for institutional resource collections in herpetology and ichthyology: An Online Reference. Version 7.1 (21 March 2019). Electronically accessible at http://www.asih.org, American Society of Ichthyologists and Herpetologists, Washington, DC. Santana, G.G.; Vieira, W.L.S.; Pereira-Filho, G.A.; Delfin, F.R., Lima, Y.C.C. & Vieira, K.S. 2008. Herpetofauna em um fragmento de Floresta Atlântica no Estado da Paraíba, região Nordeste do Brasil. Biotemas 21: 75-84. Santos-Costa, M.C.; Maschio, G.F. & Prudente, A.L.C. 2015. Natural history of snakes from Floresta Nacional de Caxiuanã, eastern Amazonia, Brazil. Herpetology Notes 8: 69-98. Silva, F.M.; Menks, A.C.; Prudente, A.L.C.; Costa, J.C.L.; Travassos, A.E.M. & Galatti, U. 2011. Squamate Reptiles from municipality of Barcarena and surroundings, state of Pará, north of Brazil. Check List 7: 220-226. Solis, J.M.; Bowman, D. & Ward, D. 2015. Epicrates cenchria (Rainbow Boa): Feeding Observation. The Herpetological Bulletin 132: 25-26. SOS Mata Atlântica Foundation and Instituto Nacional de Pesquisas Espaciais. 2016-2017. http://mapas.sosma.org. br/dados/solicitacao_mapas/ accessed 5 September 2019. SOS Mata Atlântica Foundation & Instituto Nacional de Pesquisas Espaciais. 2020. Atlas dos remanescentes florestais da Mata Atlântica período 2018-2019. Turci, L.C. & Bernarde, P.S. 2008. Levantamento herpetofaunístico em uma localidade no município de Cacoal, Rondônia, Brasil. Bioikos 22: 101-108. Uetz, P.; Freed, P. & Hošek, J. (eds.). 2019. The Reptile Database, http://www.reptile-database.org. Last accessed 9 April 2019. Appendix 1 Specimens examined beyond the sample cited by Passos and

Fernandes (2009). The Institutional acronyms follow Sabaj (2019), except for Coleção de Tecidos Animais do Departamento de Ciências Biológicas (UFES-CTA), Universidade Federal do Espírito Santo, Vitória, Brazil. Asterisks correspond to the specimen records with identification confirmed through photos. Epicrates cenchria.—Brazil. Rio de Janeiro: Macaé, RJ-168 Highway (MNRJ 20349), RJ-106 Highway (MNRJ 20350); Cachoeiras de Macacu, Km 35 of the BR-116 Highway (MNRJ 27233). Minas Gerais: Ipatinga (19°29’14.1”S; 42°31’33.0”W; MZUFV 1140*). Espirito Santo: Linhares (19°34’00.0”S; 39°47’00.0”W; MNRJ 23874), BR-101 Highway (19°01’16.9”S; 40°00’54.4”W; UFES-CTA 2703*).

Appendix 2 Literature records. Countries are given in bold capitals, states in plain capitals. Epicrates cenchria.—BRAZIL. ACRE: Avila-Pires et al. (2009): Juruá. Bernarde et al. (2013): lower Moa river, Cruzeiro do Sul. Miranda et al. (2014): São José I Farm, Senador Madureira. AMAZONAS: Prudente et al. (2010): Petroleum Basin of Urucu, Coari. Leite & Dorado-Rodrigues (2017): Juruá River, Carauari. BAHIA: Martins et al. (2018): Ilhéus. MATO GROSSO: Carvalho et al. (2017): Nova Canaã. MINAS GERAIS: Palmuti et al. (2009): Reserva Particular do Patrimônio Natural Feliciano Miguel Abdala, Caratinga. PARAÍBA: Santana et al. (2008): Mata do Buraquinho, João Pessoa. PARÁ: Avila-Pires et al. (2009): Curuá-Una. Avila-Pires et al. (2018): Parque Estadual do Utinga, Belém. Fiorillo et al. (2019): Senador José Porfírio. Mendes-Pinto et al. (2011): Floresta Nacional do Trairão, Trairão. Silva et al. (2011): Barcarena. Santos-Costa et al. (2015): Floresta Nacional de Caxiuanã. Prudente et al. (2010): Estação Científica Ferreira Penna, Melgaço. RONDÔNIA: Bernarde & Abe (2006): Espigão do Oeste. Turci & Bernarde (2008): Cacoal. Avila-Pires et al. (2009): Guajará-Mirim. GUYANA: Cole et al. (2013): Dubulary Ranch, Katarbo, Konawaruk Camp. PERU: Solis et al. (2015): Pacaya Samiria National Reserve, Confluence of the Marañon and Ucayali rivers, Ucamara depression, Loreto. VENEZUELA: Barrio-Amorós & Díaz de Pascual (2008): Uribante dam, Táchira.

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Nota

Primer registro de ectoparásitos en cinco especies de lagartijas del género Liolaemus (Liolaemidae) y en Teius teyou (Teiidae) Viviana I. Juárez Heredia1, Ana G. Salva1,2, Cecilia I. Robles1 Instituto de Comportamiento Animal (ICA), Fundación Miguel Lillo, Miguel Lillo 251, T4000JFE, San Miguel de Tucumán, Tucumán, Argentina. 2 CONICET, Consejo Nacional de Investigación Científica y Técnica, Buenos Aires, Argentina. 1

Recibida: 0 8

Mayo

2020

Revisada: 2 3

Junio

2020

Aceptada: 2 1

Julio

2020

E d itor As o c i a d o : C . B or te i ro doi: 10.31017/CdH.2020.(2020-029)

ABSTRACT First record of ectoparasites in five lizard species of the genus Liolaemus (Liolaemidae) and in Teius teyou (Teiidae). Ectoparasites of the Trombiculidae family and the genus Neopterygosoma were identified in six lizard species from north-western and central-western Argentina, Liolaemus ramirezae, L. scapularis, L. cuyanus, L. olongasta, L. riojanus and Teius teyou. Description of their distribution on the host body are provided. The highest intensity of infestation was recorded in the eyelids, armpits and belly. This work constitutes a new host registry for trombiculid and Neopterygosoma mites. Key Words: Mites; Trombiculidae; Neopterygosoma; Lizards.

Los ectoparásitos más comunes en las lagartijas son diferentes grupos de ácaros como trombicúlidos y garrapatas (de Oliveira et al., 2019; Schall et al., 2000; Stekolnikov y González Acuña, 2012; Tälleklint Eisen y Eisen, 1999). Entre los factores que pueden modificar la intensidad de infestación en la población del hospedador podemos nombrar: sexo, edad, estación del año, condiciones del hábitat, vegetación, humedad y temperatura (Talleklint Eisen y Eisen 1999; Schall et al., 2000; Slowik y Lane 2001; Eisen et al., 2001, 2004; Amo et al., 2005; Martín et al., 2007). La distribución de los ectoparásitos sobre el cuerpo de su hospedador puede variar, con especies que se ubican preferiblemente debajo de las escamas, con una distribución homogénea o concentrados en regiones específicas del cuerpo (axilas, ingle, cuello o cola; Jack, 1962; Bertrand et al., 2000). Los registros sobre la infestación por ectoparásitos en lagartijas de Argentina son escasos (e.g Dittmar de la Cruz et al., 2004; Juárez Heredia et al., 2014; Castillo et al., 2017) por lo que este estudio tiene como objetivo reportar el primer registro de infestación de ectoparásitos y su distribución corporal, en seis especies de hospedadores: Liolaemus ramirazae Lobo y Espinoza, 1999, L. scapularis Laurent, 1982, L. cuyanus Cei y Scolaro, 1980, L. olongasta Etheridge, 1993, L. riojanus Cei, 1979, y

Teius teyou Daudin, 1802. Las lagartijas fueron capturadas con la técnica de lazo corredizo y mantenidas en bolsas de tela y se identificaron siguiendo a Abdala y Quinteros (2014). Se utilizaron características diagnosticas externas para la identificación de los ácaros que infectan a las seis especies de lagartijas. El conteo de los ectoparásitos se realizaron utilizando un microscopio (Wild Heerbrugg, precisión 10x), y se tomaron fotografías del cuerpo del hospedador con cámara digital (Samsung PL 120) para registrar las zonas con mayor concentración de ectoparásitos. Para la recolección de ácaros, con un hisopo previamente humedecido con alcohol 70%, se rozó suavemente las zonas donde el ectoparásito estaba inserto, lo cual facilitó la extracción con una aguja metálica fina sin dañar tanto al hospedador como a los ejemplares de ácaros. Los ectoparásitos extraídos fueron colocados en tubos tipo Eppendorf con alcohol al 70 %. Posteriormente, fueron montados con alcohol polivinílico (PVC) y solución de Hoyer (Krantz, 1970), para su identificación. La identificación del ácaro Neopterygosoma se basó en la presencia de hipostoma con ápice redondeado liso; cuerpo 1,2 veces más ancho que largo; dorso del cuerpo con numerosas setas plumosas; numerosas setas localizada anterior o lateralmente en la genitalia de hembras, entre otras características

Autor para correspondencia: vijuarez@lillo.org.ar

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V. I. Juárez Heredia et al. - Ectoparásitos en lagartijas diagnósticas, según Fajfer (2019). En Trombiculidae se tuvo en cuenta la presencia de quelíceros con artejo distal; escudo burdamente rectangular, más ancho que largo, con borde posterior convexo con 5 sedas y sensilas flageliformes, con ramas; ojos 2/2 en una placa con la formación tricúspide, entre otros características diagnósticas, según Hoffmann (1990). Posterior a la toma de todos los datos, cada lagartija fue liberada en su sitio exacto de captura. Se informan los parámetros ecoparasitológicos definidos por Bush et al., (1997), Prevalencia (P): porcentaje de la población parasitada; Intensidad Media (IM): número promedio de ectoparásitos por hospedador infestado, salvo para T. teyou ya que se capturó un solo ejemplar. Durante los meses de enero, febrero y noviembre de 2015 y diciembre de 2017 se realizaron cuatro viajes de campo a Los Cardones, Amaicha del Valle, Provincia de Tucumán, Argentina (26°40’1.5” S, 65°49’5.1” W, datum: WGS84, 2700 m s.n.m), donde se capturaron 15 lagartijas (9 hembras y 6 machos) de L. ramirazae. El ambiente se caracteriza por un sustrato arenoso, con rocas grandes, arbustos y cactus dispersos. Las lluvias alcanzan un valor medio anual de 160 mm, siendo el mes de enero el que registra mayores precipitaciones (http://www.mineria.gov. ar). Durante noviembre de 2018 y enero de 2019 se capturaron 26 lagartijas (10 hembras y 16 machos) de L. scapularis en los Médanos de Cafayate, Provincia de Salta (26° 3’51.62” S; 65°54’35.31” O; datum: WGS84, 1700 m s.n.m). El ambiente es desértico, formando complejos de arena que superan los 25 m de altura con escasa vegetación, constituida por especies de Monte. El clima es muy seco, con precipitaciones

de 200 a 250 mm, durante los meses de Octubre a Marzo (Hueck, 1950). En diciembre del año 2017 en Ticucho, Departamento de Trancas, Provincia de Tucumán (26°32’57,57” S; 65°15’19,93” O; 1701 m s.n.m), se colectó un ejemplar macho de T. teyou. El sitio cuenta con una vegetación perteneciente a Chaco Serrano, en particular al bosque xerófilo serrano y precipitaciones marcadamente estivales durante los meses de octubre a marzo (500 mm a más 800 mm anuales, Santillán de Andrés y Ricci, 1966). Durante febrero de 2020, se colectaron 18 ejemplares (6 machos y 12 hembras) de L. cuyanus, 18 de L. olongasta (11 machos y 7 hembras) y 32 de L. riojanus (20 machos y 12 hembras). Las tres especies de lagartijas fueron capturadas en el Parque Nacional Talampaya (29°46’3,45” S; 68° 0’6,67” O; datum: WGS84; 1300 m s.n.m) a 400 km de la capital de La Rioja. La zona se encuentra dentro de la provincia fitogeográfica del Monte (Burkart et al., 1999), donde predominan el matorral -o estepa arbustiva xerófilay bosques marginales de algarrobo y precipitación media anual menor a 200 mm (Chebez, 2005). Tres de los 15 ejemplares de L. ramirazae (2 hembras y 1 macho) estaban infestados por ácaros adultos del género Neopterygosoma (Fig. 1a). Los ácaros se concentraron en la región ventral, en los laterales del vientre y debajo de las escamas del hospedador (Fig. 2). Larvas de ácaros de la familia Trombiculidae fueron hallados parasitando al macho de T. teyou, a L. scapularis (3 hembras y 4 machos), L. cuyanus (5 hembras y 2 machos), L. riojanus (1 hembra) y a L. olongasta (3 hembras y 7 machos) (Figs. 1b, 3, 4, 5). La prevalencia e intensidad media para cada población muestreada son registradas en

Figura 1. (A) Ácaro adulto del género Neopterygosoma; (B) Larva de Trombiculidae

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Figura 2. Ácaros del género Neopterygosoma (flechas rojas) fijos debajo de las escamas de la región gular del saurio Liolaemus ramirezae.

la Tabla 1. En cuanto a la distribución de los ácaros en T. teyou, estos se concentraron en el pliegue posterior de las patas traseras (n= 128), sobre pequeños pliegues de piel blanda y escamas granulares (Fig. 3). En L. scapularis, L. cuyanus, L. olongasta y L. riojanus los ácaros se encontraron en los párpados superiores e inferiores, con iguales características que los pliegues de T. teyou (Figs. 4, 5). Los Trombiculidae representan una de las familias de ectoparásitos más extensamente distribuidas en la región Neotropical, ocupando gran variedad de ambientes y condiciones climáticas como por ejemplo vegetación costera (Cunha Ba-

Figura 3. Región posterior de pata trasera del saurio Teius teyou con ácaros Trombiculidae (color naranja).

rros et al., 2003), savanas (Carvalho et al., 2006), y ecotonos entre bosques secos estacionales y campos rupestres (Clopton y Gold, 1993; Rocha et al., 2008). Ciertas especies de trombicúlidos son sensibles a las variaciones ambientales y los efectos de degradación ambiental, prefieren áreas de humedad relativa alta, temperatura baja a moderada y poca incidencia de luz solar (Clopton y Gold 1993), las cuales son características microclimáticas similares al ambiente aquí ocupado por el ejemplar de T. teyou estudiado, pero no así el de las otras especies. Teniendo en cuenta que este resultado es producto del análisis de solo un ejemplar, consideramos importante continuar estudiando esta especie de hospedador, las características de su infestación y su relación con el ambiente. Los trombicúlidos también tienen cierta preferencia de infestación en zonas del cuerpo con adaptaciones como pliegues de la piel o “bolsillos”, donde los ácaros tienden a agregarse (Rodrigues, 1987; Bauer et al., 1993), reduciendo los daños mecánicos y manteniendo las condiciones de humedad (Arnold, 1986; Cunha Barros et al., 2003; García de la Peña et al., 2004). Los trombicúlidos se alimentan de tejido dérmico (Georgi, 1988) y la presencia de escamas imbricadas es un factor que hace probable una mayor intensidad de infestación por la protección que ofrecen al ectoparásito (e.g. T. torquatus Cunha Barros y Rocha, 2000). Sin embargo, en las cinco especies donde se encontró la presencia de 307

V. I. Juárez Heredia et al. - Ectoparásitos en lagartijas

Figura 4. Larvas de Trombiculidae (flecha amarilla) ubicadas en el párpado superior del saurio Liolaemus scapularis.

trombicúlidos no registraron pliegues o “bolsillos” de la piel y los ácaros se ubicaron en regiones de piel blanda y escamas granulares, lo que permitió reconocerlos fácilmente por estar expuestos y por su color naranja. Hallazgos similares se han realizado también en Cnemidophorus cf. littoralis, Tropidurus torquatus y Ameiva ameiva (Cunha Barros y Rocha, 2000). Consideramos que estas zonas de inserción con escamas granulares representan una mayor exposición a la eliminación por el hospedador y a factores ambientales, causando que los ácaros estén más fijos y sea más dificultosa su extracción, comparada con los ácaros de L. ramirezae que se ubican debajo de las escamas y fueron de fácil eliminación. En muchas lagartijas que viven en ambientes áridos se ha observado un comportamiento de enterramiento o zambullida en la arena (Minton, 1966; Steyn, 1963; Arnold, 1995; Halloy, 1995, Halloy et al., 1998). Entre las ventajas ecológicas de este comportamiento se atribuye un menor riesgo de depredación y mayor termorregulación

(Arnold, 1995). La carga de ectoparásitos también está relacionada al comportamiento de zambullida, atribuyéndose la menor prevalencia e intensidad de infestación a los efectos de la fricción entre las regiones del cuerpo y la arena (McCoy et al., 2012; Toyama et al., 2019). Halloy et al., (1998), describe este comportamiento para L. scapularis, L. riojanus, L. cuyanus y L. olongasta, pero en nuestro trabajo sus prevalencias e intensidad de infestación son mayores que la de L. ramirazae y otras especies que no tienen esta conducta como L. teniuis, L. pacha y L. pictus (Carothers y Jaksic, 2001; Juárez Heredia et al., 2014; Espinoza Carniglia et al., 2016). Por lo tanto, la infestación en estas cuatro especies que se zambullen podría estar relacionada a las condiciones ambientales de los sitios de estudio (altas temperaturas y bajas precipitaciones), a la especie de ectoparásito y sus adaptaciones morfológicas y a las características de la piel de las regiones de inserción de los ácaros. En L. ramirazae la mayor intensidad de ácaros fue en la región gular, los flancos del vientre y la cola. Esta distribución es más homogénea en las regiones corporales del hospedador como por ejemplo T. hispidus infestado con Geckobiella sp. (Delfino et al., 2011; Bauer et al., 1993; Bertrand y Modry, 2004) lo cual estaría relacionado con las características morfológicas adaptativas y el ciclo de vida del ácaro Neopterygosoma sp., comparado con los trombicúlidos de L. scapularis, L. cuyanus, L. riojanus, L. olongasta y T. teyou. Los ácaros Neopterygosoma, son llamados “ácaros de las escamas”, por ubicarse bajo las escamas de su hospedador, en especial en la región ventral (Fajfer, 2012, 2019; Bertrand et al., 2013). Al igual que en L. pacha, especie sintópica de L. ramirezae (Juárez Heredia et al., 2014; Juárez Heredia et al., 2020), los ácaros de L. ramirazae se encontraron solo en la región ventral

Figura 5. Ácaros Trombiculidae (flechas amarillas) en párpados superior e inferior de saurios del género Liolaemus.

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Cuad. herpetol. 34 (2): 305-311 (2020) Tabla 1. Descriptores cuantitativos eco-parasitológicos de las seis especies de saurios estudiadas. N (total de hospedadores); n (total de infestados); P: prevalencia; IM: intensidad media de infestación.

Especie

P (%)

Liolemus ramirazae

8,6

Liolemus cuyanus

38,8

9,4

Liolemus olongasta

55,5

13,3

Liolemus riojanus

3,1

Liolemus scapularis

1,8

Teius teyou

y debajo de las escamas imbricadas del hospedador. La distribución de los ácaros y la baja prevalencia de infestación en la población de L. ramirezae estaría relacionada al tipo de escamas ventrales, las cuales son más largas, delgadas y finas (Lobo y Espinoza, 1999), comparadas con las de L. pacha cuyos ácaros son supraepidérmicos y fueron encontrados alojados en cámaras formadas por dos escamas superpuestas (Juárez Heredia et al., 2020). Esta característica de escamación dificultaría la inserción por parte del ectoparásito debajo de las escamas de su hospedador. La distribución ventral de los ácaros favorecería a la menor eliminación de los mismos por comportamientos de rascado o fricción de alguna parte de su cuerpo, la menor incidencia directa del sol y el contacto cercano con el suelo permitiría mantener las condiciones de humedad y protección para su mantenimiento (Clopton y Gold, 1993). En algunos casos un hospedador puede estar infestado por más de una especie de ectoparásito en diferentes regiones de su cuerpo (García de la Peña et al., 2010; Delfino et al., 2011; Espinoza Carniglia et al., 2015). En este trabajo, en cada una de las seis especies de lagartijas estudiadas solo se encontró un tipo de ectoparásito en el cuerpo del hospedador. El registro de presencia de ácaros del género Nepterygosoma en L. ramirazae es el tercer hallazgo de ectoparasitismo para las especies del género Liolaemus de Argentina (Dittmar de la Cruz et al., 2004; Juárez Heredia et al., 2014). En el caso de T. teyou, L. scapularis, L. riojanus, L. cuyanus y L. olongasta constituyen un nuevo registro de hospedadores para los ácaros Trombiculidae. En base a los resultados obtenidos en este trabajo, consideramos importante continuar con los estudios de la identificación y relación de los ectoparásitos que infestan a las lagartijas de Argentina, ya que son escasos y potencialmente útiles como indi-

cadores de la salud de la población de hospedadores. Agradecimientos Agradecemos a la Fundación Miguel Lillo y a la beca de Finalización de Doctorado 2015 de CONICET, quienes financiaron los viajes de campo bajo el proyecto del Instituto de Comportamiento Animal. Gracias al Dr. Ricardo Paredes León por la identificación de los ácaros. Agradecemos a Pablo Corrales, Viviana García Alvarez, Gimena Toledo por sus respectivas colaboraciones en los muestreos de campo. Gracias a la Dirección de Flora, Fauna silvestre y suelo de Tucumán (Res. N° 169-13), Administración de Parques Nacionales (Autorización de Investigación DRC 366) y a la Secretaría de Ambiente y Desarrollo Sustentable de la Provincia de Salta (Res. N°552-18) por otorgarnos los permisos de investigación. Literatura citada

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M.C.; Victoriano Sepúlveda, P. & Moreno Salas, L. 2016. Abundancia y distribución de ácaros parásitos (Eutrombicula araucanensis y Pterygosoma sp.) en lagartijas (Liolaemus pictus) de Chile central. Revista Mexicana de Biodiversidad 87: 101-108. Etheridge, R. 1993. Lizards of the Liolaemus darwinii complex (Squamata: Iguania: Tropiduridae) in northern Argentina. Bollettino del Museo Regionale di Scienze Naturali (Torino) 11: 137-199. Fajfer, M. 2012. Acari (Chelicerata) parasites of reptiles. Acarina 20: 108-129. Fajfer, M. 2019. Systematics of reptile-associated scale mites of the genus Pterygosoma (Acariformes: Pterygosomatidae) derived from external morphology. Zootaxa 4603: 401-440. García de la Peña, C.; Contreras Balderas, A.; Castañeda, G. & Lazcano, D. 2004. Infestación y distribución corporal de la nigua Eutrombiculida alfredduguesi (Acari: Trombiculidae) en el lacertilio de las rocas Sceloporus couchi (Sauria: Phrynosomatidae). Acta Zoológica Mexicana 20: 159-165. García de la Peña, C.; Gadsden, H. & Salas Westphal, A. 2010. Carga ectoparasitaria en la lagartija espinosa de Yarrow (Sceloporus jarrovii) en el cañón de las Piedras Encimadas, Durango, México. Interciencia 35: 772-776. Georgi, J.R. 1988. Parasitologia veterinária. 4 ed, Manole, São Paulo. Jack, K.M. 1962. Observations on the genus Pterygosoma (Acari: Pterygosomatidae). Parasitology 52: 261-295. Halloy, M. 1995. Sand burying behavior in Neotropical species of lizards, Liolaemus, Tropiduridae: a phylogeny of the boulengeri group. PhD Dissertation, University of Tennessee, Knoxville. Halloy, M.; Etheridge, R. & Burghardt, G.M. 1998. To bury in sand: phylogenetic relationships among lizard species of the boulengeri group, Liolaemus (Reptilia: Squamata: Tropiduridae), based on behavioral characters. Herpetological Monographs 12: 1-37. Hoffmann, A. 1990. Los trombicúlidos de México (Acarida: Trombiculidae): Parte taxonómica (No. 2). UNAM, México. Hueck, K. 1950. Estudio ecológico y fitosociológico de los médanos de Cafayate (Salta). Lilloa 23: 63-115. Juárez Heredia, V.I.; Vicente, N.; Robles, C. & Halloy, M. 2014. Mites in the neotropical lizard Liolaemus pacha (Iguania: Liolaemidae): Relation to body size, sex and season. South American Journal of Herpetology 9: 14-19. Juárez Heredia, V.I.; Miotti, M.D.; Hernández, M.B.; Robles, C.I. & Halloy, M. 2020. Distribución corporal e inserción de ácaros (Pterygosomatidae: Neopterygosoma) en la lagartija Liolaemus pacha (Iguania: Liolaemidae). Acta Zoológica Lilloana 64: 1-12. Krantz G.W. 1970. A manual of Acarology. Oregon State University Bookstores, Corvallis. Laurent, R.F. 1982. Las especies y “variedades” de Liolaemus descritas por J. Koslowsky (Sauria Iguanidae). Neotropica 28: 87-96. Lobo, F. & Espinoza, R.E. 1999. Two new cryptic species of Liolaemus (Iguania: Tropiduridae) from northwestern Argentina: resolution of the purported reproductive bimodality of Liolaemus alticolor. Copeia 1999: 122-140. Martín, J.; López, P.; Gabirot, M. & Pilz, K.M. 2007. Effects of testosterone supplementation on chemical signals of male Iberian wall lizards: consequences for female mate choice. Behavioral Ecology and Sociobiology 61: 1275-1282.

Cuad. herpetol. 34 (2): 305-311 (2020) McCoy, E.D.; Styga, J.M.; Rizkalla, C.E. & Mushinsky, H.R. 2012. Time since fire affects ectoparasite prevalence on lizards in the Florida scrub ecosystem. Fire Ecology 8: 32-40. Minton, S.A. 1966. A contribution to the herpetology of West Pakistan. Bulletin of the American Museum of Natural History 134: 29-181. Rocha, C.F.D.; Cunha Barros, M.; Menezes, V.A.; Fontes, A.F.; Vrcibradic, D. & Van Sluys, M. 2008. Patterns of infestation by the trombiculid mite Eutrombicula alfreddugesi in four sympatric lizard species (genus Tropidurus) in northeastern Brazil. Parasite 15: 131-136. Rodrigues, M.T. 1987. Sistemática, ecologia e zoogeografía dos Tropidurus do grupo torquatus ao sul do rio Amazonas (Sauria: Iguanidae). Arquivos de Zoologia 31: 105-230. Santillán de Andrés, S. & Ricci, T. 1966. La Región de la Cuenca de Tapia, Trancas. Serie monográfica 15. Departamento de Geografía. Facultad de Filosofía y Letras, Universidad Nacional de Tucumán. Schall, J.J.; Prendeville, H.R. & Hanley, K. 2000. Prevalence of the tick, Ixodes pacificus, on western fence lizards, Sceloporus

occidentalis: trends by site, gender, size, season, and mite infestation. Journal of Herpetology 34: 160-163. Slowik, T.J. & Lane, R.S. 2001. Nymphs of the western blacklegged tick (Ixodes pacificus) collected from tree trunks in woodland grass habitat. Journal of Vector Ecology 26: 165-171. Stekolnikov, A.A. & González-Acuña, D. 2012. A revision of the chigger mite genus Paratrombicula Goff & Whitaker, 1984 (Acari: Trombiculidae), with the description of two new species. Systematic Parasitology 83: 105-115. Steyn, W. 1963. Angolosaurus skoogi (Andersson) a new record from South West Africa. Cimbebasia 6: 8-11. Talleklint Eisen, L. & Eisen, R. 1999. Abundance of ticks (Acari: Ixodidae) infesting the Western fence lizard, Sceloporus occidentalis, in relation to environmental factors. Experimental and Applied Acarology 23: 731-740. Toyama, K.S.; Florián, J.C.; Ruiz, E.J.; Gonzáles, W.L. & Gianoli, E. 2019. Sand-swimming behaviour reduces ectoparasitism in an iguanian lizard. The Science of Nature 106: 53.

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Nota

Antes verde, ahora azul: primer caso de axantismo en Smilisca baudinii (Duméril y Bibron, 1841) (Amphibia: Anura) Víctor Vásquez-Cruz1, Axel Fuentes-Moreno2 PIMVS Herpetario Palancoatl, Avenida 19 número 5525, Colonia Nueva Esperanza, C.P. 94540, Córdoba, Veracruz, México. 2 Colegio de Postgraduados, Campus Montecillo. Carretera México-Texcoco km 36.5, Montecillo, C.P. 56230, Texcoco, Estado de México, México. 1

Recibida: 1 2

Febrero

2020

Revisada: 1 5

Junio

2020

Aceptada: 0 9

Julio

2020

E d itor As o c i a d o : C . B or te i ro doi: 10.31017/CdH.2020.(2020-007)

ABSTRACT First green now blue: first case of axanthism in Smilisca baudinii (Duméril and Bibron, 1841) (Amphibia: Anura). Cases of pigmentary abnormalities have been documented in several amphibians and reptiles. These abnormalities have been classified as leucism, albinism, melanism and axanthism, among others. We report here the first case of axanthism in the frog Smilisca baudinii, as well as in the entire corresponding genus. To our knowledge, it is also the first report of axanthism in wild amphibians from Mexico. Key Words: Amphibians; Chromatophores; Pigmentary abnormalities.

Casos de anormalidades pigmentarias totales o parciales han sido reportados para anfibios y reptiles (e.g., Rivera et al., 2001; Jablonski et al., 2014), estas anormalidades pigmentarias ocurren cuando existe una ausencia o predominio de algún tipo de células pigmentarias llamadas cromatóforos o variaciones en la producción de pigmentos por las mismas (Duellman y Trueb, 1994). Los cromatóforos son clasificados de acuerdo con el color del pigmento producido: negro-marrón (melanóforos), amarillo (xantóforos), azul (cianóforos), rojo (eritróforos) y blanco (leucóforos) (Fernández Guiberteau et al., 2012). En anfibios, los casos de anormalidades pigmentarias más frecuentemente descritas son el albinismo y leucismo, que presentan producción deficitaria de melanina (Lunghi et al., 2017). Los casos de melanismo, con exceso de dicho pigmento, son poco frecuentes (e.g. Vásquez-Cruz et al., 2020), mientras que el axantismo lo es aún mucho menos (Jablonski et al., 2014). El axantismo es la condición en la que un individuo carece de pigmentación amarilla, por lo que muestra un fenotipo diferente del resto de la población, con coloraciones azules, grises u anormalmente oscuras (Chilote y Moreno, 2019). En individuos de coloración oscura, el axantismo suele confundirse con el melanismo, aunque en el primero suele discernirse aún el patrón de diseño

corporal (Jablonski et al., 2014). Por otro lado, en especies con coloración típica verde, resultante de la combinación de pigmentos amarillos y azules, el individuo axántico presentará un patrón de color azul (Martínez-Silvestre et al., 2016). Actualmente, no hay información científica publicada sobre axantismo en anfibios silvestres de México. Smilisca baudinii (Duméril y Bibron, 1841) es un hílido con amplia distribución en la vertiente atlántica desde el sur de Texas y la vertiente del pacífico desde el sur de Sonora, a lo largo de ambas costas, hasta Costa Rica (Canseco-Márquez y GutiérrezMayén, 2010). La coloración general es variable: verde claro con marcas verde oliva o marrón oscuro, flancos amarillos o crema con motas marrón oscuro o negro (ver Duellman, 2001). Aquí presentamos el primer caso de axantismo en S. baudinii y una actualización de su ocurrencia en anfibios. El 10 de septiembre del 2018, alrededor de las 10:00 h un individuo adulto de Smilisca baudinii con coloración dorsal azul fue encontrado en un arbusto en una zona agrícola de la Reserva Ecológica Natural Cuenca Alta del río Atoyac (18°55’09” N; 96°52’33” O; WGS84; 560 m s.n.m), en el municipio de Amatlán de los Reyes, estado de Veracruz, México. El individuo presentó un fenotipo compatible con axantismo (Fig. 1a), ya que presentó un patrón azul (resultado de la ausencia de xantóforos) en el dorso

Autor para correspondencia: victorbiolvc@gmail.com

313

Vásquez-Cruz & Fuentes-Moreno - Axantismo en Smilisca baudinii factores genéticos, pero también factores ambientales, contaminación y calidad de la dieta como posibles orígenes de esta anormalidad pigmentaria (Jablonski et al., 2014). De acuerdo a nuestra revisión de literatura (Tabla 1), la mayoría de los registros de axantismo han sido reportados en Estados Unidos (35%), España (13.3%) y Japón (11.6%). La familia Ranidae cuenta con el mayor número de casos publicados, reportándose en 12 especies, seguido de Hylidae con siete, y Bufonidae y Salamandridae con cinco especies cada una, concentrándose la mayoría de los registros en América del Norte, Europa y Asia Oriental. En los últimos años se han reportado varios registros de axantismo en Polonia (Bufo bufo; Kolenda et al., 2017), Rusia (Dryophytes japonicus; Maslova et al., 2018), Argentina (Melanophrynicus estebani; Chilote y Moreno, 2019), y Brasil (Dendropsophus minutus; Castro et al., 2020) (Tabla 1). Particularmente en especies mexicanas de anfibios, esta anormalidad pigmentaria sólo se ha reportado en la salamandra Ambystoma mexicanum (Shaw y Nodder, 1798), en condiciones de cautiverio (Frost et al., 1984). El presente reporte es el primer caso de axantismo en Smilisca baudinii, así como en todo el género y, para nuestro conocimiento, es también el primer caso en un anfibio silvestre en México. Aunque en este caso no se confirmó el origen genético de la alteración, consideramos poco probable una inducción por contaminación ambiental en el área de estudio dado el predominio en la misma de técnicas de cultivo no contaminantes y de tipo tradicional.

Figura 1. A) Individuo macho adulto axántico de Smilisca baudinii de Playa la Junta, Amatlán de los Reyes, Veracruz. B) individuo macho adulto de S. baudinii con coloración típica.

del tronco y extremidades, vientre de color beige, y ojos con iris grisáceo; en contraposición a la característica coloración de fondo verde (clara u obscura) con patrón de manchas, vientre amarillo y ojos con iris amarillo-dorado (Fig. 1b). El referido individuo se encontraba en apariencia saludable, y luego de examinado fue liberado en el sitio de observación. Las causas inmediatas del axantismo son variadas, se consideran en la literatura principalmente 314

Agradecimientos A Enrique Espinosa Jiménez por proporcionarnos la fotografía utilizada del individuo axántico de S. baudinii y tanto a él como a José Enedino González Nava por facilitarnos los detalles de la observación. A dos revisores anónimos por sus valiosas recomendaciones. Literatura citada

Black, J.H. 1967. A blue leopard frog from Montana. Herpetologica 23: 314-315. Bechtel, H.B. 1995. Reptile and amphibian variants: colors, patterns, and scales. Krieger Publishing Company, Malabar, Florida. Berns, M.W. & Narayan, K.S. 1970. An histochemical and ultrastructural analysis of the dermal chromatophores of the variant blue frog. Journal of Morphology 132: 169-180. Berns, M.W. & Uhler, L.D. 1966. Blue frogs of the genus Rana.

Salamandra salamandra

Bufo bufo

Bufotes viridis

Melanophryniscus estebani

Dicroglossidae

Craugastor phasma

Bufo bufo

Craugastoridae

Anaxyrus fowleri

Bufonidae

Alytes obstetricans

Lissotriton helveticus

Alytidae

Ichthyosaura alpestris

Salamandridae

Ambystoma mexicanum

Ambystomatidae

Especie

Las Tablas, Costa Rica

San Luis, Argentina

Pezinok, Eslovaquia

Sulistrowiczki, Polonia

París, Francia

California, Estados Unidos

Arteixo, España

Sobrado, España

Alemania

Girona, España

Fontainebleau, Francia

Malá Morávka, República Checa

Laboratorio

Localidad

oscuro

Patrón dorsal

no visible, de quince a veinte puntos negros

blanco-grisáceo

color negro con abundantes manchas azules

oscuro

oscuro, parcialmente visible visible

gris oscuro, casi negro, excepto por cinco franjas longitudinales más claras.

cinco franjas longitudinales más claras, ubicadas simétricamente a ambos lados del cuerpo.

negro

negro, marrón

pigmentación anormal marrón rosa grisáceo

negro

Color de ojos

oscuro, claro ventralmente

manchas blancas

normal

azul grisáceo ventralmente

gris

Color de fondo

azul

pecho sin manchas, verrugas en cada uno de los puntos oscuros más grandes

visible

manchas espaciadas en el vientre

Tabla 1. Lista de casos reportados de axantismo en anfibios.

adulto

juvenil

2 renacuajos, 1 adulto adulto

Sexo

juvenil

adulto

juvenil

adulto

larva, adulto

Estadio

orilla de río

área natural

área urbana

estanque en bosque

Hábitat

Lips y Savage, 1996

Chilote y Moreno, 2019

Jablonski et al., 2014

Kolenda et al., 2017

Dubois, 1969

Bechtel, 1995

Galán et al., 1990

Fernández-Guiberteau et al., 2012

Rivera et al., 2002

Dubois et al., 1973

Dandová y Zavadil, 1993

Frost et al., 1984

Referencia

Cuad. herpetol. 34 (2): 313-320 (2020)

315

316

Dryophytes cinereus

Dryophytes japonicus

Hyla arborea

Hyla meridionalis

Smilisca baudinii

Lithobates catesbeianus

Ranidae

Pelobates fuscus

Dendropsophus minutus

Pelobatidae

Acris crepitans

Hylidae

Euphlyctis cyanophlyctis

Nova Scotia, Canadá

Kentucky, Estados Unidos patrón de manchado

pequeños parches amarillentos

Yanga, Veracruz, México

Lutherstadt Wittenberg, Sajonia-Anhalt, Alemania

visible

gris

gris claro, con coloración gris más oscura en la cabeza, parches amarillos en flancos

negro

marrón grisáceo oscuro; verde olivo grisáceo oscuro

azul

azul claro, azul oscuro, azul verdoso

gris-azulado

azul

oscuro

azul

grisáceos

negro

marrón grisáceo oscuro; verde olivo grisáceo obscuro

azul

negro

color típico

negro

azul

gris oscuro, cabeza y región escapular verdes

patrón moteado de gris tostado, verde y azul

grisáceo

parcialmente visible

Huelva, España

Cataluña, España

Apleton, Austria

Laboratorio

Asan, Corea del Sur

Vladivostok, Rusia

Yachiyo-cho, Japón

Hesaka, Japón

Tottori, Japón

Konosu, Japón

Brazos County, Texas, Estados Unidos

Guaramiranga, Brazil

Lago Harrison, Charles City, Estados Unidos

Yangdi Khola, Suikhet, Nepal

adulto

larvas

área natural

2H, M

área agrícola

Gilhen y Russell, 2015

Berns y Uhler, 1966

Sacher, 1985

Este estudio

Gónzalez et al., 2001

Rivera et al., 2001

Hinz, 1976

Miura, 2018

Maslova et al., 2019

área perturbada -

Maslova et al., 2018

Nishioka y Ueda, 1985d

Nishioka y Ueda, 1985a

Cain y Utesch, 1976

Castro et al., 2020

Niccoli, 2013

Dubois, 1976

lago artificial

lago

área urbana

adulto

2 H, 1M

2 adultos, 1 juvenil

adulto

1 juvenil, 2 adultos

juvenil

adulto

juvenil

adulto

Vásquez-Cruz & Fuentes-Moreno - Axantismo en Smilisca baudinii

118 Kenai, Estados Unidos

Lithobates clamitans

Lithobates sphenocephalus

Lithobates pipiens

Lithobates sylvaticus

Odorrana ishikawae

Pelophylax kl. esculentus

visible, normal

Maine, Vermont, Massachusetts, New York, New Jersey, Estados Unidos. SE de Canadá

Georgia, Estados Unidos

Broadus, Montana, Estados Unidos

Polonia

azul grisáceo

oscuro, parcialmente visible

oscuro

coloración azul sobre cabeza y dorso

azul claro, azul oscuro, azul verdoso

azul cielo claro, verde, marrón oscuro

pequeños parches de azul

parcialmente azul

azul y verde

azul claro, azul oscuro, azul verdoso

azul

Laboratorio

Yukon Delta, Estados Unidos

Tetlin, Estados Unidos

Innoko, Estados Unidos

oscuro, visible

Wisconsin, Minnesota, Estados Unidos

Laboratorio

parcialmente visible

Isla Sapelo, Georgia, Estados Unidos

patrón característico de la especie

Maine, Estados Unidos

Tennessee, USA

patrón característico de la especie

Estados Unidos

Virginia, Estados Unidos

Lithobates clamitans

Maine, Vermont, Massachusetts, New York, New Jersey, SE de Canadá

Lithobates clamitans

patrón de manchado

Wisconsin, Minnesota, Estados Unidos

Lithobates clamitans

Maine, Estados Unidos

Lithobates catesbeianus

negro

adulto

larvas, adulto -

M-H

adulto

pálido doradoamarillo -

adulto

manchas doradas y azules

área natural

Juszczyk, 1987

Miura, 2018

Reeves et al., 2008

Richards et al., 1969

Black, 1967

Berns y Uhler, 1966

Martof, 1964

Hall et al., 2018

Lindemann et al., 2019

Berns y Narayan, 1970

Berns y Uhler, 1966

Lindemann et al., 2019

Cuad. herpetol. 34 (2): 313-320 (2020)

317

318

Pelophylax kl. esculentus

Pelophylax lessonae

Pelophlax lessonae

Pelophylax nigromaculatus

Pelophylax perezi

Pelophylax porosus

Pelophylax plancyi

Zhangixalus arboreus

Zhangixalus schlegelii

Rhacophoridae

Pelophylax kl. esculentus

obscuro, parcialmente visible

Svätý Kríž, República Checa

Okuyama, Ashiya, Kyogo, Japón

Laboratorio -

visible marrón oscuro

azul

rayas dorsolaterales y dorsomediales amarillentas

Maki-cho, Nishikambara-gun, Japón -

semitransparente, negruzco

Wei-hsiu Yuan, China

azul

Laguna de Cospeito, Lugo, España

azul

oscuro

grisáceo

normal

Huelva, España

visible

no visible

Pantà de Vallvidrera, España

Masquefa, España

visible

ciudades de Aioi, Wajima, Mihama y Kaga de Japón

parcialmente visible

Žermanice, República Checa

Wei-hsiu Yuan, China

oscuro, visible

normal, visible

Oldenburg, Alemania

Havířov, República Checa

negro

adulto

subadulto

adulto

marrón amarillento claro -

adulto

negro

3M, 1H

campo de arroz

estanque de lotos

Laguna

Nishioka y Ueda, 1985b

Miura, 2018

Liu, 1931

Nishioka y Ueda, 1985c

Rivera et al., 2001

Martínez-Silvestre et al., 2016

lago artificial _

Martínez-Silvestre et al., 2016

Miura, 2018

Liu, 1931

Dandová et al., 1995

lago artificial

VIček, 2008

Fischer, 1999

lago artificial mina inundada

VIček, 2003

humedales

Vásquez-Cruz & Fuentes-Moreno - Axantismo en Smilisca baudinii

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rufescens (Caudata: Plethodontidae) in Veracruz, México. Cuadernos de Herpetología 34: 99-101. Vlček, P. 2003. Skokan zelený s černou duhovkou. ŽIVA 51: 225. Vlček, P. 2008. Axanthismus u skokana krátkonohého (Pelophylax lessonae). Herpetologické Informace 7: 15.

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Micrablepharus maximiliani Reinhardt and Lütken, 1861 (Reptilia, Gymnophthalmidae): New record of the Caatinga region in Brazil Tatiana Feitosa Quirino1, Dalilange Batista-Oliveira2 Programa de Pós-graduação em Sistemática, Uso e Conservação da Biodiversidade, Departamento de Ciências Biológicas, Universidade Federal do Ceará, Campus Universitário do Pici, CEP 60021970, Fortaleza, CE, Brazil. 2 Universidade Regional do Cariri (URCA), Programa de Pós-Graduação em Bioprospecção Molecular. Cel. Antônio Luis, Pimenta Street 1161, CEP 63.105-000 Crato, CE, Brazil. 1

Locality- Six individuals of Micrablepharus maximiliani were found in Caatinga region, Sítio Cuncas (S 7° 5’ 24.09”; W 38°43’28.20”), municipality of Barro, state of Ceará. The area is located in the drainage basin of Salgado river, prevailing alongside its extension, and the vegetation composed of Deciduous Thorny Woodland and semi-deciduous Tropical Rainforest (IPECE, 2017). The specimens were captured in August, 2014, through the visual surveys. They were collected by Tatiana F. Quirino and Dalilange B. Oliveira. The lizards were deposited in the Herpetology Collection in the Universidade Regional do Cariri, and categorized into the numbers: URCA-H 9574-9575-9576-9577-9578-9671.

Comments- Micrablepharus maximiliani (Fig 1) is a small gymnophthalmid lizard (CRL 38,2-45,7 mm) that is widespread distributed in South America, with records for Atlantic Forest, Caatinga, Cerrado, and Pantanal in Brazil, and Humid Chaco in Paraguay (Rodrigues, 1996a). According to Werneck et al. (2009), this species is widespread in Cerrado and enters neighboring biomes, as such as the Caatinga, where it occurs punctual form, in mesic habitats, generally associated with the most prominent relief region (Vanzolini et al., 1980; Rodrigues, 2003). The population of this species also occurs in enclaves of Savannah in the Amazon region (Avila-Pires, 1995; Gainsbury and Colli, 2003). This species is diurnal

Figure 1. Individual of Micrablepharus maximiliani from Cuncas, Ceará (photo by Herivelto Oliveira). Author for correspondence: tata_tatifeitosa@hotmail.com

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T. F. Quirino and D. Batista-Oliveira - New record Micrablepharus maximiliani for the Caatinga and have semifossorial habits, living in the leaf-litter or open ground, and in isolated forests known as “Brejos de Altitude” (Rodrigues, 2003; Moura et al., 2010; Abrantes et al., 2011). As we mentioned before, this species is a semifossorial lizard and often is associated with rock outcrops, leaf-litter and bare ground, usually found in sandy-soil habitats, or inside termite mounds (Rodrigues, 1996a, 2003; Mesquita et al., 2006; Werneck et al., 2009). According to literature and collection records, Micrablepharus maximiliani occurs in the municipalities of Palmeira dos Índios, state of Alagoas (Rodrigues, 1996a); Lençóis, Santo Inácio and Vacaria, state of Bahia (Juncá, 2005; Rodrigues, 1996b); Arajara, Caucaia, Crateús, Crato, Fortaleza, Ibiapaba, Milagres, Mulungú, São Benedito, Tianguá and Ubajara, state of Ceará (Moura et al., 2010; Rodrigues, 1996a; Borges-Nojosa and Caramaschi, 2003; Borges-Nojosa and Gascon, 2005) (Fig 2). The current work spreads the distribution of Micrablepharus maximiliani in the state of Ceará toward to the Sítio Cuncas (S 7° 10’ 36”; W 38°46’54”), municipality of Barro, around 440 km to the northwest in relation to the location of type-species in the Maruim, municipality of Sergipe (Rodrigues, 1996a). It stretches about to 80 km southwest of Crato, Ceará (Borges-Nojosa and Caramaschi, 2003), in relation to the Sítio de Cuncas, municipality Barro, Ceará, thereby stretching the distribution of this species to the Caatinga region inward.

Figure 2. Geographic distribution of Micrablepharus maximiliani in Caatinga. Pink circles represent the previous records from literature (Rodrigues, 1996a.; Rodrigues, 1996b; BorgesNojosa and Caramaschi, 2003; Borges-Nojosa and Gascon, 2005; Juncá, 2005; Moura et al., 2010), the black star represents the type-locality (Rodrigues, 1996a) and the red triangle shows the our new record, Cuncas, municipality Barro, Ceará (Map by Tatiana F. Quirio).

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Acknowledgements We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CA PES) for authors grants. We thank to H. F. for his photography. Finally, we thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for collecting permits. Literature cited

Abrantes, S.H.F.; Abrantes, M.M.R. & Falcão, A.C.G.P. 2011. A fauna de lagartos em três brejos de altitude de Pernambuco, nordeste do Brasil. Revista Nordestina de Zoologia 5: 23-29. Avila-Pires, T.C.S. 1995. Lizards of Brazilizan Amazonia (Reptilia: Squamata). Zoologische Verhandelingen 299: 1-706. Borges-Nojosa, D.M. & Caramaschi, U. 2003. Composição e análise comparativa da diversidade e das afinidades biogeográficas dos lagartos e anfisbenídeos (Squamata) dos brejos nordestinos; p. 463-512 In: I.R. Leal, M. Tabarelli and J.M.C. Silva (ed). Ecologia e Conservação da Caatinga. Recife: Editora Universitária da UFPE. Borges-Nojosa, D.M. & Gascon, P. 2005. Herpetofauna da área da reserva da Serra das Almas, Ceará; p. 243-258 In: F.S. Araújo, M.J.N. Rodal and M.R.V. Barbosa (ed.). Análise das Variações da Biodiversidade do Bioma Caatinga: suporte a estratégias regionais de conservação. Brasília: Ministério do Meio Ambiente (MMA). Gainsbury, A.M. & Colli, G.R. 2003. Lizards assemblages from natural Cerrado enclaves in southwestern Amazonia: the role of stochastic extinctions and isolation. Biotropica 35: 503-519. Instituto de Pesquisa e Estratégia Econômica do Ceará – IPECE. 2017. PERFIL MUNICIPAL. Fortaleza, Ceará, Brasil. Disponible en: http://www.ipece.ce.gov.br Juncá, F.A. 2005. Anfíbios e Répteis; p. 337-356 In F.A. Juncá, L. Funch and W. Rocha (ed.) Biodiversidade e Conservação da Chapada Diamantina. Brasília: Ministério do Meio Ambiente (MMA). Mesquita, D.O.; Colli, G.R.; França, F.G.R. & Vitt, L.J. 2006. Ecology of a Cerrado Lizard Assemblage in the Jalapão Region of Brazil. Copeia 2006: 460-471. Moura, M.R.; Dayrell, J.S. & São-Pedro, V.A. 2010. Reptilia, Gymnophtalmidae, Micrablepharus maximiliani (Reinhardt and Lutken, 1861): Distribution extension, new state record and geographic distribution map. Check List 6: 419-426. Rodrigues, M.T. 1996a. A New Species of Lizard, Genus Micrablepharus (Squamata: Gymnophthalmidae), from Brazil. Herpetologica 52: 535-541. Rodrigues, M.T. 1996b. Lizards, snakes, and amphisbaenians from the quaternary sand dunes of the middle rio São Francisco, Bahia, Brazil. Journal of Herpetology 30: 513-523. Rodrigues, M.T. 2003. Herpetofauna da Caatinga; p. 181-236 In I.R. Leal, M. Tabarelli and J.M.C. Silva (ed.). Ecologia e Conservação da Caatinga. Recife: Editora Universitária da UFPE. Vanzolini, P.E.; Ramos-Costa, A.M.M & Vitt, L.J. 1980. Répteis das Caatingas. Academia Brasileira de Ciências, Rio de Janeiro.

Cuad. herpetol. 34 (2): 321-323 (2020) Werneck, F.P.; Colli, G.R. & Vitt, L.J. 2009. Determinants of assemblage structure in Neotropical dry forest lizards. Austral Ecolology 34: 97-115. Recibida: 2 8 S e p t i e m b r e 2 0 1 9 Revisada: 0 9 M a r z o 2 0 2 0 Aceptada: 3 1 M a r z o 2 0 2 0 Editor Asociado: A. S. Quinteros doi: 10.31017/CdH.2020.(2019-035)

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Confirmación de la presencia de Aspronema dorsivittatum Cope, 1862 (Squamata: Scincidae) en la provincia de San Juan Rodrigo Gómez Alés1,2, Juan Carlos Acosta1,3, Mariano Basso1 DIBIOVA (Diversidad y Biología de Vertebrados del Árido). Departamento de Biología. Facultad de Ciencias Exactas, Físicas y Naturales. Universidad Nacional de San Juan. Av. Ignacio de la Roza 590 (O), Rivadavia, San Juan, CPA: J5402DCS. Argentina. 2 CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas), Argentina. 3 CIGEOBIO-CONICET. Facultad de Ciencias Exactas, Físicas y Naturales. Universidad Nacional de San Juan. Av. Ignacio de la Roza 590 (O), Rivadavia, San Juan, CPA: J5402DCS. Argentina. 1

Localidad- República Argentina. Provincia de San Juan, Departamento Rawson (31° 38’ 14.37’’ S; 68° 28’ 52.65’’ O, 588 m s.n.m.; Fig. 1). Fecha de colección: octubre 2019. Colector: Mariano Basso. El ejemplar capturado fue depositado en la Colección Herpetológica del Departamento de Biología, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de San Juan (UNSJ- 2633). Comentarios- La distribución geográfica de Aspronema dorsivittatum es particularmente irregular, con citas para Argentina, Bolivia, Brasil, Paraguay y Uruguay; con presencia confirmada en Argentina para Buenos Aires, Chaco, Corrientes, Córdoba, Entre Ríos, Formosa, Mendoza, Misiones, San Luis, Salta, Santa Fe, Santiago del Estero y Tucumán (Cei,

Figura 1. Mapa de distribución de Aspronema dorsivittatum en Argentina, indicando en gris las provincias donde ha sido citada (Cei, 1993; Abdala et al., 2012; Avila et al., 2013). En San Juan, se señala el registro a confirmar reportado por Haene (1991) para la localidad de Las Tumanas, departamento Valle Fértil (círculo negro) y el nuevo registro para la provincia en la localidad Médano de Oro, departamento Rawson (estrella roja).

1993; Williams y Kacoliris, 2011; Abdala et al., 2012; Avila et al., 2013). Para la provincia de San Juan, A. dorsivittatum fue mencionada por primera vez por Haene (1991), quien basó su reporte en un ejemplar hallado en las nacientes del río Las Tumanas en el departamento de Valle Fértil y luego fue liberado. Por esa razón, posteriormente Avila et al. (1998) lo mencionan como especie a confirmar por no poder corroborarse la cita con un ejemplar de referencia. Esta categoría se mantuvo en trabajos posteriores (Avila et al., 2013; Acosta et al., 2015) y no es mencionada en la última revisión de los reptiles de San Juan (Acosta et al., 2018). Un ejemplar hembra (longitud hocico-cloaca 80 mm) fue hallado muerto, con el extremo caudal cortado, en el interior de una pileta en la localidad del Médano de Oro, departamento Rawson, ubicado al sureste de San Juan. Este registro se encuentra a 138 km y 220 km aproximadamente en línea recta hacia el norte de los registros confirmados más cercanos en Las Heras y La Paz (Provincia de Mendoza), respectivamente (Harvard University y Morris, 2020; Faivovich y Rodríguez, 2020). El individuo capturado presenta algunos caracteres diagnósticos y merísticos propios de la especie como: dos escamas frontoparietales, una escama rostral ancha y más angosta que la mental, siete escamas supralabiales (la segunda y tercera en contacto con dos loreales, y la quinta en contacto con supralabiales), escama frontonasal en contacto con la rostral y frontal pentagonal, cuatro escamas superciliares. Presenta 32 escamas alrededor de la mitad del cuerpo, las escamas ventrales y dorsales son lisas cicloides e imbricadas, de coloración dorsal marrón brillante con línea vertebral marrón más oscura que el dorso del cuerpo, cuatro bandas longitudinales dorsolaterales claras (2 a cada lado del cuerpo), las bandas

Autor para correspondencia: rodri.gomezales@gmail.com

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R. Gómez Alés et al. - Aspronema dorsivittatum en San Juan

Figura 2. Vista dorsolateral de Aspronema dorsivittatum (LHC= 80 mm; UNSJ- 2633) colectado en el departamento Rawson, provincia de San Juan. Foto: Juan Carlos Acosta.

se prolongan desde la región cefálica hasta parte de la cola; ventralmente de coloración grisáceo claro (Gallardo, 1968; Cei, 1993; Cabrera, 2017; Fig. 2). Esta especie es considerada un generalista ecológico y de hábitat, relacionada con su amplia distribución (Gudynas, 1980; Cei, 1993). Se ha reportado su presencia en ambientes de pastizales húmedos con bosque, ambientes secos con algo de bosque, lomas pedregosas con pastos y en zonas de viviendas con plantación artificial; por otro lado, se ha mencionado un comportamiento acuático principalmente cuando se siente amenazada, por lo que se asocia su presencia a cuerpos de agua cercanos y a hábitat de bañados u orillas de lagunas (Gallardo 1968; Gudynas, 1980; Cei 1993; Cabrera, 2017). En este sentido, el sitio donde fue encontrada la hembra se caracteriza por ser una zona rural con diversos cultivos y algunos parches con vegetación natural; se trata de una zona húmeda por la proximidad de las napas freáticas a la superficie y pueden observase numerosos “piletones” como reservorio de agua para regadío y piletas de uso recreativo. Asimismo Las Tumanas (Dpto. Valle Fértil), el sitio donde la especie fue citada con anterioridad a 133 km en línea recta hacia el noreste de la provincia (Haene, 1991), se caracteriza por ser un ambiente húmedo serrano con un estrato arbóreo y herbáceo correspondiente al Chaco Occidental, con cursos de agua permanentes en las nacientes del arroyo Las Tumanas. Con este registro la diversidad de reptiles de San Juan asciende a 64 especies, confirmando con material de referencia la presencia de Aspronema dorsivittatum para la provincia. Agradecimientos A Jorge Williams por su amabilidad al brindarnos 326

material bibliográfico, y a Kevin Rojas por su colaboración en la edición de imágenes. Al Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, beca doctoral RGA). A S. Quinteros por sus sugerencias para mejorar la nota. Literatura citada

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Cuad. herpetol. 34 (2): 325-327 (2020) Herpetology National Collection (MACNHe). Museo Argentino de Ciencias Naturales. Occurrence dataset https:// doi.org/10.15468/yjmpnn accessed via GBIF.org on 202005-01. https://www.gbif.org/occurrence/2231739. Gallardo, J.M. 1968. Las especies argentinas del género Mabuya Fitzinger. Revista del Museo Argentino de Ciencias Naturales, Zoología 9: 177-196. Gudynas, E. 1980. Notas adicionales sobre la distribución, ecología y comportamiento de Mabuya dorsivittata (Lacertilia: Scincidae). Contribuciones en Biología del Centro Educativo Don Orione 2: 1-13. Haene, E. 1991. Presencia de Mabuya dorsivittata Cope (Reptilia,

Scincidae) en la provincia de San Juan, República Argentina. Boletines Científicos APRONA 19: 46-47. Harvard University M. & Morris, P.J. 2020. Museum of Comparative Zoology, Harvard University. Version 162.204. Museum of Comparative Zoology, Harvard University. Occurrence dataset https://doi.org/10.15468/ p5rupv accessed via GBIF.org on 2020-05-01. https://www. gbif.org/occurrence/476660863. Williams, J. & Kacoliris, F. 2011. Squamata, Scincidae, Mabuya dorsivittata (Cope, 1862): distribution extension in Buenos Aires province, Argentina. Check List 7: 388.

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Primer registro de Philodryas nattereri (Steindachner 1870) (Serpentes, Dipsadidae) en Bolivia Gonzalo Navarro-Cornejo, Lucindo Gonzales Museo de Historia Natural Noel Kempff Mercado, Universidad Autónoma Gabriel René Moreno, Departamento de Herpetología. Casilla 2489, Tel./Fax: 3-366574. Santa Cruz, Bolivia.

Localidad- Bolivia, Departamento Santa Cruz, Provincia Chiquitos, Arroyo El Arco, Serranía Santiago de Chiquitos (18°20’48.70”S; 59°33’38.34”O, 800 m s.n.m, Fig. 1). El 19 de julio de 2007 fue colectado un ejemplar hembra de Philodryas nattereri en pastizal natural del campo rupestre (formación del Cerrado). El espécimen está depositado en la colección herpetológica del Museo de Historia Natural “Noel Kempff Mercado” en Santa Cruz (MNKR 5554). Comentarios- Este representa el primer registro de Philodryas nattereri para Bolivia, aumentando a 13 las especies del género presentes en el país. La especie

Figura 1. Mapa de distribución de Philodryas nattereri. Estrella: nuevo registro en Bolivia. Puntos: los registros más cercanos en Brasil y Paraguay. Ecorregiones según Ibisch et al. (2003).

fue originalmente descrita del Estado de Mato Grosso en Brasil, y durante mucho tiempo se la consideró endémica de Brasil, hasta su hallazgo en Paraguay (Smith et al., 2013). La referida localidad en Bolivia, dista un poco más de 200 km hacia el oeste de los registros más cercanos conocidos en Brasil (Fig. 1) mencionados por Nogueira et al. (2019). La Serranía de Santiago de Chiquitos corresponde a la ecorregión del Cerrado (Ibisch et al., 2003), coincidiendo con los ambientes preferentemente habitados por la especie en Brasil y Paraguay, donde también habita en Bosques Secos Chiquitanos y la Caatinga (Cabral y Bueno-Villafañe, 2015; Caccialli et al., 2016; Nogueira et al., 2019). Durante un recorrido casual, el ejemplar fue observado y luego capturado a horas 15:30 mientras se desplazaba por el suelo en el área de pastizal, el día era soleado con poca nubosidad. El ejemplar mide 437 mm de longitud hocicocloaca, extremidad caudal parcialmente amputada (78+ mm), escamas dorsales 21-21-17, lisas, ventrales 211, placa anal dividida, subcaudales en 55+ pares, loreal 1/1 (derecha/izquierda), preocular 1/1, postoculares 2/2, temporales 2+3+4/2+3+3, supralabiales 8(4-5)/8(4-5), infralabiales 11(1-5)/11(1-5). Dentición maxilar 13+2. La coloración es la típica de la especie destacando una franja latero ventral naranja-amarillenta en la zona posterior a la comisura bucal (Fig. 2). El nuevo registro se ubica en la “Reserva Municipal de Vida Silvestre Valle de Tucabaca”, área protegida, con una extensión de 2623 km2, de importancia turística por los diferentes atractivos naturales en la zona y considerablemente afectada por incendios de gran magnitud suscitados en el año 2019. Por tanto, considerando el tiempo transcurrido desde la colecta del espécimen, la carga antropogénica y el impacto por las quemas recientes, es necesario realizar muestreos en la zona para conocer el estado de conservación actual de la especie en el país.

Autor para correspondencia: gonzalonavarrocornejo@gmail.com

329

G. Navarro Cornejo & L. Gonzales - Philodryas nattereri en Bolivia

Figura 2. Vista dorsal (arriba) y ventral (abajo) del ejemplar de Philodryas nattereri registrado en Bolivia.

330

Cuad. herpetol. 34 (2): 329-331 (2020) Agradecimientos A Pier Cacciali por las contribuciones realizadas para la mejora de la presente nota y a M. L. Rivero por la preparación del mapa. Literatura citada

Cacciali, P.; Scott, N.; Aquino, A.; Fitzgerald, L. & Smith, P. 2016. The Reptiles of Paraguay: Literature, Distribution, and an Annotated Taxonomic Checklist. Special Publication of the Museum of Southwestern Biology 11: 1-373. Cabral, H. & Bueno-Villafañe, D. 2015. The Genus Philodryas (Wagler, 1830) (Serpentes: Dipsadidae) in Paraguay: Distribution and Ecological Affinities. Boletín del Museo Nacional de Historia Natural del Paraguay 19: 5-18. Ibisch, P. L.; Beck, S. G.; Gerkmann, B. & Carretero, A. 2003. La diversidad biológica: ecorregiones y ecosistemas: 47-88. En: Ibisch, P.L. & Mérida, G. (eds.) Biodiversidad: La Riqueza

de Bolivia. Editorial Fundación Amigos de la Naturaleza (FAN), Santa Cruz-Bolivia. Nogueira C. C.; Argôlo A.J.S.; Arzamendia V.; Azevedo J. A.; Barbo F.E.; Bérnils R.S.; Bolochio B.E.; Borges-Martins M.; Brasil-Godinho M.; Braz H.; Buononato M. A.; CisnerosHeredia D.F.; Colli G.R.; Costa H.C.; Franco F.L.; Giraudo A.; Gonzalez R.C.; Guedes T.; Hoogmoed M.S.; Marques O. A. V.; Montingelli G.G.; Passos P.; Prudente A.L.C.; Rivas G. A.; Sanchez P.M.; Serrano F.C.; Silva N.J.; Strüssmann C.; Vieira-Alencar J.P.S.; Zaher H.; Sawaya R.J.; & Martins M. 2019. Atlas of Brazilian Snakes: Verified Point-Locality Maps to Mitigate the Wallacean Shortfall in a Megadiverse Snake Fauna. South American Journal of Herpetology 14: 1-274. Smith, P.; Scott N.; Cacciali, P.; Atkinson, K. & Pheasey, H. 2013. Confirmation of the presence of Philodryas nattereri Steindachner, 1870 (Squamata: Dipsadidae) in Paraguay. Herpetozoa 26: 91-94.

Recibida: 0 7 J u l i o 2 0 2 0 Revisada: 0 8 J u l i o 2 0 2 0 Aceptada: 28 Julio 2020 Editor Asociado: J. Goldberg doi: 10.31017/CdH.2020.(2020-052)

331

Novedad zoogeográfica

Cuad. herpetol. 34 (2): 333-337 (2020)

First records of Homonota underwoodi Kluge, 1964 (Squamata: Phyllodactylidae) for the province of Córdoba, Argentina José Manuel Sánchez1,2, Rafael Alejandro Lara-Reséndiz1,2, Suelem Muniz Leão1,2, Nicolás Pelegrin1,2 Universidad Nacional de Córdoba, Facultad de Ciencias Exactas, Físicas y Naturales, Centro de Zoología Aplicada, Rondeau 798, X5000AVP Córdoba, Argentina. 2 Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Instituto de Diversidad y Ecología Animal (IDEA), CONICET/UNC. Córdoba, Argentina. 1

Localities- Argentina. Province of Córdoba, Department of San Alberto, Las Toscas (30°09’30.32”S, 64°53’29.99”W; WGS84, 183 m a.s.l.). Date: December 10, 2019. Collected by N. Pelegrin, R. A. Lara-Reséndiz, and J. M. Sánchez. Vouchers: LECOH00732 and LECOH00733. Argentina. Province of Córdoba, Department of San Alberto, Las Toscas (30°10’42.36”S, 64°53’23.66”W; WGS84, 192 m a.s.l.). Date: January 18, 2020. Collected by J. M. Sánchez and G. P. Pesci. Voucher: LECOH 00734. All specimens are deposited in the collection of Laboratory of Ecology and Conservation of Herpetofauna (IDEA, CONICETUNC). Comments- The genus Homonota is distributed from 15° to 54° latitude South in the Monte, Chaco, Espinal, Andes, and Pampas biomes, with records in Bolivia, Paraguay, Brazil, Argentina, and Uruguay (Cei 1978, Abdala 1993, Morando et al. 2014). Homonota underwoodi belongs to the horrida group along with H. horrida, H. septentrionalis, and H. marthae (Cacciali et al. 2018), and is the only in this group with irregular coloration in the dorsum (opposed to a banded coloration pattern). It can be distinguished from H. darwinii, H. uruguayensis, H. taragui, H. williamsii, H. borelli, and H. rupicola, by the lack of keeled scales, and from H. andicola and H. withii—morphologically most similar to H. underwoodi—by the absence of chromatophores in the belly (Cacciali et al. 2018). Homonota underwoodi is endemic to Argentina, with records for the provinces of Catamarca, La Rioja, San Luis, La Pampa, San Juan, Mendoza, Neuquén, and Río Negro (Cei 1978, Abdala 1993, Cei 1993, Tiranti y Avila 1997, Ávila et al. 1998, Guerreiro et al. 2005, Perez et al. 2005, Corbalán y

Debandi 2008, Sanabria y Quiroga 2009, Sanabria y Quiroga 2010, Perez et al. 2011, Medina et al. 2012, Morando et al. 2014, Daza et al. 2017) (Fig. 1, Table 1). It is a species of psammophile habits and typical of the dry conditions of the Monte desert (Cei 1978). The species known distribution is mainly restricted to the Monte desert and in Monte desert-Arid Chaco ecotonal areas (Fig. 1, Table 1). During a sampling carried out in Salinas Grandes Multiple Use Reserve (Salinas Grandes reserve), nineteen specimens of H. underwoodi were

Figure 1. Distribution of Homonota underwoodi based on records from different data sources (listed in Table 1). Locality for the new records in Salinas Grandes is shown as a red star.

Author for correspondence: pelegrin.nicolas@gmail.com

333

J. Sánchez et al. - First records of Homonota underwoodi for Córdoba Table 1. List of records showed in Figure 1, including Province, georeference, type of record, and bibliographic source. Some points were extracted from maps included in publications; these points are noted in the table with an asterisk. From GBIF, only records with preserved specimens were included.

Province

Longitude

Latitude

Type of record

La Rioja

-67.611612

-29.989231

Published Records

Cei, 1993*

La Rioja

-67.554186

-28.802028

Published Records

Cei, 1993*

La Rioja

-66.807654

-28.756366

Published Records

Cei, 1993*

La Rioja

-67.324484

-28.573719

Published Records

Cei, 1993*

La Rioja

-66.991244

-29.079211

Published Records

Cei, 1986*

La Rioja

-68.550000

-29.550000

Published Records

Cajade et al., 2013

La Rioja

-67.933333

-29.833333

Published Records

Kass et al., 2018

La Rioja

-67.783333

-29.733333

Published Records

Kass et al., 2018

La Rioja

-67.733333

-30.116667

Published Records

Kass et al., 2018

La Rioja

-67.047472

-31.423639

GBIF

Gbif, 2019

La Rioja

-67.816670

-29.800000

GBIF

Gbif, 2019

Catamarca

-66.003697

-27.797471

Published Records

Cei, 1993*

Catamarca

-66.348250

-28.756366

Published Records

Cei 1993*

Catamarca

-67.600000

-27.520000

Published Records

Cajade et al., 2013

Catamarca

-66.316700

-27.600000

GBIF

Gbif, 2019

Catamarca

-66.416700

-28.116700

GBIF

Gbif, 2019

Córdoba

-64.889906

-30.178433

New Record

this work

San Luis

-67.152208

-32.089668

Published Records

Cei, 1993*

San Luis

-67.066667

-32.616667

Published Records

Guerreiro et al., 2005

La Pampa

-67.094782

-37.432084

Published Records

Cei, 1993*

La Pampa

-66.427214

-37.387089

Published Records

Tiranti and Avila, 1997

La Pampa

-68.082125

-37.583319

Published Records

Tiranti and Avila, 1997

La Pampa

-67.615019

-37.207383

Published Records

Tiranti and Avila, 1997

San Juan

-68.054820

-30.110290

Type Locality

San Juan

-67.439335

-30.719817

Published Records

Cei and Castro, 1978*

San Juan

-67.324484

-30.856802

Published Records

Cei and Castro, 1978*

San Juan

-67.898739

-32.044006

Published Records

Cei and Castro, 1978*

San Juan

-67.783889

-31.952683

Published Records

Cei, 1993*

San Juan

-67.324484

-31.587390

Published Records

Cei, 1993*

San Juan

-67.956165

-31.450405

Published Records

Cei, 1993*

San Juan

-67.611612

-30.354525

Published Records

Cei, 1993*

San Juan

-68.128442

-29.989231

Published Records

Cei, 1993*

San Juan

-68.642108

-31.088525

Published Records

Ávila et al., 1998

San Juan

-68.534272

-30.144342

Published Records

Ávila et al., 1998

San Juan

-69.438994

-30.667300

Published Records

Ávila et al., 1998

San Juan

-68.683333

-31.316667

Published Records

Marinero et al., 2003

San Juan

-68.683333

-31.316667

Published Records

Marinero et al., 2003

San Juan

-67.916667

-30.083333

Published Records

Sanabria and Quiroga, 2009

San Juan

-68.700000

-31.550000

Published Records

Sanabria and Quiroga, 2010

San Juan

-68.446000

-31.313000

Published Records

Cacciali et al., 2017

San Juan

-68.209000

-31.662000

Published Records

Cacciali et al., 2017

334

Source

Kluge, 1964

Cuad. herpetol. 34 (2): 333-337 (2020) San Juan

-67.791626

-32.218735

GBIF

Mendoza

-68.587846

-33.002901

Published Records

Cei and Castro, 1978*

Mendoza

-68.932399

-33.231209

Published Records

Cei and Castro, 1978*

Mendoza

-68.817548

-33.322533

Published Records

Cei and Castro, 1978*

Mendoza

-69.047250

-33.459518

Published Records

Cei and Castro, 1978*

Mendoza

-68.013590

-34.007458

Published Records

Cei and Castro, 1978*

Mendoza

-68.932399

-34.692383

Published Records

Cei and Castro, 1978*

Mendoza

-68.128442

-34.098782

Published Records

Cei, 1993*

Mendoza

-68.472995

-33.550842

Published Records

Cei, 1993*

Mendoza

-68.185867

-33.185548

Published Records

Cei, 1993*

Mendoza

-68.760123

-33.139886

Published Records

Cei, 1993*

Mendoza

-68.185867

-32.546285

Published Records

Cei, 1993*

Mendoza

-68.020000

-32.380000

Published Records

Werner et al., 1996

Mendoza

-68.883333

-34.083333

Published Records

Corbalán and Debandi, 2008*

Mendoza

-68.698121

-32.610713

Published Records

Corbalán and Debandi, 2008*

Río Negro

-67.083333

-39.100000

Published Records

Perez et al., 2005

Río Negro

-66.300000

-39.050000

Published Records

Perez et al., 2011

Río Negro

-66.533333

-39.083333

Published Records

Perez et al., 2011

Río Negro

-67.250000

-38.883333

Published Records

Perez et al., 2011

Neuquén

-69.140056

-38.422891

Published Records

Medina et al., 2012

Neuquén

-68.237762

-38237762

Published Records

Medina et al., 2012

Neuquén

-69.092336

-37.262336

Published Records

Medina et al., 2012

registered (12 adults, 5 juveniles, and 2 newborns), from which three were collected, and 16 were released after identification and measurement. Voucher specimens LECOH00732 (SVL: 44 mm) and LECOH00733 (SVL: 46 mm) are adult individuals captured with drift fence-pitfall traps in an Arid Chaco forest surrounding the Salinas Grandes reserve. Voucher specimen LECOH00734 is a juvenile (SVL: 29.45 mm) captured by hand in a nocturnal survey along internal paths near the park ranger station at Las Toscas. All captured individuals of H. underwoodi presented yellow coloration in parts of the body, mainly in the head above the eyes—forming yellow eyebrows sometimes extended to the nose—and in the tail. Some individuals presented yellow scales on flanks, the vertebral line, the occipital region, and around nostrils (Fig. 2). Our records extend the species known distribution ~ 215 km to the southeast of the closer published record in Catamarca (Fig. 1) and are the first records for the Province of Córdoba, increasing its total number of lizard species to 30 (Cabrera et al. 2018). Most individuals were recorded in areas with

Gbif, 2019

sandy soil (Fig. 2A), typical vegetation of transitional Arid Chaco forest composed by thorny shrubs, cacti, and woody plants like Parkinsonia praecox, Geoffrea decorticans, Prosopis sp., and Aspidosperma quebracho-blanco. Some individuals were observed in a sparse semi-halophytic shrubland located in a drainage area with calcrete floor (Fig. 2B). In these areas, H. underwoodi was found in syntopy with typical Chaco lizard species like Teius teyou, Stenocercus doellojuradoi, Vanzosaura rubricauda, and other two Homonota species, H. borelli and H. horrida. Our records locate H. underwoodi in an Arid Chaco area with extremely dry conditions (rains around 300 mm/yr and summer maximum temperatures around 50° C). Sandy soils along with local climatic conditions resemble those of the Monte desert where the species is common. The more structurally complex vegetation of the Arid Chaco seems not to be a constraining factor for the presence of the species. Acknowledgments NP thanks CONICET for funding PIP # 112201 50100566 and The Rufford Foundation for grant 335

J. Sรกnchez et al. - First records of Homonota underwoodi for Cรณrdoba

Figure 2. Homonota underwoodi from Salinas Grandes, Cรณrdoba (Argentina), showing individuals on sandy (A) and calcrete substrate (B). Note the yellow coloration in head and tail.

336

Cuad. herpetol. 34 (2): 333-337 (2020) RSG18820-2. RALR and SML thank CONICET for funding their postdoctoral fellowships. JMS thanks CONICET for funding his doctorate through an Intern Doctoral Fellowship. The authors want to thank Secretaría de Ambiente y Cambio Climático of Córdoba Province for permission to work on Salinas Grandes Multiple Use Reserve (#78223505370719). We also thank family Bustamante for permitting us to work in their property and for kindly accepting us in their home. Literature cited

Abdala, V. 1993. Análisis fenético del género Homonota (Sauria: Gekkonidae). Acta Zoologica Lilloana 42: 283-289. Ávila, L.J.; Acosta, J.C. & Murúa, F. 1998. Herpetofauna de la provincia de San Juan, Argentina: lista comentada y distribución geográfica. Cuadernos de Herpetologia 12: 11-29. Cabrera, M.R.; Muniz Leão, S. & Pelegrin, N. 2018. First records of Ameivula abalosi (Cabrera, 2012)(Squamata: Teiidae) for the province of Córdoba, Argentina. Cuadernos de Herpetologia 32: 71-73. Cacciali, P.; Morando, M.; Avila, L.J. & Koehler, G. 2018. Description of a new species of Homonota (Reptilia, Squamata, Phyllodactylidae) from the central region of northern Paraguay. Zoosystematics and Evolution 94: 147-161. Cacciali, P.; Morando, M.; Medina, C.D.; Köhler, G.; Motte, M. & Avila, L.J. 2017. Taxonomic analysis of Paraguayan samples of Homonota fasciata Duméril & Bibron (1836) with the revalidation of Homonota horrida Burmeister (1861) (Reptilia: Squamata: Phyllodactylidae) and the description of a new species. PeerJ 5: e3523. Cajade, R.; Etchepare, E.G.; Falcione, C.; Barrasso, D.A. & Alvarez, B.B. 2013. A new species of Homonota (Reptilia: Squamata: Gekkota: Phyllodactylidae) endemic to the hills of Paraje Tres Cerros, Corrientes Province, Argentina. Zootaxa 3709: 162-176. Cei, J.M. 1978. Estado taxonómico y distribución geográfica de las especies del género Homonota (Sauria, Gekkonidae). Publicaciones Ocasionales del Instituto de Biología Animal Serie científica nº 9. Cei, J.M. 1986. Reptiles del centro, centro-este y sur de la Argentina. Herpetofauna de las zonas áridas y semiáridas. Museo Regionale di Scienze Naturali. Torino. Cei, J.M. 1993. Reptiles del noroeste, nordeste y este de Argentina. Herpetofauna de las selvas subtropicales, puna y pampas. Museo Regionale di Scienze Naturali. Torino. Cei, J.M. & Castro, L.P. 1978. Atlas de los vertebrados inferiores de la región de Cuyo. Publicaciones Ocasionales del Instituto de Biología Animal Serie Científica 2: 1-39. Corbalán, V.E. & Debandi, G. 2008. La lacertofauna de Mendoza: lista actualizada, distribución y riqueza. Cuadernos de Herpetologia 22: 5-24. Daza, J.D.; Gamble, T.; Abdala, V. & Bauer, A.M. 2017. Cool Geckos: does plesiomorphy explain morphological similarities between Geckos from the Southern Cone? Journal of Herpetology 51: 330-342. Gbif. 2019. Homonota underwoodi Kluge, 1964. Disponible en:

https://www.gbif.org/species/2446162. Último acceso: 20 abril 2020. Guerreiro, A.; Baldoni, J. & Brigada, A. 2005. Herpetofauna from Sierra de las Quijadas (San Luis, Argentina). Gayana (Concepción) 69: 6-9. Kass, C.; Kass, N.A.; Velasco, M.A.; Juri, M.D.; Williams, J.D. & Kacoliris, F.P. 2018. Inventory of the herpetofauna of Talampaya National Park, a World Heritage Site in Argentina. Neotropical Biology and Conservation 13: 202-211. Kluge, A.G. 1964. A revision of the South American gekkonid lizard genus Homonota Gray. American Museum Novitates 2193. Marinero, J.A.; Acosta, J.C. & Villavicencio, H.J. 2003. Homonota underwoodi (Underwood’s gecko). Body temperature. Herpetological Review 34: 144-145. Medina, C.; Morando, M.; Minoli, I.; Breitman, M.; Sites, J.J. & Avila, L.J. 2012. Lagartijas de la Provincia de Neuquén (Argentina): estado de conservación, diversidad genética y mapas de distribución geográfica. Informe Técnico. INIBIOMA, CONICET-UNCO. Morando, M.; Medina, C.D.; Avila, L.J.; Perez, C.H.; Buxton, A. & Sites Jr, J.W. 2014. Molecular phylogeny of the New World gecko genus Homonota (Squamata: Phyllodactylidae). Zoologica Scripta 43: 249-260. Perez, C.H.F.; Frutos, N.; Kozykariski, M.; Morando, M.; Perez, D.R. & Avila, L.J. 2011. Lizards of Río Negro Province, northern Patagonia, Argentina. Check List 7: 202-219. Perez, D.R.; Perez, C.H.F. & Ávila, L.J. 2005. Geographic distribution. Homonota underwoodi (Underwod’s Marked Gecko). Herpetological Review 36: 468. Sanabria, E.A. & Quiroga, L.B. 2009. Actualización de la herpetofauna del Parque Provincial Ischigualasto: Comentarios sobre su distribución. Cuadernos de Herpetologia 23: 55-59. Sanabria, E.A. & Quiroga, L.B. 2010. Herpetofauna del Parque Provincial Presidente Sarmiento, San Juan, Argentina. Cuadernos de Herpetologia 24: 57-61. Tiranti, S. & Avila, L. 1997. Reptiles of La Pampa province, Argentina: an annotated checklist. Bulletin of Maryland Herpetological Society 33: 97-117. Werner, Y.; Carrillo De Espinoza, N.; Huey, R.; Rothenstein, D.; Salas, A. & Videla, F. 1996. Observations on body temperatures of some neotropical desert geckos (Reptilia: Sauria: Gekkoninae). Cuadernos de Herpetologia 10: 62-67.

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Notas Records of predation on Ophiodes striatus (Spix, 1824) (Squamata: Diploglossidae) by Oxyrhopus petolarius (Linnaeus, 1758) (Squamata: Dipsadidae) in the northern Atlantic Forest, Brazil Marcos Jorge Matias Dubeux, Ubiratan Gonçalves, Tamí Mottr

247

Diet of Dermatonotus muelleri (Anura: Microhylidae) in a semi-deciduous forest in western Brazil Juan Fernando Cuestas Carrillo, Caroline Galvão, Luciano Alves dos Anjos, Diego José Santana

251

Primer registro de cifoescoliosis en Sceloporus formosus (Squamata: Phrynosomatidae) en Veracruz, México Jorge Luis Castillo-Juárez1, Víctor Vásquez-Cruz2, Laura Pamela Taval-Velázquez

257

First record of the rare snake Cercophis auratus (Schlegel, 1837) (Serpentes: Colubridae: Dipsadinae) in a relictual forest enclave at Caatinga Castiele Holanda Bezerra, Bruno Ferreira Guilhon, Antônio Rafael Lima Ramos, Diva Maria BorgesNojosa

261

Defensive behaviors in two Proceratophrys species (Anura: Odontophrynidae) from central Brazilian Cerrado Afonso Santiago de Oliveira Meneses, Bruno Alessandro Augusto Peña Corrêa

265

Cytogenetic analysis of Rhinella jimi (Stevaux, 2002) (Anura, Bufonidae) from northeastern Brazil Marcelo João da Silva, Maria Rita dos Santos Cândido, Flávia Manoela Galvão Cipriano, Ana Paula de Araújo Vieira, Tamaris Gimenez Pinheiro, Edson Lourenço da Silva

271

Estudo dos hábitos alimentares das serpentes Sibynomorphus neuwiedi e Sibynomorphus mikanii (Squamata, Dipsadidae) de Minas Gerais, Brasil Vinícius José Pilate, Fabiano Matos Vieira, Bernadete Maria de Sousa

275

Dietary composition and feeding strategy of Leptodactylus fuscus (Anura: Leptodactylidae) from a suburban area of the Caribbean Region of Colombia Luis F. Montes, Oscar F. Hernández, Jill L. Martínez, Jose A. Jarava, Jorge A. Díaz

279

New dietary records and geographic variation in the diet composition of the snake Philodryas nattereri in Brazil Raul Fernandes Dantas Sales, Juliana Delfino Sousa, Carolina Maria Cardoso Aires Lisboa, Paulo Henrique Marinho, Eliza Maria Xavier Freire, Marcelo Nogueira de Carvalho Kokubum

285

295

299

Primer registro de ectoparásitos en cinco especies de lagartijas del género Liolaemus (Liolaemidae) y en Teius teyou (Teiidae) Viviana I. Juárez Heredia, Ana G. Salva, Cecilia I. Robles

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Antes verde, ahora azul: primer caso de axantismo en Smilisca baudinii (Duméril y Bibron, 1841) (Amphibia: Anura) Víctor Vásquez-Cruz, Axel Fuentes-Moreno

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Novedades Zoogeográficas Micrablepharus maximiliani Reinhardt and Lütken, 1861 (Reptilia, Gymnophthalmidae): New record of the Caatinga region in Brazil Tatiana Feitosa Quirino, Dalilange Batista-Oliveira

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Confirmación de la presencia de Aspronema dorsivittatum Cope, 1862 (Squamata: Scincidae) en la provincia de San Juan Rodrigo Gómez Alés, Juan Carlos Acosta, Mariano Basso

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Primer registro de Philodryas nattereri (Steindachner 1870) (Serpentes, Dipsadidae) en Bolivia Gonzalo Navarro-Cornejo, Lucindo Gonzales

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First records of Homonota underwoodi Kluge, 1964 (Squamata: Phyllodactylidae) for the province of Córdoba, Argentina José Manuel Sánchez, Rafael Alejandro Lara-Reséndiz, Suelem Muniz Leão, Nicolás Pelegrin

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Cuadernos de

HERPETOLOGÍA VOLUMEN 34 - NUMERO 2 - SEPTIEMBRE 2020 ppct.caicyt.gov.ar/index.php/cuadherpetol/

VOLUMEN 34 - NUMERO 2 Trabajos Bushmaster bites in Brazil: ecological niche modeling and spatial analysis to improve human health measures Nathalie Citeli, Mariana de-Carvalho, Bruno Moreira de Carvalho, Mônica de Avelar Figueiredo Mafra Magalhães, Rosany Bochner

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Serra do Navio, Guiana Shield lowland area, Brazil: a region with high diversity of Squamata Ana Lúcia da Costa Prudente, João Fabrício de Melo Sarmento, Karla Kaliana Camara Costa, Ângelo Cortez Moreira Dourado, Marina Meireles dos Santos, Janaina Reis Ferreira Lima, Jucivaldo Dias Lima, Ulisses Galatti

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Estados de desarrollo en Anadia bogotensis: aportes a la comprensión de la evolución del plan corporal en Gymnophthalmoidea (Squamata) Adriana Jerez, Andrea Bonilla-Garzón, David Samuel Castellanos Montilla

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Diet overlap of three sympatric species of Leptodactylus Fitzinger (Anura: Leptodactylidae) in a Protected area in the Brazilian Amazon Raimundo Rosemiro de Jesus Baia, Patrick Ribeiro Sanches, Fillipe Pedroso dos Santos, Alexandro Cezar Florentino, Carlos Eduardo Costa-Campos

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Herpetofauna of the Environmental Protection Area Delta do Parnaíba, Northeastern Brazil Kássio Castro Araújo, Arthur Serejo Neves Ribeiro, Etielle Barroso de Andrade, Ocivana Araújo Pereira, Anderson Guzzi, Robson Waldemar Ávila

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Serpentes de uma área de proteção urbana da Floresta Atlântica nordestina brasileira Vanessa do Nascimento Barbosa, Jéssica Monique da Silva Amaral, Reginaldo Augusto Farias de Gusmão, Luiz Filipe Lira Lima, José Víctor de Melo Souza, Ivyson Diogo Silva Aguiar, Ednilza Maranhão dos Santos

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Natural history of Xenodon matogrossensis (Scrocchi and Cruz, 1993) (Serpentes, Dipsadidae) in the Brazilian Pantanal Hugo Cabral, Liliana Piatti, Marcio Martins, Vanda L. Ferreira

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Miembro de Publication Integrithy & Ethics

Revista de la Asociación Herpetológica Argentina

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