Animal Biodiversity and Conservation issue 31.1 (2008) by Museu Ciències Naturals de Barcelona MCNB

Formerly Miscel·lània Zoològica

2008

and

Animal Biodiversity Conservation 31.1

Dibuix de la coberta: escurçó pirinenc, víbora áspid, asp viper (Vipera aspis) de Jordi Domènech Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de redacció / Secretaría de redacción / Editorial Office

Secretària de redacció / Secretaria de redacción / Managing Editor Montserrat Ferrer

Museu de Ciències Naturals Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 Nou e–mail abc@bcn.cat

Consell assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Pere Abelló Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Javier Alba–Tercedor Univ. de Granada, Granada, Spain Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament–CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Michael J. Conroy Univ. of Georgia, Athens, USA Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Ignacio Doadrio Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Antonio Donazar Estación Biológica de Doñana–CSIC, Sevilla, Spain Gary D. Grossman Univ. of Georgia, Athens, USA Damià Jaume IMEDEA–CSIC, Univ. de les Illes Balears, Spain Jordi Lleonart Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Jorge M. Lobo Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pablo J. López–González Univ de Sevilla, Sevilla, Spain Juan José Negro Estación Biológica de Doñana–CSIC, Sevilla, Spain Vicente M. Ortuño Univ. de Alcalá de Henares, Alcalá de Henares, Spain Miquel Palmer IMEDEA–CSIC, Univ. de les Illes Balears, Spain Montserrat Ramón Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Ignacio Ribera Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pedro Rincón Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Alfredo Salvador Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Ciències Naturals de Barcelona, Barcelona, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana–CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle–CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Jersey, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana–CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Barcelona, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 31.1, 2008 © 2008 Museu de Ciències Naturals, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Romargraf S. A. ISSN: 1578–665X Dipòsit legal: B–16.278–58 The journal is freely available online at: http://www.bcn.cat/ABC

Animal Biodiversity and Conservation 31.1 (2008)

Topological properties in the spatial distribution of amphibians in Alabama USA for the use of large scale conservation X. Chen

Chen, X., 2008. Topological properties in the spatial distribution of amphibians in Alabama USA for the use of large scale conservation. Animal Biodiversity and Conservation, 31.1: 1–13. Abstract Topological properties in the spatial distribution of amphibians in Alabama USA for the use of large scale conservation.— Large–scale biodiversity conservation is urgently needed due to increasing habitat loss and fragmentation. Understanding topological perspectives of species’ distribution patterns can provide useful information for linking conservation studies at larger scales. We studied topological properties of localities in Alabama where 60 species of 12 families of amphibians were present. Analysis included a clustering coefficient which measures the strength of a population group, the relationship between occurrence localities and species number, the fractal dimension of occurrence localities (which emphasizes spatial irregularity), and distance to nearest–neighbor. The results indicate that the clustering coefficients of most amphibian species were low, but were higher for species with few occurrence localities, such as Rana sylvatica and Limnaoedus ocularis. The general relationship between species number and occurrence localities was that the majority of species held few localities in their distribution, while the remaining species occupied a greater number of localities. The fractal dimension (FD) for all amphibian localities was about 1.58, although FD was low for most individual species. We identified four relationships in the distribution of distance to nearest–neighbor: linear, logarithmic, power and polynomial. These topological properties may indicate intrinsic features about amphibians in Alabama and provide useful information for regional planning. Enhancing landscape linkages across a large area using undisturbed areas, such as 300–500 km in diameter may be a good approach to conservation practice in this region. Steps needed for biodiversity conservation planning in Alabama include creating or conserving small habitats across agricultural and urban land, and maintaining suitable spatial complexity and distance to nearest neighbors. Key words: Amphibians, Clustering coefficient, Distance to nearest–neighbor, Fractal dimension, Topology. Resumen Características topológicas de la distribución de anfibios en Alabama, EUA, para su conservación a gran escala.— La conservación a gran escala de la biodiversidad es una necesidad urgente debido a la pérdida y fragmentación de los hábitats. La comprensión de las perspectivas topológicas de los patrones de distribución de una especie, puede proporcionarnos una información de gran utilidad para vincular los estudios conservacionistas a escalas mayores. Se han estudiado las propiedades topológicas de ciertas localidades de Alabama en las que estaban presentes 60 especies de 12 familias de anfibios. Los análisis incluyen un coeficiente de agrupamiento, que mide el número de individuos de un grupo de población, la relación entre las localidades en que se encuentran los anfibios y el número de especies, la dimensión fractal de dichas localidades (que pone su énfasis en la irregularidad espacial), y la distancia a la vecina más próxima. Los resultados indican que los coeficientes de agrupamiento de la mayoría de especies de anfibios son bajos, pero eran mayores en las especies que se hallaban en pocas localidades, tales como Rana sylvatica y Limnaoedus ocularis. La relación general entre el número de especies y las localidades en que se hallaban indicó que la mayoría de las especies contaban con unas pocas localidades en su distribución, mientras que el resto ocupaban un número mayor de localidades. La dimensión fractal (FD) de todas las localidades con anfibios fue aproximadamente de 1,85, aunque la FD era baja para la mayoría de las especies individuales. Se identificaron cuatro relaciones en la distribución de la distancia a la vecina más ISSN: 1578–665X

Chen

cercana: lineal, logarítmica, potencial y polinómica. Estas propiedades topológicas pueden indicar características intrínsecas de los anfibios que habitan en Alabama, y proporcionar una información útil para la planificación regional. Un buen enfoque para la práctica conservacionista en esta región sería estimular la vinculación geográfica para formar una gran área, utilizando zonas no perturbadas, de p. ej. de 300– 500 km de diámetro. Los pasos necesarios para la planificación de la conservación de la biodiversidad en Alabama incluyen la creación o conservación de pequeños hábitats a lo largo de los terrenos urbanos y dedicados a la agricultura, así como mantener la complejidad espacial adecuada y la distancia a las localidades vecinas más cercanas. Palabras clave: Anfibios, Coeficiente de agrupamiento, Distancia al vecino más cercano, Dimensión fractal, Topología. (Received: 24 IV 07; Conditional acceptance: 17 VII 07; Final acceptance: 28 VIII 07) Xiongwen Chen, Center for Forestry, Ecology & Wildlife, P. O. Box 1927, Alabama A. & M. University, Normal, AL 35762, U.S.A. E–mail: xiongwen.chen@aamu.edu

Animal Biodiversity and Conservation 31.1 (2008)

Introduction Biodiversity conservation is experiencing a paradigm shift (Boersma, 1997) from the original consideration of single species at small scales to multiple species at larger scales (Chen et al., 2005) in response to increased species loss under the increasing pressure of urbanization, land use change, and invasive species. Noss (2002) indicated that management actions undertaken at a local scale to increase biodiversity might have an opposite effect on a large scale. Every local area is only a piece of a bigger ecological puzzle, and its importance can be understood only in relation to a larger whole, such as population or species’ source–sink dynamics’ role in species conservation within a landscape context. It is important for conservationists to expand their thinking to larger scales as a whole in which these species are embedded (Noss & Harris, 1986). Also, some properties of complexity can only emerge at a large scale (Green et al., 2006). The survival of complex systems depends largely on their topological structure (Albert et al., 2000; Newman, 2003), that is, the configuration of these species and locality in terms of the layout (such as ring and tree topology). For example, there are some general rules governing circulatory systems or the drainage networks of watersheds. Understanding the topological perspective of ecological patterns and possible underlying processes could provide a formal structure for linking studies at local scales to larger ones (Thompson et al., 2001). A change in an ecologist’s typical thinking about ecosystems and landscapes is required in order to focus on the topological perspective. There has recently been much renewed interest in topological analysis of food webs in ecological research (Williams & Martinez, 2000; Solé & Montoya, 2001; Camacho et al., 2002). Major issues concern how individuals (or species) are connected to others through the network or which individuals exert the most influence. Many natural systems can be represented by networks, and topological analysis can illustrate system properties using the number and distribution of nodes, or connections in an integrated network. Ricotta et al. (2001) aggregated cells of numerical surface variables into hierarchically–related topological entities to characterize the spatial structure of plant species richness across the city of Rome in Italy. Network analysis has shown that the sensitivity of a network to node loss depends on the frequency distribution of connections among nodes (Albert et al., 2000). Rhodes et al. (2006) applied network analysis to the conservation of habitat trees in the urban environment of Brisbane, Australia. Chen et al. (2006c) studied tolerance of potential habitat loss within a reserve network system in southern California and found that the current network of habitats for species group (plants, reptiles, mammals, birds, and overall species) had low tolerance for further habitat loss. Therefore, a topological approach, modified to incorporate basic biological realism, may

provide a framework for understanding ecological properties resulting from patterns of species distributions. The amphibians of Alabama are used here to characterize topological properties as they are highly diverse in this state due to its particular geography and climate (Mount, 1975). In recent decades, however, a global decline in amphibian species and populations has been reported (e.g., Gibbons et al., 2000; Gardner, 2001). Amphibians play an important role in both aquatic and terrestrial ecosystems, such as an energetic link between trophic levels (Pough, 1980; Whiles et al., 2006). Holomuzki et al. (1994) and Wissinger et al. (1999) indicated that amphibians may have a strong impact on ecosystem structure because they are keystone species in some habitats. Many causal factors have been considered in the world–wide decline of amphibians. These include physical habitat modification and habitat loss (Sjogren, 1991; Alford & Richards, 1999; Chen et al., 2006a), ultraviolet radiation (e.g., Blaustein et al., 1994), chemical pollutions (e.g., Beebee et al., 1990), diseases (Laurance et al., 1996), and climate change (Pounds & Crump, 1994; Chen et al., 2006b). With the global decline of biodiversity and possible complexity of underlying mechanisms, the previous reductionist approach, which concerns detailed information on a single species at a small scale, may not be sufficient to provide a general picture about all amphibians and regional conservation strategies (Smallwood et al., 1998; Chase et al., 2000; Chen et al., 2005). New ideas and approaches are needed to further our understanding of biodiversity patterns and structure and also to effectively conduct conservation programs on a large scale so that Alabama can maintains its high diversity of amphibians during its economical development. This approach could also be used for large–scale animal conservation in other regions. The goal of this study was to analyze topological properties in the spatial distribution of amphibians in Alabama, USA to obtain inference for large scale conservation efforts. Metrics were applied to describe amphibians’ topological structure, and topological characteristics were compared for each species and family. The implications for large scale conservation based on topological characteristics are discussed. Material and methods Study area The study area covers the entire state of Alabama (fig. 1), which is located between the southern foothills of the Appalachian Mountain Range and the Gulf of Mexico (between 31° and 35° N latitude) and includes a total of 67 counties. Alabama has a warm, humid, subtropical climate. Summers are hot and humid with temperatures around 33°C. Late summer and fall are usually the driest time of the year. Winters are typified by a series of cold fronts. Regional rainfall varies from 1,500 mm to

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1,620 mm in the north and from 1,800 mm to 1,950 mm along the coast (Carter & Carter, 1984). Due to a combination of all these factors, especially the mild and humid climate, remarkable surface drainage and diverse physiographic subdivisions, the amphibians of Alabama have reached a high level of diversity (Mount, 1975). They are therefore an important consideration for conservation in the USA.

directed edge is not distinguished. Besides, the different lengths of direct edges could change the clustering even with the same structure. Albert et al. (1999) used the diameter to characterize the whole network, but networks with the same diameter may also display different structures. Here we used the following equation to estimate clustering coefficient (CC) for each species and family

Amphibian dataset

The dataset for amphibians in Alabama is from the book "The Reptiles and Amphibians of Alabama" (Mount, 1975), which included thousands of locality records (hereafter referred to as localities) of 60 species in 12 families examined by its author and from the literature. All these records were digitized using ArcGIS 9 (ESRI, Redland, California). This dataset may not represent all species within the state or the current distribution of species, but it represents data from all records that were available in the 1970s. The data reflect the period prior to the most recent major growth in suburban development, and therefore provide a bench mark for topological properties of amphibians in Alabama. The names of all species are listed in table 1. Metrics of topological properties Many metrics are available to characterize topological properties in physics. However, to efficiently monitor status and trends of biodiversity, it is necessary to identify indicators that can be applied to various landscape types but with reasonable costs. Indices selected for this study took biological meaning, available data and possible applications for large scale conservation into account. Clustering coefficient The clustering coefficient is important to quantify the hierarchical structure of a network (Ravasz & Barabasi, 2003). Some methods for estimating cluster (e.g., K function), emphasize local scales and ignore properties at large scales. Watts & Strogatz (1998) introduced the clustering coefficient graph measure. The clustering coefficient ci for each vertex i of the network (here referring to distribution of species occurred locations) as ei ci = di (di – 1) where di is the number of the different nearest neighbors of vertex i (with di g 0,1) and ei is the number of directed edges that connect those nearest neighbors. This formula is a generalization for undirected network. The clustering coefficient for the whole system is the average of the clustering coefficients for all vertexes (Watts & Strogatz, 1998). However as ei is the number of directed edges that connect those nearest neighbors, the length of

CCi = Di where Di is the minimum diameter (km) of a circle to cover all localities of a species or family. This index can describe (i) the extent of the species’ clustering; and (ii) the coefficient which can be used to compare clustering with other species. Statistical distribution of occurrence localities of species Based on the distribution for each species, the occurrence localities were classified as 0–10, 10– 20, 20–30, and so on, up to 130–140. The number of species in each group of localities was counted. The midpoint in each group of localities was used for the subsequent calculation and plotting, i.e. 5 was used to represent the group 0–10 and 15 for the group 10–20. Networks with power–law degree distribution, sometimes also referred to as scale– free networks, have been the focus of much attention in the literature (e.g., Strogatz, 2001). Power–laws can be generated from the study of a species’ exponential growth, exponential decay and highly optimized tolerance (Brookings et al., 2005). In scale–free networks, some nodes act as highly connected hubs (high degree), while most nodes are of low degree. Scale–free network structure and dynamics are independent of the system’s size (N) and the number of nodes the system has. In other words, a network that is scale–free will have the same properties no matter how many nodes it has (e.g., Albert & Barabási, 2000). Fractal dimension of occurrence localities The notion of dimension is also called topological dimension. The fractal dimension of localities can be used for measuring spatial complexity of biodiversity distributions or the degree of occupation of the physical space by a contorted or fragmented surface (Mandelbrot, 1977; Frontier, 1987). Here, the fractal dimension of localities for species in each family was determined by the box–counting method, using box lengths of 50, 25 and 10 km, respectively. The fractal dimension (D) was determined by the formula: N( ) D = lim log10 (1/ ) where

is the box length, and N( ) is the number of

Animal Biodiversity and Conservation 31.1 (2008)

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boxes with the length of that covered the occurrence localities (e.g., Jumarie, 2000; Li, 2000). Amphiumidae and Cryptobranchidae are not included in this analysis as they were found in few localities. A species (or family) with a high fractal dimension has high complexity in its spatial distribution.

Distance to nearestโ neighbor The distance to nearestโ neighbor is important for species interpopulation migrations, such as for "rescue effect", because immigrants have a higher probability of entering a cluster with a high connectivity and therefore preventing a population from

Chen

Table 1. Amphibian species, families and their identification numbers included in this study (source from Mount, 1975): FN. Family number; SN. Species number. Tabla 1. Especies y familias de anfibios, y los números de identificación que se usaron en este estudio (procedencia: Mount, 1975): FN. Número de la familia; SN: Número de la especie.

Family FN

Family Species name

Bufonidae 1

Species name

Amphiumidae

Bufo americanus americanus

Bufo quercicus

Bufo terrestris

Cryptobranchidae

Bufo woodhousei fowleri

Hylidae 2

FN 7

Amphiuma means

Amphiuma tridactylum

Cryptobranchus alleganiensis

Plethodontidae

Acris crepitans crepitans

6 7

Aneides aeneus

Acris gryllus

Desmognathus aeneus

Hyla avivoca

Desmognathus fuscus

Hyla cinerea

Desmognathus monticola

Hyla crucifer

Desmognathus ochrophaeus

Hyla femoralis

Eurycea bislineata

Hyla gratiosa

Eurycea longicauda

Hyla squirella

Eurycea lucifuga

Hyla versicolor

Gyrinophilus palleucus

Limnaoedus ocularis

Gyrinophilus porphyriticus

Pseudacris brachyphona

Hemidactylium scutatum

Pseudacris nigrita nigrita

Manculus quadridigitatus

Pseudacris ornate

Phaeognathus hubrichti

Pseudacris triseriata

Plethodon cinereus polycentratus

Microhylidae

Plethodon dorsalis dorsalis

Plethodon glutinosus

Pseudotriton montanus flavissimus

Pseudotriton rubber

Gastrophryne carolinensis

Pelobatidae 4

Scaphiopus holbrooki holbrooki

Ranidae 5

Proteidae

Rana areolata sevosa

Rana catesbeiana

Rana clamitans

Salamandridae

Rana grylio

Rana heckscheri

Sirenidae

Rana palustris

Rana pipiens sphenocephala

Rana sylvatica

Ambystomatidae 6

Ambystoma cingulatum

Ambystoma maculatum

Ambystoma opacum

Ambystoma talpoideum

Ambystoma texanum

Ambystoma tigrinum tigrinum

Necturus maculosus

Necturus beyeri

Notopthalmus viridescens

Siren intermedia

Siren lacertian

Animal Biodiversity and Conservation 31.1 (2008)

150 Clustering coefficient (*1,000 unit)

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Clustering coefficient (*1,000 unit)

0 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40 42 44 46 48 50 52 54 56 58 60 Species ID 7 6

5 4 3 2 1 0

R Amb Amp Family names

Fig. 2. The clustering coefficients of amphibian species (A) and families (B). Species and family names are listed in table 1. Most species and families have low clustering coefficients. Abbreviations: B. Bufonidae; H. Hylidae; M. Microhylidae; P. Pelobatidae; R. Randiae; Amb. Ambystomatidae; Amp. Amphiumidae; C. Cryptobranchidae; Pl. Plethodontidae; Pr. Proteidae; Sl. Salamandridae; Sr. Sirens. Fig. 2. Coeficientes de agrupamiento de las especies de anfibios (A) y de las familias (B). Los nombres de dichas especies y familias se hallan en la tabla 1. La mayoría de las especies y las familias tienen coeficientes de agrupamiento bajos. (Para las abreviaturas de las familias, ver arriba.)

extinction (Brown & Kodric–Brown, 1977). We used two methods to evaluate the distance to nearest– neighbor. The first approach was to estimate the average distance to nearest–neighbor for each family by measuring the nearest distance between the species’ localities. The second way was to examine the distribution of distances to nearest–neighbors

for each species. The distances were classified into 25 classes (< 10, < 15, < 20,…, < 125, and < 130 km), and the total distance to nearest– neighbor in each class was calculated for each species. Due to their limited localities, 10 species (No. 14, 25, 28, 29, 35, 36, 39, 50, 51 and 60 listed in table 1) were not included in this analysis. Differ-

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Number of species

14 12 y = –3.9354 Ln(x) + 19.68 R2 = 0.8567 p < 0.01

10 8 6 4 2 0 0

60 80 100 Number of occurred locations

120

140

160

Fig. 3. The logarithmic relationship between the locality records and species number. Fig. 3. Relación logarítmica entre la presencia y el número de especies en las distintas localidades.

ent species may have different distributions of distance to nearest–neighbor. For example, a linear relationship could mean there is even distribution of the distance to nearest–neighbor. A logarithmic relationship would mean that there are more long distances to nearest–neighbor than short ones, or oppositely, a power relationship would indicate that there are more short distances to nearest–neighbor than long ones. Polynomial relationships include a mixture of all the above types as they may occur in a combination across a different scale of distances. Results Clustering coefficient The clustering coefficients for most amphibian species were below 10 (fig. 2A), but both Ranta sylvatica (No. 28) and Limnaoedus ocularis (No. 14) had clustering coefficients of more than 100, because they had only two localities. At the family level, the clustering coefficients were below 3 for most families (fig. 2B), but the clustering coefficient of the family of Cryptobranchidae (giant salamanders) was above 6.

Fractal dimension of locality records Families Hylidae, Plethodontidae, and overall amphibian families had a fractal dimension of over 1.0 (fig. 4). Families Pelobatidae, Proteidae, Salamandridae and Sirens had fractal dimensions less than 0.4. The fractal dimension (FD) for all amphibian localities was about 1.58, while for most species FD values were lower than this. Distances to nearest–neighbor The average distance to nearest–neighbor was more than 50 km for families Ambystomatidae and Sirens (fig. 5), but was less than 30 km for families Bufonidae, Microhylidae, Cryptobranchidae and Plethodontidae. Based on the distribution of distances to nearest–neighbor, there were four types of relationships: linear, logarithmic, power and polynomial (fig. 6; table 2). Species from the families Microhylidae, Salamandridae, and Sirens showed linear relationships, while single species from the family Cryptobranchidae showed a polynomial relationship. Discussion

Statistical distribution of occurrence localities A relationship was found between the number of localities and species’ richness (fig. 3). Only a limited number of species (three) had more than 100 locality records, while most species had less than 20 occurrence localities.

Spatial clustering is often observed in nature due to a combination of ecological processes including limits to dispersal imposed by landscape structure, disturbance, and heterogeneity of the abiotic environment (Coomes et al., 1999). There are several ways to characterize spatial clustering. Chen et al.

Animal Biodiversity and Conservation 31.1 (2008)

1.8 Fractal dimension

1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0

R Amb Amp Family names

overall

Fig. 4. Fractal dimensions of locality records for 12 amphibian families based on box accounting method. (For the abbreviations of families, see fig. 2.) Fig. 4. Dimensiones fractales de la presencia en las localidades para 12 familias de anfibios, basadas en el método de contabilización de cajas. (Para las abreviaturas de las familias, ver fig. 2.)

Average distance to nearest neighbor (km)

80 70 60 50 40 30 20 10 0

R Amb Amp Family names

Fig. 5. The average distance of nearest–neighbor for each family based on locality records. (For the abbreviations of families, see fig. 2.) Fig. 5. Distancia promedio al vecino más próximo para cada familia, basándose en la presencia en las localidades. (Para las abreviaturas de las familias, ver fig. 2.)

(2005) applied an aggregation index to measure the spatial scale of localities for different species groups. However, the scale identified by an aggregation index is a local scale and may be misleading under increasing habitat loss and fragmentation.

From the perspective of large–scale conservation, more attention should be focused on the extent of clustering, such as size of cluster area for a given species including all its sub–populations. Clustering coefficients should also be included so that patterns

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Percentage

logarithmic linear power polynomial

Distance to nearest neighbor Fig. 6. The possible four conceptual models for Alabama amphibians in the distribution of distance to nearest–neighbor. Fig. 6. Los cuatro posibles modelos conceptuales para los anfibios de Alabama, en la distribución de la distancia al vecino más cercano.

can be compared. For further clarification, the magnitude of clustering coefficients (high, medium, or low) for species is generally distinguished as having a narrow, flexible or broad distribution, respectively. In the present study, three species (Limnaoedus ocularis, Ranta sylvatica, and Phaeognathus hubrichti) and one family (Cryptobranchidae) of amphibians showed relatively high clustering coefficients due to their limited distribution. This also indicates that they were rare from a spatial perspective, even though their population might not be low (currently all three species are protected in Alabama). Condit et al. (2000) indicated that the rare tree species tend to be more aggregated than abundant species. Most amphibian species had low clustering coefficients in this study, meaning they were broadly distributed. Although the distribution centers may differ between species, the average diameter of their distribution was around 380 km. When a sub–population decreases dramatically at one location, the "rescue effect" n depends on the immigration from neighboring sub–populations. If all recorded locations of a species are considered to work as nodes (Bunn et al., 2000), it is important to maintain the integrity of these networks for amphibian conservation at a large scale in view of current rates of habitat loss and fragmentation. Most species in the study had a low number of occurrence localities, consistent with the pattern reported by Chen et al. (2006c) in a previous study. However, in the present study, the relationship between locality number and species number can be described using a logarithm. Although a weak power–law relationship also fits the data, it may underestimate the relationship in this study. This

means that the relationships of locality number and species number may be derived from the available data set and results may differ from a theoretical approach. This pattern indicates that in order to preserve a greater number of species, some key locations shared by most species need to be preserved with priority if the entire area can not be preserved. By using this algorithm it is also possible to estimate the number of rare amphibian species based on their occurrence localities. There is self–similarity in the distribution of amphibians in Alabama. Generally, the high fractal dimension indicates the high spatial complexity in the species distribution pattern. The overall fractal dimension of localities of all families was about 1.58, and the minimum fractal dimension was only 0.17 for the family of Sirenidae. The self–similarity of amphibian families may be due to the self– similarity in natural resources, such as vegetation and wetland landscapes. Burrough (1981) reported that many landscape features, such as vegetation, have fractal structure. Ostling et al. (2000) indicated that clustering distribution is consistent with self–similar distribution. We found that families with relatively lower fractal dimensions, such as Pelobatidae and Sirens, usually have relatively higher clustering coefficients, (figs. 2B, 4). Mandelbrot (1977) indicated that as fractal dimension decreases, clusters of visited points (here localities) become increasingly packed. Maintaining proper spatial complexity (part of spatial integrity), such as for habitats, vegetation and other environmental factors, is considered to be beneficial for species survival. This should be taken into account in strategy–making concerning land–use changes, preservation, construction and urban development.

Animal Biodiversity and Conservation 31.1 (2008)

Table 2. The species ID and family names in the four distribution types of distance to nearestneighbor (source from Mount, 1975): *Family only listed in this type of distribution. Tabla 2. Número de identificación de las especies y familia a la que pertenecen, distribuidas en los cuatro tipos de distancia al vecino más cercano (procedencia: Mount, 1975): * Familia que sólo se halla en ese tipo de distribución.

Relationship

Species

Family*

Linear

1, 2, 3, 10, 11, 13, 19, 21, 32, 38, 47, 49, 58, 59

Bufonidae, Hylidae, Microhylidae*, Ranidae, Ambystomatidae, Plethodontidae, Salamandridae*, Sirens*

Logarithmic

4, 5, 6, 7, 8, 18, 22, 23, 24, 25, 26, 31, 40, 41, 43, 44, 45, 48, 52, 53, 55

Bufonidae, Hylidae, Randidae, Ambystomatidae, Plethodontidae

Power

9, 12, 15, 16, 17, 20, 27, 33, 34, 54, 57

Hylidae, Pelobatidae, Randidae, Ambystomatidae, Plethodontidae, Proteidae

Polynomial

35, 36, 37, 42, 46, 56

Ambystomatidae, Cryptobranchidae*, Plethodontidae, Proteidae

Spatial complexity in landscape or species distribution may also decrease spatial synchrony, and this could contribute to species extinction (e.g. Chen et al., 2006b). The distance to nearest–neighbor is important for amphibians to maintain populations across space. The richness of amphibian species decreases significantly with increasing distance to nearest intermittent or permanent wetlands (Schurbon & Fauth, 2003). Evidence suggests that several amphibian species have difficulty dispersing more than a few hundred meters from their natal ponds (Semlitsch, 1998; 2000; Fauth, 1999). Based on the statistical distribution of distances to nearest– neighbor, we found at least four types of relationships in amphibians of Alabama. Distance to a neighbor (or a potential source for new colonizers) is critical for "rescue effect" or dispersal success (Foppen et al., 2000). Based on this, we may infer that species with a logarithmic distribution of distance to nearest–neighbor may have strong dispersal abilities and these species may re–colonize after local disturbances, such as local extinction. Alternatively, these local populations may be more stable because of quick re–colonization. On the other hand, species with power and linear relationships may not have strong dispersal ability and may be more sensitive to local disturbances. Species with a polynomial relationship may be more stable after local disturbances, because they have varied dispersal abilities. Hubbell (2001) indicated that weak dispersers are generally good competitors and often dominate the communities they colonize. This was partially supported in our study given that species with power relationships in the distance to nearest–neighbor usually had low clustering coefficients.

General implications for amphibian conservation at a large scale The topological characteristics of animal species have not been used previously to address problems in the conservation of biodiversity at large scales. The above topological properties reveal some intrinsic features about amphibians in Alabama and also provide useful information for regional planning. The clustering coefficient may indicate that in order to conduct large scale conservation of amphibians, the intensive agricultural activities and urban growth in the entire region should be taken into consideration. Alabama has a long history of farming practices, such as cotton and cattle. Maintaining large and adequately connected (both physically and functionally) habitats for amphibians is a big challenge. If clustering of amphibians is taken into consideration, it is clear that it is necessary to maintain and preserve habitats across a large area, such as 300–500 km (the diameter of species networks). The current Alabama Natural Heritage Program (http://www.alnhp.org/) may help to promote public concern for large scale conservation in biodiversity. Landscape linkages should be enhanced through the development of formal policies (Semlitsch, 2002). For successful conservation at a large scale all occurrence localities should be taken as nodes of amphibian networks. The linkages (both long and short) which can promote regional connectivity should be conducted to different nodes (locations) for species movement along corridors (Bunn et al., 2000). Even small and seemingly unimportant landscape elements can contribute as high quality patches or functionas linkage. Creating or conserving small elements across agricultural and urban lands and maintaining suitable spatial

complexity should be considered when such patches may enlarge the source areas or act as stepping– stones for species. Maintaining proper neighbor habitats (or nodes) for sub–populations is necessary for species "sink–source" dynamic processes and also for maintaining spatial complexity. The four types of relationships (linear, power, logarithmic and polynomial) in the distribution of distances from nearest–neighbor may provide new understanding of the species distribution patterns, tolerance to habitat loss, and dispersal (or competition) ability. Forestry and agricultural management practices, the mainstay of human acitivityin Alabama, should include a mixture of strategies for large scale conservation (Dobson, 2001), such as land planning and zoning for logging and prescribed burning or intensive agricultural development. The adoption of a topological approach would provide a hierarchical understanding of the complicated ecological distribution of biodiversity, allowing highly efficient use of management resources and improving outcome for biodiversity conservation at large scales. Acknowledgements This study was partially supported by the School of Agricultural and Environmental Sciences and COE of Alabama A & M University and Dept. of Energy DE–FC26–06NT43029. Special thanks to Dr. Z. Felix and Ms. K. A. Roberts for editorial work. References Albert, R. & Barabasi, A.–L., 2000. Topology of evolving networks: local events and universality. Physical Review Letters, 85: 5234–5237. Albert, R., Jeong, H., Barabási, A.–L., 1999. Diameter of the world–wide web. Nature, 401: 130–131. – 2000. Error and attack tolerance of complex networks. Nature, 406: 378–382. Alford, R. A. & Richards, S. J., 1999. Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics, 30: 133–165. Beebee, T. J. C., Flower, R. J., Stevenson, A. L., Patrick, S. T. & Appleby, P. C., 1990. Decline of the Natterjack Toad (Bufo calamita) in Britain. Paleological evidence for breeding site acidification. Biological Conservation, 53: 1–20. Blaustein, A. R., Hoffman, D. D., Hokit, D. G., Kiesecker, J. M., Walls, S. C. & Hayes, J. B., 1994. DNA repair and resistance to solar UV–B in amphibian eggs: a link to population declines. Proceeding of National Academy of Science of USA, 91: 1791–1795. Boersma, P. D., 1997. Conservation Biology: a paradigm shift. Newsletter of Society for Conservational Biology, 11: 1. Brookings, T., Carlson, J. M. & Doyle, J., 2005. Three mechanisms for power laws on the Cayley

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"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 24.1, 2001 © 2001 Museu de Zoologia, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Sociedad Cooperativa Librería General ISSN: 1578–665X Dipòsit legal: B–16.278–58

Animal Biodiversity and Conservation 31.1 (2008)

Two new Bryconamericus: B. cinarucoense n. sp. and B. singularis n. sp. (Characiformes, Characidae) from the Cinaruco River, Orinoco Basin, with keys to all Venezuelan species

C. Román–Valencia, D. C. Taphorn B. & R. I. Ruiz–C.

Román–Valencia, C., Taphorn B., D. C. & Ruiz–C., R. I., 2008. Two new Bryconamericus: B. cinarucoense n. sp. and B. singularis n. sp. (Characiformes, Characidae) from the Cinaruco River, Orinoco Basin, with keys to all Venezuelan species. Animal Biodiversity and Conservation, 31.1: 15–27. Abstract Two new Bryconamericus: B. cinarucoense n. sp. and B. singularis n. sp. (Characiformes, Characidae) from the Cinaruco River, Orinoco Basin, with keys to all Venezuelan species.— Here we describe for the first time Bryconamericus cinarucoense n. sp. and Bryconamericus singularis n. sp., two new species of Characiformes from the Cinaruco River, Orinoco Basin in Venezuela. B. cinarucoense n. sp. is distinguished from all other species of the genus in having: upper jaw extending beyond lower, maxilla short with only one or two teeth, cartilaginous rhinosphenoid extending to anterior part of prevomer, pelvic bone with cartilage along anterior edge, lateral line pores in straight line. B. singularis n. sp. is distinguished from congeners by having top of head flat, dentary with six or seven small unicuspid teeth, a dark lateral band extending from posterior edge of humeral spot to midbase of caudal fin which widens behind dorsal–fin origin, and in having five supraneurals which lack cartilage on the upper and lower extremities. Keys to aid identification of all known Venezuela species are included. Bryconamericus motatanensis is placed in the synonymy of B. alpha. Previous reports of B. breviceps and B. heteresthes from Venezuela are misidentifications, and are here considered as either B. cinarucoense n. sp., or another as yet undescribed species. Key words: B. cinarucoense n. sp., B. singularis n. sp., Tropical fish, Taxonomy, Osteology, Teeth. Resumen Dos nuevos Bryconamericus: B. cinarucoense sp. n. y B. singularis sp. n. (Characiformes, Characidae) del río Cinaruco, cuenca del Orinoco, con claves para todas las especies de Venezuela.— Se describen dos especies nuevas de Bryconamericus de la cuenca del Orinoco en Venezuela: Bryconamericus cinarucoense sp. n. y B. singularis sp. n. (Characiformes, Characidae). B. cinarucoense sp. n. se distingue de sus congéneres por presentar la mandíbula superior sobresaliente, la maxila corta y con uno o dos dientes, el rinoesfenoides cartilaginoso se extiende hacia la parte anterior del prevomer, el hueso pélvico con cartílago a lo largo de su margen anterior, y por presentar los poros de la línea lateral en línea recta. B. singularis sp. n. se diferencia de las demás especies por presentar el extremo de la cabeza aplanado, seis o siete pequeños dientes unicúspides en el dentario y una banda lateral oscura que se extiende desde el extremo posterior de la mancha humeral hasta la base media de la aleta caudal que se ensancha en su parte posterior detrás del nivel del origen de la aleta dorsal, y por presentar cinco supraneurales sin cartílago en sus extremos superior e inferior. Se incluyen claves para la determinación de las especies conocidas de Bryconamericus en Venezuela. Bryconamericus motatanensis se ubica como sinónimo de B. alpha. Citas previas de B. breviceps y B. heteresthes de Venezuela son identificaciones erróneas, y aquí se considera como B. cinarucoense, u otra especie aún no descrita. Palabras claves: B. cinarucoense sp. n., B. singularis sp. n., Pez tropical, Taxonomìa, Osteología, Dientes.

ISSN: 1578–665X

Román–Valencia et al.

(Received: 18 VI 07; Conditional acceptance: 27 VIII 07; Final acceptance: 7 IX 07) César Román–Valencia & Raquel I. Ruiz–C., Lab. de Ictiología, Univ. del Quindío, A. A. 2639, Armenia, Quindío, Colombia.– Donald C. Taphorn B, UNELLEZ, BioCentro, Colección de Peces, Museo de Zoología, Guanare, Portuguesa, 3310, Venezuela. Corresponding autor: C. Román–Valencia. E–mail: ceroman@uniquindio.edu.co

Animal Biodiversity and Conservation 31.1 (2008)

Introduction Species of the genus Bryconamericus Eigenmann (including Knodus Eigenmann) are predominantly small to medium–sized (usually 30–50 mm maximum SL), silvery fishes with a humeral spot and a dark lateral body stripe, silvery in life, that often extends onto the middle caudal rays (Géry, 1977; Román–Valencia, 2002a, 2002b, 2003a, 2003b). Bryconamericus is complex genus of the family Characidae, with about fifty described species (Lima et al., 2003) widely distributed in a variety of freshwater ecosystems in both the lowlands and highlands of South and Middle America (Vari & Siebert, 1990; Jiménez et al., 1998; Román–Valencia, 2001, 2002a, 2002b, 2003a, 2003b, 2003c, 2003d, 2005). Species of the genus are abundant in small brooks as well as along the banks of larger rivers, with high concentrations of dissolved oxygen (ca. 8 mg/l) and almost neutral pH (Jiménez et al., 1998; Román– Valencia, 1998, 2000, 2002a; Román–Valencia & Muñoz, 2001). Bryconamericus species are known from all major drainages in Venezuela (Román– Valencia, 2003a) but have frequently been misidentified. In recent studies by Lima & Zuanon (2004), Weitzman et al. (2005), Ferreira & Lima (2006), and Ferreira & Carvajal (2007), the genus Knodus was considered valid, although this was mainly for convenience and based on the character of a scaled caudal fin. However, there are no characters that would allow us to confidently separate Bryconamericus from Knodus; as pointed out by Román–Valencia (2000, 2003a, 2005). In one key to Characidae, Planquette et al. (1996) attempt to differentiate Bryconamericus and Knodus from Hemibrycon by its fewer than six teeth on the maxilla; they furthermore state that the only difference between Bryconamericus and Knodus is the presence of scales on the caudal fin in the latter. There seems to be a consensus that the genus Bryconamericus, as currently defined, is not monophyletic (Vari & Siebert, 1990; Malabarba & Malabarba, 1994; Silva & Malabarba, 1996; Malabarba & Weitzman, 2003; Silva, 2004). However, there is still no published evidence that might indicate that some groups of Bryconamericus species are more closely related to any other taxa (Vari & Sieber, 1990; Malabarba & Kindel, 1995), nor proposals of any new phylogenies. The difficulty in diagnosing Bryconamericus and related genera was evident when Malabarba & Malabarba (1994) described Hypobrycon maromba, but commented that it might be better to locate it in Bryconamericus. Serra & Langeani (2006) redescribed the type species of Bryconamericus (= B. exodon) and augmented the number of characters available for its diagnosis, but commented that many of them may not represent characters uniquely defining Bryconamericus. Malabarba y Weitzman (2003) presented a hypothesis, placing Bryconamericus as a member of a clade named "Clade A", supported by two synapomorphies: four teeth in the innter premaxillary row, and ii,8 dorsal–fin rays. Using molecular characters

Calcagnotto et al. (2005: fig. 6) found further support for the monophyly of Bryconamericus and indicate that Knodus is its sister taxon, and that both are closely related to Creagrutus and Hemibrycon. Also using molecular characters, Romàn–Valencia & Vanegas–Ríos (in press) recently proposed that the genus Bryconamericus is a monophyletic group, at least for the species from Central America. This was also proposed by Fink (1976). Furthermore, both groups (Fink, 1976; Román–Valencia & Vanegas– Ríos, in press) present evidence that indicates the diversification of Bryconamericus in Central America can be explained by dispersion from northwestern South America. However, Lima et al. (2003) lists Bryconamericus as insertae sedis in Characidae. Taxonomically, Bryconamericus species from Central America have now been clearly resolved (Román–Valencia, 2002a), but the South American species are still poorly understood; for most countries, for example Colombia (Magdalena drainage), Peru, Ecuador (Pacifico and Amazon drainages) and Bolivia, the available keys and species descriptions are of little use to determine the nominal species reported. We consider twelve species as valid records from Venezuela in this report, including six from the Orinoco Basin. The description of two new species of Bryconamericus from the Cinaruco River in Venezuela adds to the first author's ongoing revision of the species in northern South America, and is further proof of the as–yet undocumented biodiversity of the genus. We provide keys to aid identification of all Venezuelan species for the following regions: Maracaibo Basin, Caribbean coastal drainages, Orinoco Basin, and the Rio Negro drainage in Amazonas state. Material and methods Twenty–one measurements were taken with digital calipers, recorded to hundredths of millimeters and expressed in most cases as percentages of standard or head length (table 1). Nine counts were made using a stereoscope with a dissection needle to extend the fins. Counts and measurements were taken from the left side of specimens when possible, basically following the guidelines in Vari & Siebert (1990). Observations of bones and cartilage were made on cleared and stained specimens prepared according to techniques outlined in Taylor & Van Dyke (1985) and Song & Parenti (1995). Bone nomenclature follows Weitzman (1962), Vari (1995), Ruiz–C. & Román–Valencia (2006). Specimens are deposited in the Auburn University Museum Fish Collection, Auburn, Alabama (AUM), the Museo de Biología, Instituto de Zoología Tropical, Universidad Central de Venezuela, Caracas (MBUCV), Museo de Historia Natural La Salle, Caracas (MHNLS), the Museo de Ciencias Naturales de la UNELLEZ– Guanare, Venezuela (MCNG), the Ichthyology Laboratory at the Universidad del Quindío, Armenia, Colombia (IUQ) and in the Instituto de

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Table 1. Morphometric and meristic data of Bryconamericus singularis n.sp. and B. cinarucoense. n. sp. (Standard and total length in mm, averages in parenthesis.) Tabla 1. Datos morfométricos y merísticos de Bryconamericus singularis sp. n. y B. cinarucoense. sp. n. (Longitud estándar y total en mm, medias entre paréntesis)

B. singularis

B. cinarucoense

Holotipo

Paratipos

Standard length

33.41

27.31–33.57 (30.50)

19.75–33.57 (26.81) 28.98

Paratipos

Holotipo

Total length

41.07

35.40–41.55 (38.82)

23.62–42.88 (32.96) 36.76

Body depth

19.47

19.47–25.99 (23.58)

16.97–25.94 (20.61) 19.43

Snout–dorsal fin distance

52.05

47.19–52.29 (49.71)

40.94–56.78 (50.41)

Snout–pectoral fin distance

26.58

21.99–30.07 (26.33) 19.44–29

Snout–pelvic fin distance

49.75

42.25–52.10 (47.84)

39.94–53.56 (46.75) 46.69

Dorsal–pectoral fin distance

36.55

33.78–40.62 (37.09)

29.91–40.97 (36.51) 32.15

Snout–anal fin distance

66.96

63.33–68.98 (65.65)

48.46–65.62 (59.77)

Dorsal fin–hypural distance

46.96

46.85–56.23 (51.46)

35.03–54.10 (47.85) 47.70

Dorsal–anal fin distance

27.49

21.48–37.31 (25.09)

16.54–44.70 (22.23) 19.57

Dorsal–fin length

21.88

18.66–28.38 (25.59)

14.4–26.60 (20.65)

19.60

Pectoral–fin length

19.84

17.72–28.01 (22.85)

15.63–26.0 (20.8)

23.50

Pelvic–fin length

16.55

13.85–22.56 (18.45)

10.68–20.10 (15.24) 14.84

Anal–fin length

18.26

17.45–20.18 (18.63)

13.11–21.06 (16.49) 18.77

Percentages of SL 53.00

.45 (24.76) 25.85

60.08

Caudal peduncle depth

8.8

7.88–10.55 (9.28)

6.05–9.54 (8.22)

8.45

Caudal peduncle length

10.72

8.64–16.80 (11.77)

8.3–22.81 (14.68)

14.53

Head length

21.59

21.59–27.38 (24.06)

18.77–30.85 (24.42) 23.78

Snouth length

21.63

21.63–29.52 (25.35)

18.49–34.55 (25.71) 26.27

Orbital diameter

53.09

39.59–53.09 (46.79)

35.76–54.74 (44.79) 45.28

Postorbital distance

29.17

29.17–37.50 (33.15)

27.72–49.64 (36.31) 30.19

Maxilla length

32.93

18.27–32.93 (27.30)

21.34–37.54 (29.75) 21.80

Interorbital distance

28.40

28.40–38.05 (33.87)

25.57–39.46 (32.63) 32.51

Mandible superior superior

19.87

19.87–31.06 (25.60)

19.20–30.70 (25.03) 20.14

30–32

35–37

5–6

4–5

3–4

Predorsal median scales

10–11

Dorsal–fin rays

ii,8

iii–iv,8

i–iii,7–8

iii,7

Percentages of HL

Lateral–line scales

Scale row between dorsal–fin origin and lateral line 5 Scale rows between anal–fin origin and lateral line 4 Scale rows between pelvic–fin and lateral line

Anal–fin rays

iii,17

iii,17–18

iii–iv,18–21

iii,20

Pelvic–fin rays

ii,8

ii,6

Pectoral–fin rays

ii,10

ii,10–11

ii,11

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1 cm

Fig. 1. Bryconamericus cinarucoense n. sp.: holotype, MCNG 52002, 28.98 mm SL. Fig. 1. Bryconamericus cinarucoense sp. n.: holotipo, MCNG 52002, 28,98 mm LE.

Investigaciones Biológicas "Alexander Von Humboldt", Villa de Leyva, Boyacá (IaVH). In the lists of paratypes, the number of individuals is given in parentheses immediately after the catalog number, which is followed by the range of Standard Length (SL) in mm for that lot; for example: MCNG 53000 (23 ex.) 19.34–25.44, indicates 23 individuals in lot MCNG 53000, with the smallest fish 19.34 mm SL and the largest 25.44 mm SL. All collections were made in Venezuela. If no measurements are presented, the paratypes were not measured. Comparative material (all from Venezuela) Bryconamericus alpha Eigenmann, Henn and Wilson 1914 (see Román–Valencia, 2003a) Bryconamericus breviceps Eigenmann 1908 (see Román–Valencia, 2003d) Bryconamericus heteresthes Eigenmann 1908 (see Román–Valencia, 2003a) Bryconamericus orinocoense Román–Valencia Román–Valencia 2003d Holotype: MBUCV 29464, 28.1 mm SL; Amazonas State, Río Orinoco 0.5 km upstream from Esmeraldas (aprox. 2° 53´ 06'' N, 64° 58' 06'' W); 12 III 1987. Paratypes: collected with holotype: IUQ 433 (9 ex.) MBUCV 25834 (26); MBUCV 6055 (1 ex.) Amazonas, La Esmeralda, Caño Cadabaudi, 23 XI 1969. MBUCV 19395 (3 ex.); Amazonas, Río Mavacá near base camp; MBUCV 21658 (3 ex.), Amazonas, Río Cataniapo, 10 XI 1989.

Results Bryconamericus cinarucoense n. sp. (fig. 1, table 1) Holotype: MCNG 52002, 28.98 mm SL: Venezuela, Orinoco River basin, Cinaruco River, Apure State, Pedro Camejo County, sand beach, 6º 32' 55'' N; 67º 24' 58'' O, 21 V 1999 A. Arrington, C. García.

Paratypes: all from Venezuela, Orinoco River basin, Apure State, Cinaruco River: MCNG 34679 (6 ex.), 17.44–34.26 mm SL, beach in front of Laguna Larga, Apr1997, coll. David Jepsen, Douglas Rodríguez; MCNG 34705 (31 ex.) 12.80–20.08, beach near Laguna Larga, 4 IV 97, coll. David Jepsen and Douglas Rodriguez; MCNG 39174 (2 ex.), 31.66– 33.62, beach above Laguna Larga, 11 VI 99, A. and J. Arrington; MCNG 39248 (27 ex.) 30.11–36.87, beach below Laguna Larga, 11 VI 99, coll. A. & J. Arrington; MCNG 41277 (88 ex.) 17.53–35.63, beach, 19 IV 1999, coll. A. & J. Arrington; MCNG 41292 (26 ex.) 23.27–32.64, beach, 19 VI 1999, coll. A. & J. Arrington; MCNG 41638 (247 ex.), 18.86–37.26, IUQ 526 (16 ex.), IUQ 527 (3 ex.) (C & S), 25.2–28.4 collected with holotype; MCNG 41677 (13 ex.) 18.06– 32.81, beach 7, 21 V 1999, coll. A. Arrington & C. García; MCNG 44438 (10 ex.) 30.94–36.79, beach upstream from Laguna Larga, 20 VI 2001, coll. C. Layman; MCNG 44496 (27 ex.) 29.67–35.61, beach upstream from Laguna Larga, C. Layman. Non–type material examined From Venezuela, Orinoco River basin, Apure State, Cinaruco River: MCNG 39175 (4 ex.), above Laguna Larga, 11 VI 1999, coll. A. & J. Arrington; MCNG 39221 (1 ex.), in front of Laguna Larga, 11 VI 1999, coll. A. & J. Arrington; MCNG 40549 (178 ex.), Laguna Espinar, 18 Mar 1999, coll. A. & J. Arrington; MCNG 40842 (64 ex.), Cinaruco River 24 III 1999, coll. A. & J. Arrington; MCNG 41147 (5 ex.), beach 4, 15 IV 1999, coll. A. & J. Arrington; MCNG 41575 (14 ex.), beach 2, 21 V 1999, coll. A. Arrington & C. García; MCNG 45013 (1 ex.), 17 V 1999, coll. A. Arrington & C. García; MCNG 45014 (1 ex.), downriver from Laguna Larga, 11 VI 1999, coll. A. & J. Arrington. From Guyana Essequibo River basin: AUM 38844 (54 ex.), Takuku River 3.77 km SSW Lethem Rupununi, latitude 03.35500, 1 XI 2003, coll. J. W. Armbruster et al.; AUM 39017 (34 ex.), Essequibo river at Yukanopito Falis, 44.5 km SW mouth of Kuyuwini River, latitude 01.91461, 9 XI 2003, coll. J. W. Armbruster et al.; AUM 44686 (4 ex.), Pirara

River, at Pirara Ranch, latitude 03.62517, 26 XI 2005, coll. L. S. de Souza et al.; AUM 38952 (18 ex.), Araquai Creek 77.3 km SSE Lethem Rupununi, latitude 02.76261, coll. J. W. Armbruster et al., 15 XI 2003; AUM 44948 (30 ex.), Guyana, Ireng River, 6.9 km WSW Karasabal, latitude 04.01957, 1 XI 2002, coll. J. W. Armbruster; AUM 38104 (5 ex.), Creek and Kuyuwini River 28.0 km E Kuyuwini Landing Rupununi, latitude 02.04747, 5 XI 2003, coll. J. W. Armbruster et al. Diagnosis Bryconamericus cinarucoense n. sp. is distinguished from congeners by having the upper jaw extending beyond lower, maxilla short with one or two teeth, cartilaginous rhinosphenoid extending to anterior part of prevomer, pelvic bone with cartilage along anterior edge, and lateral line pores in a straight line. It differs from B. subtilisform Román–Valencia (Román–Valencia, 2003b), the most similar Venezuelan species, in having fewer pored lateral line scales (35–37 vs. 38–39), more scales below lateral line to origin of pelvic–fin (4– 5 vs. 2–3), more branched anal–fin rays (20–21 vs. 17–18), and pelvic–fin rays usually ii,6 vs. i,7 in B. subtilisform [see also: table 1 (this paper), and table 1 (Román–Valencia, 2003b), and keys included below]. Description Body slender and elongate (mean maximum body depth about 20% SL). Area above orbits flat. Dorsal profile of head and body oblique from the supraoccipital to dorsal origin and from the last dorsal–fin ray to the base of the caudal fin. Ventral profile of body convex from the snout to the base of anal fin. Caudal peduncle laterally compressed. Head and snout short, mandibles not equal, the upper longer than the lower; mouth terminal, lips soft and flexible and not covering the outer row of premaxillary teeth; ventral border of the upper mandible straight; posterior edge of the maxilla reaching anterior edge of orbit; opening of posterior nostrils vertically ovoid; opening of anterior nostrils with a membranous flap. Dorsal surface of mesethmoid covered with cartilage, which extends all along the sensorial canal. Four or five infraorbitals with latero–sensorial canal present; first infraorbital thin and narrow, extending between the dorsal edge of maxila and lateral ethmoid, second infraorbital short and wide, not completely covering the dorsal part of the angulo– articular, anterior part squared off and exposed to surface. Third infraorbital the widest and longest, its ventral border in contact with the preopercle; fourth and fifth infraorbitals short and narrow, covering the hyomandibular. Supraorbital present. Premaxilla with ascending lateral process and two rows of teeth; external row with six tricuspid teeth arranged in a straight line except for the first proximal tooth which is a little out of line; internal row with four teeth, each with three to five cusps, the central cusp largest. Maxilla short, the posterior edge not reaching ante-

Román–Valencia et al.

rior edge of the second or third infraorbital. Maxilla with one or two teeth with three or four cusps each. Dentary with four large pentacuspid teeth with the central cusp largest, followed by six or seven small teeth, the first tricuspid and the last two unicuspid. Rhinosphenoid osseous, with cartilaginous border and attached to orbitosphenoid by cartilage and extending to anterior edge of prevomer. Orbitosphenoid wide, short and united to pterosphenoid by a band of cartilage. Palatine united with parasphenoid by cartilage. Dorsal fin with oblique dorsal edge, the second ray simple and the first two branched rays the longest. Radial and proximal pterygiophores of all rays of the dorsal fin inserted between the neural spines 11–18. Four to six supraneurals present between the head and the anterior part or the dorsal fin, with cartilage on the upper and lower edges. Pterygiophores of the anal fin completely cartilaginous, with just a small ossification of the three proximal anterior pterygiophores. Pectoral girdle with a pointed dorsal process above the cleithrum that surpasses the entire supracleithrum, which is joined to the postemporal. Cartilage present at the union of scapular with the internal surface of the supracleithrum. Four proximal radials. Pelvic bone short, straight, blunt and with cartilage at the anterior tip, its posterior projection extending between the junction of the two rows of pelvic rays. Pelvic fin long, but not reaching the origin of the anal fin. Caudal fin not scaled, forked with short pointed lobes, 9–10/9–10 principal caudal rays. Cartilage present at the basal part of the last caudal vertebra and the urostyle. Lateral line with 35–36 pored scales that extend in a straight line from the supracleithrum to the hypurals. Total vertebra 35. No sexual dimorphism was observed. Distribution This species is known from the Cinaruco River of southern Apure State (fig. 3) and from the Essequibo River Basin of Guyana, and probably extends into similar rivers throughout the Orinoco Basin in Venezuela and Colombia. Etymology Bryconamericus cinarucoense n. sp. is named for the Cinaruco River of southern Apure Sate, where the type series was collected. Habitat Bryconamericus cinarucoense n. sp. was collected along shore over sandy substrates in the mainstream of rivers, as well as tributaries with flow. The transparency of the tea–colored water is usually moderate to high, total dissolved solids and conductivity are very low, and pH is usually slightly acidic.

Bryconamericus singularis n. sp. (fig. 2, table 1) Holotype: MCNG 54500, 33.41 mm SL, Venezuela, Apure state, Orinoco River basin, Cinaruco River,

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1 cm

Fig. 2. Bryconamericus singularis n. sp.: holotype, MCNG 33.41 mm SL. Fig. 2. Bryconamericus singularis sp. n.: holotipo: MCNG 33,41 mm LE.

beach (6° 32.33´ N – 67° 25.35´ W), 20 II 1999, coll. D. A. Arrington. Paratypes: All from Venezuela, Apure State, Cinaruco River. Taken with holotype: IUQ 541 (3 ex. cleared and stained), MCNG 39659 (137 ex.); MCNG 39177 (14 ex.) 28.19–32.41, beach upstream from Laguna Larga (6° 33.15´ N – 67° 25.45´ W), 11 I 1999; MCNG 39194 (6 ex.) 25.76–33.60, beach upstream from Laguna Larga (6° 32' 20'' N – 67° 24' 81'' W), 11 VI 1999; MCNG 39232 (3 ex.) 29.44–30.69, beach downstream from Laguna Larga (6° 32.52´ N – 67° 24.52´ W), 11 VI 1999; MCNG 39245 (8 ex.) 27.73–32.78, beach downstream from Laguna Larga (6° 32.50´ N – 67° 24.08´ W), 11 I 1999; MCNG 39440 (10 ex.) 25.26–31.13, beach downstream from Laguna Larga (6° 33.37´ N – 67° 2.55´ W), 6 VI 1999; MCNG 40060 (28 ex.) 20.30–23.36, & MBUCV 33029, 22.23–25.45, Río Cinaruco, Laguna Espiñer, Dtto. Pedro Camejo, Edo. Apure, 17 II 1999; MCNG 40149 (15 ex.) 23.93– 34.03, beach (6° 36.32´ N – 67° 14.87´ W), 1 II 1999; MCNG 40374 (12 ex.) 26.24–30.83, Laguna Estrechura (6° 32.25´ N – 67° 16.95´ W), 16 III 1999; MCNG 40932 (2 ex.) 29.39–29.83, Laguna Espiñer, 12 VI 1999; MCNG 41014, (6 ex.) 26.62–32.01, Laguna Estrechura, 13 VI 1999; MCNG 41640 (18 ex.) 29.02–37.85, beach 5 (6° 32.92´ N – 67° 24.97´ W), 21 VI 1999; MCNG 41657 (17 ex.) 29.44–38.62, beach 6 (6° 32.52´ N – 67° 24.52´ W), 21 V 1999. Non–type material examined All from Venezuela, Apure State, Cinaruco River: MCNG 39149 (1 ex.) beach upstream from Laguna Larga (6° 38.05´ N – 67° 26.05´ W), 11 VI 1999; MCNG 39562 (2 ex.) beach, (6° 32.92´ N – 7° 24.97´ W) 2 X 1999; MCNG 39565 (4 ex.) beach (6° 32.50´ N –67° 24.97´ W), 10 II 1999; MCNG 39686 (5 ex.) beach (6° 33.05´ N – 67° 26.62´ W), 2 II 1999; MCNG 39721 (36 ex.) beach (6° 32.92´ N – 67° 24.97´ W), 20 II 1999; MCNG 39770 (19 ex.) beach (6° 32.52´ N – 67° 24.52´ W), 18 II 1999; MCNG 39801 (42 ex.) beach (6° 32.50´ N –

67° 24.08´ W), 18 II 1999; MCNG 39902 (17 ex.) beach (6° 33.37´ N – 67° 22.55´ W), 16 II 1999; MCNG 39946 (4 ex.) Laguna Espiñer (6° 32.80' N – 67° 25.90´ W), 16 II 1999; MCNG 40284 (7 ex.), beach (6° 33.32´ N – 67° 14.87´ W), 15 III 1999; MCNG 40312 (16 ex.) Laguna Guayaba (6° 34' 83'' N – 67° 13' 84'' W), 16 III 1999; MCNG 40403 (35 ex.) Laguna Estrechura (6° 32.32´ N – 67° 14.87´ W), 16 III 1999; MCNG 40578 (1 ex.) beach (6° 32.92´ N – 67° 24.97´ W), 18 III 1999; MCNG 40588 (1 ex.) beach (6° 32.92´ N – 67° 24.97´ W), 18 III 1999; MCNG 40769 (1 ex.) beach (6° 32.53´ N – 67° 24.82´ W), 24 III 1999; MCNG 40792 (88 ex.) beach (6° 32.33 ´N – 67° 25.35´ W), 24 III 1999; MCNG 40809 (40 ex.) beach (6° 32.33´ N – 62° 25.35´ W), 24 III 1999; MCNG 40829 (1 ex.) beach (6° 32.33´ N – 62° 25.35´ W), 24 III 1999; MCNG 41455 (3 ex.) beach (6° 32.50´ N – 67° 24.08´ W), 17 VI 1999; MCNG 41459 (1 ex.) beach (6° 32.50´ N – 67° 24.08´ W), 17 V 1999; MCNG 41562 (1 ex.) beach (6° 32.53´ N – 67° 24.28´ W), 21 VI 1999; MCNG 41572 (1 ex.) playa 2 (6° 32.53´ N – 67° 25.45´ W), 21 V 1999. Diagnosis Bryconamericus singularis n. sp. differs from congeners in having the top of the head flat, the dentary with six or seven slight unicuspid teeth; a dark lateral band extending from posterior edge of the usually diffuse humeral spot to the base of caudal fin, and that widens and strengthens in intensity posteriorly at point beneath dorsal fin origin; five supraneural bones without cartilage on either upper or lower edges and without cartilage on all structures. Description Body elongate, dorsal profile of head and anterior body rising from snout to dorsal–fin origin, inclined downwards from last dorsal–fin ray base to base of caudal fin. Ventral profile of body straight from snout to base of anal fin. Head and snout short;

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–74

–72

–70

–68

–66

–64

–62

–60

–58

Caribbean Sea

10 Orinoco

8 Cuyuní

Guyana

Colombia

4 Orinoco

Brazil

2 Negro

0 –74

–72

–70

–68

–66

100

0 100 200 300 400 km

–64

–62

–60

0 –58

Fig. 3. Geographic distribution of B. cinarucoense n. sp. (») and B. singularis n. sp. (S) in Venezuela. Fig. 3. Distribución geográfica de B. cinarucoense sp. n. (») y de B. singularis sp. n. (S) en Venezuela.

jaws equal in length; mouth terminal; lips soft and flexible, not covering the external row of premaxillary teeth; premaxila with one ascendent processes that articulate with mesethmoid and a lateral process that supports the teeth and articulates laterally with the ascendent process of the maxilla; posterior end of maxilla extends beyond anterior edge of orbit. Five infraorbitals with sensory canal present; first infraorbital thin, extending between the dorsal border of maxilla and lateral ethmoid, the second long, covering the dorsal portion of angulo–articular and anterior part of quadrate, third infraorbital wider, its postero–ventral border in contact with preopercle, fourth and fifth infraorbitals short and narrow, covering the hyomandibular. Supraorbital absent. Premaxilla with two rows of teeth; the outer row with four tricuspid teeth with bases arranged in straight line. Internal row with five tri– to pentacuspid teeth, with the central cusp much longer than rest. Maxilla with one or two tricuspid teeth. Dentary with four large front teeth, those at middle pentacuspid, those on sides tricuspid, all with central cusp much the larger, followed by six or seven small unicuspid teeth. Along the ventral portion of the supraoccipital process there are one or two foramens above the supraoccipital canal that communicate with the neural

complex; dorsal–most portion of neural complex extending as two small apophyses that continue ventrally as a canal. Rhinosphenoid osseous united to orbitosphenoid by a thin osseous plate. Osseous rhinosphenoid united to orbitosphenoid by thin laminar bone. First two branched dorsal–fin rays longer than rest. Proximal dorsal pterygiophores inserted between neural spines 9–10 and 16–17. Five supraneurals present, lower and upper ends without cartilage. Cartilage absent from the union between scapula with the internal surface of the cleithrum, and in general from all its structures. Pectoral girdle articulated postero–laterally with cranium by fusion with the supracleithrum and ventral end of posttemporal bone; united to dorsal edge of cleithrum. Cleithrum located beneath ventral edge of opercle, three postcleithrals present above posterior edge of pectoral girdle, first postcleithral posterior to union of postcleithrum and posttemporal, second and third poiscleithrals united below with cleithrum which extends over the pectoral rays. Three or four proximal radials. Pelvic fin short, its tip not reaching anal origin. Pelvic bone long and straight, its lateral edge convex, internal concave, and located parallel to central axis of body; ischial process with a short, straight pointed apophysis.

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Caudal fin forked with long pointed lobes. Principal caudal rays 10/10, no scales at base. 30–32 pored scales in the lateral line, which ends on the caudal fin. Pores of the lateral line forming a gentle curve from first to seventh scales, the rest in straight line. Total vertebrae 33. No sexual dimorphism observed. Color in alcohol Body light yellow, darker on dorsum. Lateral portion of body with a dark band behind humeral spot that extends to the base of the caudal fin, and that widens at point beneath dorsal fin origin. Guanine present dorsally and laterally and on opercle in many specimens. Humeral spot present but usually diffuse, about same height as pupil of eye and not usually extending dorsally beyond lateral stripe. Exposed edges of scales on dorsum and upper sides edged with black. Tips of caudal lobes dark, light yellow color of body extending onto central caudal rays, forming light spot at base of caudal fin that is bordered above and below by black. Dorsal, anal, pectoral and pelvic fins hyaline. Anal fin lightly pigmented at tips of rays, body above anterior

portion of anal fin base with concentration of melanophores, some specimens with melanophores outlining the muscle bundles, forming chevrons. Head dark and countershaded. Distribution Known from the Cinaruco River, Orinoco Basin, Apure State, Venezuela (fig. 3). Diet It is omnivorous, feeding on aquatic insects, snails, seeds and aquatic plants. Stomach contents of five fish included: Hemiptera: Vellidae: Microbelia (5.8% by Number, 33.3% by Frequency of Occurrence and 5.41% Volume) insect parts (100% F, 32.4% V), Mollusca: Bivalvia (47% N, 100% F & 4.05% V), seeds (41.1% N, 100% F & 4.05% V), plant stems (5.8% N, 33.3% F & 1.35% V) and vegetable matter (66.6% F & 32.4% V). Etymology The name refers to the singular and striking aspect of this new species.

Key to the species of Bryconamericus from the Cinaruco River. Clave para las especies de Bryconamericus del río Cinaruco.

Sides of body with a well–defined, dark, lateral stripe; humeral spot absent or only weakly developed (diffuse) and not usually vertically elongated; lateral scales 33 or fewer Sides without wide, dark, lateral stripe; humeral spot strongly developed, vertically elongate; lateral scales 35 or more Unbranched dorsal fin rays usually ii; unbranched anal–fin rays usually iv; length of maxilla 32–39% of head length, mean 35%; body short and stocky, its greatest depth 25–30% of standard length, mean 27% Unbranched dorsal fin rays usually iii–iv; unbranched anal–fin rays usually iii; length of maxilla in head length 18–32%, mean 27%; body long and slender, its greatest depth 19–26% standard length, mean 24%

Bryconamericus cinarucoense

Bryconamericus orinocoense

Bryconamericus singularis

Key to the species of Bryconamericus from tributaries of the Gulf of Paria. Clave para las especies de Bryconamericus de los afluentes del golfo de Paria.

Lateral maxilla Lateral maxilla

scales 35–36; total anal-fin rays 30–31; with 3–4 teeth scales 39–42; total anal-fin rays 26–29; with 5–8 teeth

Bryconamericus lassorum Bryconamericus yokiae

Román–Valencia et al.

Key to the species of Bryconamericus of the Apure and Arauca drainages. Clave para las especies de Bryconamericus de las vertientes de Apure y Arauca.

Sides without dark lateral stripe that continues onto central caudal–fin rays; caudal fin usually with a vertically oriented, crescent–shaped dark blotch at base Sides with a dark lateral stripe that continues onto central caudal–fin rays Five or more small teeth behind main series on dentary; body elongate (maximum body depth 26.6% SL); no small red or yellow dot on upper caudal peduncle Four or fewer small teeth behind main series on dentary; body not as elongate (maximum body depth 27–3% SL), small red or yellow dot on caudal peduncle present or absent Branched anal–fin rays 20 or more; no red or yellow dot on caudal peduncle Branched anal–fin rays 17 or fewer; small red or yellow dot on upper caudal peduncle present

Bryconamericus cinarucoense 2 Bryconamericus loisae 3 Bryconamericus alpha Bryconamericus cismontanus

Key to the species of Bryconamericus from the Caribbean Coastal drainages. Clave para las especies de Bryconamericus de las vertientes de la costa caribeña.

Total anal rays (simple plus branched) fewer than 21; small red or yellow dot present on upper caudal peduncle Total anal rays more than 20 Lateral scales fewer than 35; teeth on maxilla multicuspid with all cusps of equal length Lateral scales more than 34; teeth on maxilla multicuspid with central cusp longer than others More than four small teeth behind major series of large teeth on dentary; three to four unbranched anal–fin rays; body elongate (greatest body depth 26.6% SL) Fewer than three small teeth behind major series of large teeth on dentary; more than four unbranched anal–fin rays; body shorter and higher (greatest body depth 30.1% SL)

Bryconamericus cismontanus (Caribbean drainages of Falcon, Lara, Yaracuy and other states) 2 Bryconamericus charalae (endemic to Rio Aroa drainage, Lara) 3 Bryconamericus loisae (Zulia, Falcón, Lara, Carabobo,Yaracuy) Bryconamericus alpha (Aragua, Miranda, Anzoátegui)

Key to the species of Bryconamericus from the Lake Maracaibo drainage. Clave para las especies de Bryconamericus de las vertientes del lago Maracaibo.

Anal fin rays iii,13 to iii,16; scales from lateral line to anal fin base 2–3 Anal fin rays iii–v, 18–30; scales from lateral line to anal fin base 4 or more Anal fin rays v, 18–23; lateral scales 32–38; body shorter and stocky, its greatest body depth 30.07% SL Anal fin rays iii, 24–30; lateral scales 38–41; body long and slender, its greatest body depth 26.64% SL

Bryconamericus meridae 2 Bryconamericus alpha Bryconamericus cf loisae

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Key to the species of Bryconamericus from the Guyana Shield. Clave para las especies de Bryconamericus del Macizo de Guyana.

1 2

4 5

Fewer than 34 lateral scales More than 33 lateral scales Unbranched dorsal fin rays usually ii; unbranched anal–fin rays usually iv; length of maxilla 32–39% of head length, mean 35%; body short and stocky, its greatest body depth 25–30% standard length, mean 27% Unbranched dorsal fin rays usually iii–iv; unbranched anal–fin rays usually iii; length of maxilla in head length 18–32%, mean 27%; body elongate and slender, its greatest body depth 19–26% standard length, mean 24% Central caudal–fin rays with a black stripe, or with a dark spot on their bases Central caudal–fin rays without black stripe, a vertically oriented, crescent-shaped blotch at base (sometimes diffuse) usually present More than 19 branched anal–fin rays Fewer than 20 branched anal–fin rays Lateral scales 40–41; caudal fin overall dusky, with darker spot on base of central caudal rays, and whitish spot at base of upper lobe, and sometimes a at base of lower lobe as well Lateral scales 32–39; caudal fin not pigmented as above Caudal peduncle with small red or yellow dot; maxilla with 1–2 teeth with cusps of equal length; lateral scales 32–38; branched anal–fin rays 13–18 Caudal peduncle lacks red or yellow dot; maxilla with 4–6 teeth, with central cusp longer than others; lateral scales 38–39; branched anal–fin rays 17–18

Discussion A comprehensive discussion of the relationships of Bryconamericus species from South America is not possible at this time due to our poor knowledge of the taxonomy and systematics of the genus. No synapomorphies presently define Bryconamericus as a monophyletic unit. However, in a recent study with molecular characters Román–Valencia & Vanegas–Ríos (in press) propose the first hypothesis for the monophyly of the Central American species of this genus. We include species assigned to the genus Knodus because we do not consider a lack of scales on the caudal fin as sufficient to warrant generic recognition. Work in progress will hopefully uncover osteological characters that may be useful for generic diagnosis, but at this time the boundaries between Astyanax Baird and Girard, Bryconamericus Eigenmann, Hemibrycon Günther, Hemigrammus Gill, Hyphessobrycon Durbin, and Moenkhausia Eigenmann, remain tenuous and arbitrary.

2 3

Bryconamericus orinocoense

Bryconamericus singularis 4

Bryconamericus cinarucoense Bryconamericus alpha 5

Bryconamericus macrophthalmus 6

Bryconamericus cismontanus

Bryconamericus subtilisform

Bryconamericus singularis n. sp. is similar to Bryconamericus orinocoense (Román–Valencia, 2003d, table 1), but can be distinguished by the longer maxillary bone (18.3–32.9% in B. singularis vs. 12.8–31.4%), and the shape of the opercle, which has a straight posterior edge vs. strong notch present in upper part of opercle. It also differs in the lower number of vertebrae (33 in B. singularis vs. 35–36), is longer and less deep bodied: maximum body depth (19.5–25.9% en B. singularis vs. 26.8– 31.5%), and has a longer distance separating the dorsal fin and the hypurals (46.9–56.2 % in B. singularis vs. 36.4–39.9%). The upper jaw is also longer: (19.9–31.1% in B. singularis vs. 11.7–17. 8%); and the shape of the posterior edge of the opercle is concave and lacks a notch in B. singularis. The presence of six to seven small unicuspid teeth in B. singularis coincides with the five to seven small teeth reported in B. turiuba Langeani et al. (Upper Río Paraná system) by Langeani et al. (2005) but that species has tricuspid as well as unicuspid teeth in this series.

Román–Valencia et al.

While preparing the descriptions of B. singularis (in this work) and B. orinocoense (Román–Valencia, 2003d) we noted that we could place them in the genus Moenkhausia according to some character states (Eigenmann, 1918). For example, both have the teeth in the outer row of the premaxilla in a straight row and five teeth in the inner row. However, both species lack scales on the base of the caudal fin, as would be the case if they were Moenkhausia (some Bryconamericus, however, also have a scaled caudal, and some authors place them in the genus Knodus because of this). The second infraorbital is not in contact with the preopercle in Moenkhausia species but is in contact in B. singularis and B. orinocoense. This situation simply lends further credence to the paraphyly of both Bryconamericus and Moenkhausia as currently conformed, and points out the need for a broad revision and redefinition of these, and most other characid genera. Based on the results and analysis of this study (for example, the re–identification of specimens from the localities where records of B. breviceps y B. heteresthes were previously purported to occur, and the characters presented in the keys) we consider previous reports of B. breviceps and B. heteresthes from Venezuela (Román–Valencia, 2005) to be misidentifications, and they are here considered as either B. cinarucoense, or another, as yet undescribed species. On comparing data obtained during this study with previous reports (Román–Valencia, 2003d, 2005) we can find no differences to substantiate the recognition of B. alpha and B. motatanensis as separate species. In only one character: distance from dorsal–fin origin to anal–fin origin, is there a small difference: (35.8–36.1% in B. alpha vs. 37.0– 48.1% in B. motatanensis) which we consider insufficient. Thus, based on the International Code of Zoological Nomenclature (1999), the valid name is B. alpha, and B. motatanensis (described as B. beta motatanensis) is considered a synonym. Acknowledgements We thank Carmen Montaña, D. Aubrey Arrington, and Craig Layman who collected many specimens of these new species during their research on the ecology of the fishes of the Cinaruco River as part of their thesis work under the supervision of Dr. Kirk Winemiller. We also thank the Universidad Nacional Experimental de los Llanos Occidentales “Ezequiel Zamora'' for their support of our research, FONACIT for funds that support the Fish Collection of the Museum of Zoology of UNELLEZ–Guanare, and INAPESCA for scientific collecting permits. We give special recognition to the personnel of the Fish Collection at UNELLEZ–Guanare: Keyla Marchetto, Luciano Martínez and Iraima Montaña for their help in processing the specimens. This report was made possible by the generous support of COLCIENCIAS, of the Universidad de Quindio, Facultad de Ciencias

Básicas – Programa de Biología and Vicerrectoría de investigaciones, for the trips made by C. R–V. to the museums in Guanare (MCNG), Maracay–Rancho Grande (EBRG) and Caracas (MBUCV) in Venezuela. References Calcagnotto, D., Shaefer, S. A. & DeSalle, R., 2005. Relationships among characiform fishes inferred from analysis of nuclear and mitochondrial gene sequences. Molecular Phylogenetics and Evolution, 36: 135–153. Eigenmannn, C., 1918. The American Characidae. Memoirs of Museum of Comparative Zoology, XLIII (2): 114. Ferreria, K. M. & Carvajal, F. M., 2007. Knodus shinahota (Characiformes: Characidae) a new species from the río Shinahota, río Chapare basin (Mamoré system), Bolivia. Neotropical Icthyology, 5(1): 31–36. Ferreira, K. M. & Lima, F. C. T., 2006. A new species of Knodus (Characiformes: Characidae) from the Rio Tiquié upper Rio Negro system, Brazil. Copeia, 2006(4): 630–639. Fink, W. L., 1976. A new genus and species of characid fish from the Bayano river basin, Panamá (Pisces: Cypriniformes). Proceedings of the Biological Society of Washington, 88: 331–344. Géry, J., 1977. Characoids of the World, T. F. H. publications, Inc., Neptune, USA. International Comision on Zoological Nomenclature., 1999. International code of zoological nomenclature, 4th edition. International Truch for Zoological Nomenclature, London y University of California Press, Berkeley, Los Angeles. Jiménez J., Román–Valencia, C. & Cardona, M., 1998. Distribución y constancia de las comunidades de peces en la quebrada San Pablo, cuenca del río La Paila, Alto Cauca, Colombia. Actualidades Biológicas, 20: 21–27. Langeani, F., De Lucena, Z. M. S., Lima, P. J. & Tarelho–Pereira J., 2005. Bryconamericus turiuba, a new species from the Upper Río Paraná system (Ostariophysi: Characiformes). Copeia, 2005: 386–392. Lima, C. T. F., Malabarba, L. R., Buckup, P. A., Pezzi da Silva, J. F., Vari, R. P., Harold, A., Benine, R., Oyakawa, O. T., Pavanelli, C. S., Menezes, N. A., Lucena, C. A. S., Malabarba, M. C. S. L., De Lucena, Z. M. S., Reis, R. E., Langeani, F., Cassati, L., Bertaco, V. A., Moreira, C. & Lucinda P. H. F., 2003. Genera incertae sedis in Characidae p. 106–169. InReis, R., Kullander, S. O., Ferraris Jr., C., (Eds.), 2003. Check list of the freshwater fishes of South and Central America, Edipucrs Porto Alegre, Brazil. Lima, F. C. T. & Zuanon, J., 2004. A new species of Astyanax (Characiformes: Characidae) from the rapids of the lower rio Xingu, Brazil. Neotropical Ichthyology, 2: 117–122. Malabarba, L. R. & Kindel, A., 1995. A new species of the genus Bryconamericus Eigenmann, 1907

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from southern Brazil (Ostariophysi: Characidae). Proceedings of the Biological Society of Washington, 108: 679–686. Malabarba, L. R. & Weitzman, S. H., 2003. Description of new genus with six new species from southern Brazil, Uruguay and Argentina, with a discussion of a putative characid clade (Teleostei: Characiformes: Characidae). Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia, Porto Alegre, 16: 67–151. Malabarba, M. C. S. L. & Malabarba, L. R., 1994. Hypobrycon maromba, a new genus and species of characiform fish from the upper rio Uruguay, Brazil (Ostariophysi: Characidae). Ichthyological Exploration of Freshwaters, 5: 19–24. Planquette, P., Keith, P. & Le Bail, P.–Y., 1996. Atlas des poissons d'eua douce de Guyane. Muséum National D'Histoire Naturelle, Sepanguy, Paris. Román–Valencia, C., 1998. Descripción de una nueva especie de Bryconamericus (Characiformes, Characidae) para la cuenca alta de los ríos Ariari y Meta, Colombia. Actualidades Biológicas, 20: 21–27. – 2000. Tres nuevas especies de Bryconamericus (Ostariophysi, Characidae) de Colombia y diagnóstico del género. Revista de Biología Tropical, 48(2–3): 449–464. – 2001. Descripción de una nueva especie de Bryconamericus (Ostariophysi, Characidae) del alto río Suárez, cuenca del Magdalena, Colombia. Bollettino del Museo Regionale di Scienze Naturali di Torino,18(2): 469–476. – 2002a. Revisión sistemática de las especies del género Bryconamericus (Teleostei: Characidae) de Centroamérica. Revista de Biología Tropical, 50: 173–192. – 2002b. Description of a new species of Bryconamericus (Teleostei, Characidae) from the basin of the Golfo de Paria, northeastern, Venezuela. Revista Museo Argentino de Ciencias Naturales, n.s., 4: 209–214. – 2003a. Sistemática de las especies Colombianas de Bryconamericus (Characifomes, Characidae). Dahlia (Revista de la Asociación Colombiana de Ictiólogos), 6: 17–58. – 2003b. Description of a new species of Bryconamericus (Teleostei: Characidae) from the Amazon. Bollettino del Museo Regionale di Scienze Naturali di Torino, 20: 477–486. – 2003c. Una nueva especie de Bryconamericus (Pisces: Ostariophysi: Characidae) para el nororiente de Venezuela. Memoria de la Fundación La Salle de Ciencias Naturales, 155: 21–30. – 2003d. Three new species of the genus Bryconamericus (Teleostei: Characidae) from Venezuela. Dahlia (Revista de la Asociación Colombiana de Ictiólogos), 6: 7–15. – 2005. Sinopsis comentada de las especies del género Bryconamericus (Teleostei: Characidae) de Venezuela y norte del Ecuador, con la descripción de una nueva especie para Venezuela.

Memoria de la Fundación La Salle de Ciencias Naturales, 163: 27–52 Román–Valencia, C. & Muñoz, A., 2001. Ecología trófica y reproductiva de Bryconamericus caucanus (Pisces: Characidae). Bollettino del Museo Regionale di Scienze Naturali di Torino, 18(2): 459–467. Román–Valencia, C. & Vanegas–Ríos, J. A. (in press). Análisis filogenético y biogeográfico de las especies del género Bryconamericus (Characiformes, Characidae) para América Central. Caldasia, 29. Ruiz–C., R. I. & Román–Valencia, C., 2006. Osteología de Astyanax aurocaudatus Eigenmann, 1913 (Pisces: Characidae), con notas sobre la validez de Carlastyanax Géry, 1972. Animal Biodiversity and Conservation, 29(1): 49–64. Serra, P. J. & Langeani, F., 2006. Redescrição e osteologia de Bryconamericus exodon Eigenmann, 1907 (Ostariophysi, Characiformes, Characidae). Biota Neotropica, 6: 1–14. Silva, J. F. P., 2004. Two new species of Bryconamericus Eigenmann (Characiformes: Characidae) from southern Brazil. Neotropical Ichthyology, 2(2): 55–60. Silva, J. F. P. & Malabarba, L. R., 1996. Description of a new species of Hypobrycon from the upper río Uruguai, Brazil (Ostariophysi: Characidae). Comunicações do Museu de Ciências e Tecnologia da PUCRS, Série Zoologia, Porto Alegre, 9: 45–53. Song, J. & Parenti, L. R., 1995. Clearing and staining whole fish specimens for simultaneous demostration of bone, cartilage and nerves. Copeia, 1995: 114–118. Taylor, W. R. & Van Dyke, G. C., 1985. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9: 107–119. Vari, R. P., 1995. The Neotropical fish family Ctenoluciidae (Teleostei: Ostaríophysi: Characiformes): supra and intrafamilial phylogenetic relationship, with a revisionary study. Smithsonian Contributions to Zoology, 564: 1–96. Vari, R. P. & Siebert, D. J., 1990. A new unusually sexually dimorphic species of Bryconamericus (Pisces: Ostariophysi: Characidae) from the Peruvian amazon. Proceeding Biological Society, 103: 516–524. Weitzman, S. H., 1962. The osteology of Brycon meeki, a generalized characid fish, with an osteological definition of the family. Stanford Ichthyological Bulletin, 8: 1–77. Weitzman, S. H., Menezes, N. A., Evers, H. G. & Burns, J. R., 2005. Putative relationships among inseminating and externally fertilizing characids, with a description of a new genus and species of Brazilian inseminating fish bearing an anal–fin gland in males (Characiformes: Characidae). Neotropical Ichthyology, 3: 329–360.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 31.1 (2008)

Monitoring low density populations: a perspective on what level of population decline we can truly detect P. W. W. Lurz, M. D. F. Shirley & N. Geddes

Lurz, P. W. W., Shirley, M. D. F. & Geddes, N., 2008. Monitoring low density populations: a perspective on what level of population decline we can truly detect. Animal Biodiversity and Conservation, vol. 31.1: 29–39. Abstract Monitoring low density populations: a perspective on what level of population decline we can truly detect.— Monitoring of mammal species is an important part in detecting changes in their status. Efforts are based on a variety of direct and indirect methods and many low density populations are monitored through field signs. We present data on the endangered European red squirrel from Kidland Forest in the UK. We used cone transects to both record changes in seed availability and to monitor population trends. We examined the difficulty of accurately detecting population change when populations are low and field signs are patchily distributed. Current efforts would be sufficient to detect significant population declines of 50–75% in years with a modest squirrel population but not when they fall below one squirrel for every 20 ha of forest. The findings emphasise that monitoring aims have to be clearly defined with an awareness and understanding of what level of change the adopted methodological approach can reliably detect. We propose that mammal monitoring schemes need to be based on a pilot scheme to determine effect size and planned accordingly. Key words: Squirrel, Sciurus vulgaris, Conservation, Power analysis. Resumen Seguimiento de poblaciones con baja densidad: una perspectiva de qué nivel de declive poblacional podemos detectar con certeza.— El seguimiento de las especies de mamíferos es una parte importante de la detección de los cambios producidos en su estatus. Los esfuerzos van dirigidos hacia diversos métodos directos e indirectos, y muchas poblaciones que presentan una densidad baja se monitorizan mediante rastros o signos de campo. En este trabajo presentamos datos de una especie en peligro, la ardilla roja, del bosque de Kidland en el Reino Unido. Se realizaron transectos de detección de piñas o conos para registrar tanto los cambios en la disponibilidad de semillas como para monitorizar las tendencias de la población. Examinamos la dificultad que presenta detectar con precisión los cambios poblacionales, cuando las poblaciones son pequeñas y los restos alimentarios de presencia están distribuidos de forma desigual. Los esfuerzos normales deberían ser suficientes para detectar disminuciones poblacionales significativas del 50– 75% en años con una población de ardillas modesta, pero no cuando la densidad está por debajo de una ardilla cada 20 ha de bosque. Nuestros hallazgos enfatizan que los esfuerzos de seguimiento deben estar claramente definidos, con el conocimiento y la comprensión de qué nivel de cambio puede realmente detectar de forma fiable el enfoque metodológico adoptado. Proponemos que los seguimientos de mamíferos deben estar basados en un esquema piloto, con el fin de determinar el efecto del tamaño, y ser planificados consecuentemente. Palabras clave: Ardilla, Sciurus vulgaris, Conservación, Análisis de potencia. (Received: 2 V 07; Conditional acceptance: 7 VIII 07; Final acceptance: 22 IX 07) P. W. W. Lurz & M. D. F. Shirley, IRES, Devonshire Building, School of Biology and Psychology, Univ. of Newcastle upon Tyne, NE1 7RU, UK.– N. Geddes, Forest Enterprise, Kielder Forest District, Ealsburn, Bellingham, Hexham, Northumberland, UK. ISSN: 1578–665X

Lurz et al.

Introduction Monitoring and data on the distribution and abundance of mammal species are important to the understanding and detection of changes in the environment. They inform conservation activities, help assess the impacts of pollution, road traffic schemes or land use change and indicate the spread of introduced alien species (e.g. Battersby & Greenwood, 2004; Fitzgibbon, 1997; Hlavac, 2005; Harris & Yalden, 2004; Kataev, 2005; Macdonald et al., 1998; Philcox et al., 1999). Data from surveys or monitoring generally encompasses two types of information on the status of a species: presence/absence data, and data on abundance (Macdonald et al., 1998). Distribution data either at regional or national scale in Britain are usually sightings recorded at 1 km2 resolution (e.g. Lurz et al., 2005) and these are submitted by the general public or wildlife organisations to local record centres. Monitoring within some sites may be at a much finer scale and can provide an index of population trends over time. Monitoring implies that it is repeated in the same defined study area and that it should be carried out systematically (Macdonald et al., 1998). A large number of survey or monitoring methods in mammals are based on field signs. These include systematic surveys for spraints and tracks of otters (Lutra lutra, Strachan & Jeffreries, 1996), snow tracking for pine martens (Martes martes, Zalewski 1999), sett surveys for badgers (Meles meles, Clements et al., 1988), systematic surveys for latrines and feeding stations in water voles (Arvicola terrestris, Strachan et al., 2000) or pellet counts for deer (e.g. Hemami & Dolman, 2005). For squirrels, monitoring methods based on field signs include visual transects (Gurnell et al., 2001), tracks (Andrén & Lemnell, 1992), drey counts (Fitzgibbon, 1997; Wauters & Dhondt, 1988) and feeding remains (Gurnell et al., 2001, 2004). Additionally, hair–tube surveys (Gurnell et al., 2001) are used to also determine population size and abundance. Monitoring methods employed for squirrels focus on the detection of field signs or sightings rather than the area of habitat occupied. This is because home range size may increase when food is scarce and when densities are low, so area occupied is not a reliable measure of squirrel abundance. The various squirrel monitoring methods have been described in detail by Gurnell & Pepper (1994), and Gurnell et al. (2001, 2004). Data based on squirrel field signs can be patchily distributed in space. They also vary with seasonal and annual patterns of food availability. This can lead to estimates with large associated errors making it difficult to calculate abundance accurately. In addition, it may result in insufficient statistical power to confidently determine whether a population change has truly occurred (Gurnell et al., 2004). Drey surveys are impractical in dense conifer forests and recent work (Gurnell et al., 2007) indicated that visual transects are very poor at

detecting red squirrels in Sitka spruce dominated forests. An additional limitation is that visual transects and hair–tube surveys are the only methods which can distinguish between the native red squirrel (Sciurus vulgaris) and the introduced grey squirrel (S. carolinensis) which has become naturalized in the UK and in regions of Continental Europe. However, hair–tube surveys are costly in terms of time and require expensive equipment and experienced staff (Gurnell et al., 2001). In the UK, the most commonly used method to monitor squirrel presence and abundance in red squirrel–only areas are cone transects. Whilst this method cannot distinguish between squirrel surveys, it is deemed more reliable than visual transects, cheaper than hair–tube surveys, and can be employed in the dense spruce forests of northern England and Scotland where visual transects do not work (Gurnell et al., 2001). Here we present data on a 6–year monitoring scheme from Kidland Forest, a designated red squirrel reserve. Kidland, together with the adjacent Uswayford Forest in the Cheviots, form the most isolated squirrel reserves in Northern England. Located in valley systems within the Cheviot hills, they are surrounded by open moorland incapable of supporting populations of squirrels. Due to this isolation and therefore lack of immigration and emigration opportunities, local red squirrel populations are potentially affected by timber harvesting and forest restocking operations. Conservation management therefore needs to maintain a minimum area of seed–bearing trees and avoid fragmentation of the forest through harvesting. We discuss (i) observed changes in seed food availability; (ii) describe monitoring efforts at Kidland Forest and (iii) examine the difficulty of accurately detecting population change when populations are low and field signs are patchily distributed. Material and methods Study area Kidland Forest is part of Kielder Forest District and is located in the Cheviot hills in Northumberland, north–east England. The woodland is dominated by Sitka spruce (Picea sitchensis) with smaller plantations of Japanese larch (Larix kaempferi), Scots pine (Pinus sylvestris), lodgepole pine (Pinus contorta), Douglas Fir (Pseudotsuga menziessi), Norway spruce (Picea abies) and small areas of broadleaves. Survey methodology Red squirrels at Kidland Forest were monitored using cone transect lines (Gurnell et al., 2001). The area between two rows of planted trees was cleared for up to 70 m and all cones (fallen cones as well as squirrel feeding remains) were counted on an annual basis in late autumn of each year.

Animal Biodiversity and Conservation 31.1 (2008)

The data were used to calculate an average number of cones consumed by squirrels per unit area (m2) for each conifer species and an estimated annual cone crop. Using the area for each conifer species of seed– bearing age an estimated total of consumed seed energy was calculated (table 1). From this, the number of squirrels that could have been supported by the energy consumed can be derived by using an estimate of the annual squirrel energy requirement (Grönwall (1982): red squirrel energy requirement: 418.4 kJ/day ~ 152716 kJ/year; Gurnell (1987): 389.1 kJ/day ~ 142026 kJ/year). This estimate varies since the number and size of seeds within each cone is dependent on tree species, region and season. However, estimates derived in this way have been found to be significantly correlated with estimates from trapping data (Gurnell et al., 2004).

Using the methodology of Gurnell et al. (2004), an estimate of potential carrying capacity of a forest block can be calculated by multiplying minimum and average red squirrel densities with the area of mature (seed producing) tree species: n

Tmin =

a .d i=1 i

i,min

Tave =

i=1

ai .di,ave

where Tmin and Tave are the total population sizes for poor and average seed years, n is the total number of tree species stands of cone bearing age, a is the area of the tree species stands and dmin and dave are the observed red squirrel density for that type of habitat in poor and average seed crop years. To test for heterogeneity in the squirrel population we calculated the standardized Morisita index of dispersion (Myers, 1978) for each year, see

Table 1 Estimates of caloric values (kJ cone–1) for conifer species. Tabla 1. Estimas de los valores calóricos (kJ cono–1) de las especies de coníferas.

Tree species Scots pine

Energy (kJ/cone)

References

3.84

Wauters et al., 1992

Lodgepole pine

2.48

Smith, 1968

Norway spruce

9.6–17.2

Grönwall, 1982

Sitka spruce

5.3

Smith, 1981

Japanese larch

1.7

Grodzinski & Sawicka–Kapusta, 1970

Douglas fir

6.22

Smith, 1968

European Larch (Larix decidua)

2.3

Grodzinski & Sawicka–Kapusta, 1970

Table 2. Estimates for squirrel densities in different crop types are based on fieldwork in Kielder Forest and similar habitats in the literature, and relate to the minimum number of adults (and post dispersal subadults recruited into the population) alive. Tabla 2. Las estimas de las densidades de ardillas en función de la producción anual de semillas se basan en el trabajo de campo en el bosque de Kielder y en trabajos en hábitats similares que hallamos en la literatura, y se relacionan con el número mínimo de adultos vivos (y subadultos post–dispersión) reclutados en la población.

Tree species

Red squirrel density (ha–1)

Sitka spruce

0.02–0.20

Lurz et al., 1998

Norway spruce

0.12–0.41

Lurz et al., 1998

Pine

0.16–0.43

Halliwell, 1997; Lurz et al., 1998

Larch

0.21

Other conifers

0.03–0.80

Source

Garson & Lurz, 1998 Bobyr, 1978; Lurz, 1995

Lurz et al.

Table 3. This index is independent of both population density and sample size, and the value Ip ranges from –1.0 to +1.0, with 95% confidence limits at –0.5 and +0.5. Random patterns of dispersion give an Ip of zero, clumped patterns above zero, uniform patterns below zero. Power analysis Before calculations of statistical power can be made it is necessary to ensure that the number of transects taken does not constitute such a large proportion of the total number of possible transects that the precision of the calculated power will require correction. The finite population correction, fpc (Thompson, 2002) was calculated:

fpc =

N–n /______ N–1

where n is the number of samples taken from the population of possible samples N. As n approaches N, the sampling variance approaches zero and the precision obtained from larger sample sizes becomes more significant. Conversely, if fpc is close to unity then no correction has to be made. An a priori power analysis for the Wilcoxon– Mann–Whitney U–test is conducted by first performing an a priori power analysis for the t–test for means. If the t–test model is valid, and Nt designates the sample size necessary for the t– test to achieve some given power (1 – ), then the sample size N u = N t / A.R.E. yields approximately the same power for the U–test. A.R.E. denotes the asymptotic relative efficiency (or Pitman efficiency) of the U–test relative to the t–test which is 3/ = 0.955 (see Lehmann, 1975). The power of a paired t–test was calculated using the method of Kraemer & Thiemann (1987). It is first necessary to calculate the effect size of the observed decline, which is given by:

[ 2 + 1°/°pq]1/2

where p is the proportion of samples in year 1, q is the proportion of samples in year 2, and is Glass’s effect size. Glass’s effect size is given by = ( 1 – 2) / ", where 1 is the population size in year 1, 2 is the population size in year 2, and " is the pooled standard deviation. The effect size for each pair of consecutive years (2001/ 2002, 2002/2003, etc.) was presented against the sample size (adjusted by the A.R.E. as discussed above). We employed a two–year comparison because an intervening mast year between the two survey points would mask any decline which may be present. Alternatively, if the population declines in both subsequent years, the difference between year 1 and year 3 will naturally be greater than between year 1

and 2. One would therefore think that with a bigger effect size, more power could be obtained. However, since the variance is pooled between years it is larger in the former case, so a greater change is needed to confidently detect its presence. Estimates of power therefore get lower as the gap between sampling intervals increases. Finally, from a conservation perspective, when a population is potentially declining it may not be viable to wait several years before we can be confident that the decline is actually occurring. We used the same methodology to calculate the power to detect a specific decline in squirrel population size, by replacing 2 in the above equations with a population size reduced artificially by a certain percentage (12.5%, 25%,…, 87.5%). To determine the ability to detect a change in a "healthy" population of squirrels, we calculated power based on the data for 2001 for 1, and the pooled standard deviation between 2001 and 2002 for ". A second analysis determined the ability to detect a change in size of a population which had already suffered a substantial decline, using the population size in 2005 as 1, and the pooled standard deviation between 2005 and 2006 for ". In both cases we were interested in the power of the test to detect a real population trend at a known number of samples. These analyses were dependent (in the absence of real data) on the standard deviation remaining at the observed levels following a large decline in population size. To test the impact of this assumption on the predictions of the power analysis, we calculated the number of transects required to achieve an 80% power for a range of standard deviations, using the mean population size in 2005 for 1. Results Seed crops varied strongly between years at Kidland Forest and ranged from 0.00–2.03 cones m–2 in pine and larch and from 0.4–1.2 cones m–2 in Sitka spruce over the last 6 years (fig. 1). Red squirrel feeding remains and choice of conifer cones broadly followed seed crops. However, cone availability at Kidland between the different conifer plantations was significantly clumped (table 3) and varied markedly between locations and transect lines. As a result, estimates of red squirrel abundance calculated from the cone transect lines were associated with a large errors and data were overdispersed (fig. 1). A comparison of the potential carrying capacity for Sitka spruce in 2006 (635 ha of mature forest) with an estimate of the red squirrel population based on cone transect data illustrates the factors a forester can influence and manage for and natural fluctuations in populations size. Observed densities of red squirrels in Sitka spruce plantations range from 0.02–0.2 squirrels ha –1 (table 2). Depending on seed food availability this

Animal Biodiversity and Conservation 31.1 (2008)

3.5

Total cone density

3.0 2.5 2.0 1.5 1.0 0.5 0.0 B

2001

2002

2003

2004

2005

2006

2001

2002

2003

2004

2005

2006

2.0 1.8

Squirrel cone density

1.6 1.4 1.2 1.0 0.8 0.6 0.4 0.2 0.0

Mean pine

Mean larch

Mean Sitka

Fig. 1. Cone crop patters for pine, larch and Sitka spruce at Kidland Forest: A. Total cone density (cones m–2) for each year; B. The amount of cones (m–2) stripped by squirrels. Fig. 1. Patrones de recolección de conos para los pinos, los alerces y la pícea de Sitka en el bosque de Kidland: A. Densidad total anual de conos (conos m–2); B. Cantidad de conos (m–2) descortezados por las ardillas.

would result in a potential carrying capacity of the Sitka spruce plantations at Kidland Forest of 13–127 squirrels. The plantations of larch (34 ha) would approximately support 7 and the pine plantations (107 ha) 17–46. Population size for red squirrels estimated from 2006 Sitka spruce cone transect data, the mean

density (± 1 sd) of squirrel feeding signs (0.06 ± 0.197) and seed energy values (table 1) give an estimate for the average and upper limit of 13–57 squirrels for the Sitka spruce. In 2006 pine crops failed and the very poor cone crop in larch would at most have supported two squirrels. Whilst managers can influence the lower and upper

Lurz et al.

Table 3. Standardized Morisita index (Ip) for squirrel feeding signs for each year. Values above 0.5 indicate significant clumping of the animal’s distribution. Tabla 3. Índice de Morisita estandarizado para los rastros alimentarios de la ardilla, para cada año. Los valores superiores a 0,5 indican una agrupación significativa de la distribución de animales.

Year

2001

0.57

2002

0.55

2003

0.57

2004

0.61

2005

0.54

2006

0.56

bounds of habitat carrying capacity, they have no control over fluctuations in seed crop size and thus annual squirrel abundance. The estimated population of red squirrels at Kidland for 2006 is currently near the lower third of the forest's potential carrying capacity. For the calculation of the finite population correction it was first necessary to estimate the total number of potential transects available to be sampled. The total area of mature forest at Kidland is 799 ha. The average area of a cone transect was 40.9 m2, thus the total number of possible transects (N) is therefore 195,522. The maximum combined number of transects used between two years (n) was 63. This yields an fpc of 0.9998, which is negligible and therefore cannot affect the estimation of power. Examining the 6 years of cone transect data for 2001–2006, figure 2 plots the effect size ( ) calculated from 2001–2006 cone data against the number of samples needed to achieve a range of levels of statistical power. The calculated values for fail to achieve the suggested value for statistical power of 0.80 (Cohen, 1988) at the given sample sizes. This implies that a statistically significant trend in population size has insufficient replication to confidently detect a trend which is really there. The results clearly show that current sample sizes of around 35 transects a year are not sufficient to detect small changes in effect and thus population size. This is especially true for years where the squirrel population is low (few feeding signs) and the field signs are patchily distributed across the forest. When concerned about the population decline of a rare species a more conservative approach would be to increase the likelihood

of declaring a decline has occurred, when in fact it has not —in effect increasing the rate of false positives (i.e. significance) with the benefit of simultaneously decreasing the rate of false negatives (i.e. power). Figure 2 therefore also demonstrates the impact of a 10% level of significance on the calculated number of samples required for each effect size and level of power. The highest level of power achieved was approximately 70% (for 2003–2004) rather than approximately 50% power assuming a 5% level of significance. Consequently, the a priori analysis of the sample size required to achieve statistical power (fig. 3) is particularly useful in planning future monitoring programmes. The survey effort currently employed would be sufficient to detect significant population declines of 50%–75% in years with a modest red squirrel population of 0.05 squ/ha–1 or greater as observed in 2001 (fig. 3A). However, when the population sizes are small ([ 0.02 squ/ha–1; fig. 3B) the statistical test does not achieve even a 50% power even following the maximum modelled population decline of 87.5%. The method would still indicate presence of squirrels based on the presence of feeding signs but any statistical comparisons between years lacks in sample size. Figure 4 illustrates that in pairs of years with large variations, such as from 2005 to 2006, an economically and logistically impractical number of sample transects (> 1,000) would be required to achieve adequate levels of power. Discussion The findings of our study highlight the difficulties of monitoring small populations of endangered mammals in habitats where surveys based on field signs are the only option. Kidland Forest is a rare case where conservation management (Lurz et al., 2003) has been followed by annual monitoring with the clear aim to assess the impact of forest operations on the viability of a red squirrel population. It provides a medium–term data set with which to statistically investigate the limits of field sign surveys to reliably detect population change. Cone crops at Kidland varied strongly temporally and spatially between 2001–2006. The patchiness and annual variability of field signs across the forest and the resulting large error estimates make it difficult to calculate squirrel abundance accurately. This may mask real population change and may make it difficult to distinguish the relative impacts of natural fluctuations in seed crops (Gurnell, 1983, 1987) and squirrel declines as a result of forest operations or other factors. The examination of 6 years of field data clearly shows that the current sampling programme is not sufficient to detect small changes in population size. Current efforts would be sufficient to detect significant population declines of 50–75% in years with a modest red squirrel population but not when

Animal Biodiversity and Conservation 31.1 (2008)

1,000,000

Number of samples

100,000

10,000

1,000

100

1 B

0.2

0.4

0.6

0.8

0.2

0.4

0.6

0.8

1,000,000

Number of samples

100,000

10,000

1,000

100

10% power

50% power

90% power

20% power

60% power

95% power

30% power

70% power

99% power

40% power

80% power

observed

Fig. 2. Graph illustrating the tabulated values for power at each value of and sample size for a one– sample t–test at the 5% (A) and 10% (B) levels of significance, using the method of Kraemer & Thiemann (1987). Observed values from cone transects at Kidland Forest are indicated by circles. Fig. 2. Gráfico que ilustra los valores tabulados de la potencia para cada valor de y cada tamaño de la muestra para un test–t de una sola muestra, a los niveles de significación del 5% (A) y el 10% (B), utilizando el método de Kraemer & Thiemann (1987). Los valores observados a partir de los transectos de conos del bosque de Kidland se hallan destacados mediante círculos.

Lurz et al.

Number of samples

75% population decline 50% population decline

25% population decline 10

0.1

0.3

0.5

0.7

0.9

1.1

Number of samples

50 75% population decline

50% population decline 10 0.1

0.3

0.5

0.7

0.9

Observed

80% power

50% power

95% power

1.1

Fig. 3. An a priori power analysis of the sample size required to achieve statistical power: A. Analysis using highest observed population (2001–2002) to calculate effect size ; B. Analysis using lowest observed population (2005–2006) to calculate effect size . Fig. 3. Un análisis de potencia a priori del tamaño de la muestra requerido para alcanzar un poder estadístico: A. Análisis utilizando la población observada de mayor tamaño (2001–2002) para calcular la fuerza del efecto ; B. Análisis utilizando la población observada de menor tamaño (2005–2006) para calcular la fuerza del efecto .

squirrel populations fall below 1 squirrel for every 20 ha of forest. Using field signs when densities are this low would still detect the presence of red squirrels but any meaningful statistical comparisons would require sample sizes of > 1,000 transects, a survey effort which is out of proportion in terms of time and cost for the data obtained. We also demonstrate the effects of increasing the critical level of significance

on statistical power, on the understanding that it is better to assume a population decline where there was none than to fail to detect a decline where there was one. However, in this study increasing significance to 10% still failed to achieve a statistical power of 80%. The study findings underline the importance of applying an integrated monitoring approach in which

Number of cone lines needed

Animal Biodiversity and Conservation 31.1 (2008)

1,000

100

0.05

0.1 0.15 Pooled standard deviation

0.2

0.25

Fig. 4. The number of cone lines (pooled over two years) needed to achieve 80% confidence of detecting a real change in population size (one–tailed Mann–Whitney U–test, 5% significance). The dotted lines represent the number of cone lines needed when the upper and lower 95% confidence intervals for the pooled standard deviation are used in the calculation. The arrow indicates the observed pooled standard deviation. Fig. 4. Número de líneas de conos (reunidos durante dos años) necesarias para alcanzar un 80% de confianza al detector un cambio real en el tamaño de la población (test U de Mann–Whitney de una cola, 5% de significación). Las líneas de puntos representan el número de líneas de conos necesarias cuando se utilizan para el cálculo los intervalos de confianza del 95% superior e inferior para la desviación estándar reunida. La flecha indica la desviación estándar reunida observada.

more than one method is combined (Flowerdew et al., 2004). Monitoring at Kidland without an independent assessment of carrying capacity would not be able to distinguish the relative population declines from changes in seed availability and potential impacts from harvesting operations, disease outbreaks (Sainsbury et al., 2000; McInnes et al., 2006) or other factors. The results also emphasise that monitoring aims have to be clearly defined with an awareness and understanding of what the adopted methodological approach can reliably detect. This is particularly true when monitoring small endangered populations based on widely distributed field signs. Very often the objectives of monitoring programmes are poorly defined (Yoccoz et al., 2001), and there is a need to consider carefully: (i) the types of data to be collected, (ii) the precision with which population change can be detected for an appropriate sampling method and effort and (iii) the cost effectiveness of methods given budgetary constraints (Manley et al., 2004, Gaidet–Drapier et al., 2006). We therefore propose that the setting up of mammal monitoring schemes is based on a pilot study that allows the estimation of effect size. From this, statistical power analysis can inform the moni-

toring scheme with respect to adequate sample size and/or the magnitude of population change the proposed scheme can confidently detect. Acknowledgements We would like to thank Louise Bessant, David Wood, Bodil Elmhagen, Sarah Yupp and Eleni Sofianopoulou for their assistance with the fieldwork at Kidland Forest and Linda DaVolls for support during one of the surveys. The project was funded by Forestry Commission, Kielder Forest District. We would also like to acknowledge the two referees for their highly constructive and insightful comments. References Andrén, H. & Lemnell, P., 1992. Population fluctuations and habitat selection in the Eurasian red squirrel Sciurus vulgaris. Ecography, 15: 303–307. Battersby, J. E. & Greenwood, J. J. D., 2004. Monitoring terrestrial mammals in the UK: past, present and future, using lessons from the bird world. Mammal Review, 34(1–2): 3–29.

Bobyr, G. Y., 1978. A contribution to the ecology of the Altaian squirrel (Sciurus vulgaris altaicus) acclimatised in the Teberdinsky State Reservation. Zoologicheskii Zhurnal, 57: 253–259. Cohen, J., 1988. Statistical Power Analysis for the Behavioral Sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale, New Jersey. Fitzgibbon, C. D., 1997. Small mammals in farm woodlands: The effects of habitat, isolation and surrounding land-use patterns. Journal of Applied Ecology, 34(2): 530–539. Flowerdew, J. R., Shore, R. F., Poulton, S. M. C. & Sparks, T. H., 2004. Live trapping to monitor small mammals in Britain. Mammal Review, 34(1– 2): 31–50. Gaidet–Drapier, N., Fritz, H., Bourgarel, M., Renaud, P. C., Poilecot, P., Chardonnet, P., Coid, C., Poulet, D. & Le Bel, S., 2006. Cost and efficiency of large mammal census techniques: comparison of methods for a participatory approach in a communal area, Zimbabwe. Biodiversity and Conservation, 15(2): 735–754. Garson, P. J. & Lurz, P. W. W., 1998. Red squirrel monitoring: the potential of hair–tubes for estimating squirrel abundance in conifer plantations dominated by Sitka spruce: Report to JNCC, Contract, 76–01–68. Grodzinski, W. & Sawicka–Kapusta, K., 1970. Energy values of tree–seeds eaten by small mammals. Oikos, 21: 52–58. Grönwall, O., 1982. Aspects of the food ecology of the red squirrel (Sciurus vulgaris L.). Ph. D. Thesis, University of Stockholm. Gurnell, J., 1983. Squirrel numbers and the abubdance of the seeds. Mammal Review, 13: 133–148. – 1987. The Red Squirrel. Christopher Helm, London. Gurnell, J., Lurz, P. W. W., Mcdonald, R., Cartmel, S., Rushton, S. P., Tosh, D., Sweeney, O. & Shirley, M., 2007. Developing a monitoring strategy for red squirrels (Sciurus vulgaris) across the UK Report to JNCC and PTES, London, UK. Gurnell, J., Lurz, P. W. W. & Pepper, H., 2001. Practical Techniques for surveying and monitoring squirrels. Forestry Commission Practice Note 11, Forestry Commission, Edinburgh. Gurnell, J., Lurz, P. W. W., Shirley, M. D. F., Cartmel, S., Garson, P. J., Magris, L. & Steele, J., 2004. Monitoring tred squirrels Sciurus vulgaris and grey squirrels Sciurus carolinensis in Britain. Mammal Review, 34: 51–74. Gurnell, J. & Pepper, H., 1994. Red squirrel conservation: field study methods. Research Information Note No. 255, Forestry Commission, Farnham. Halliwell, E. C., 1997. Red squirrel predation by pine martens in Scotland. In: The conservation of red squirrels, Sciurus vulgaris L.: 39–48 (J. Gurnell & P. W. W. Lurz, Eds.). London: Peoples Trust for Endangered Species. Harris, S. & Yalden, D. W., 2004. An integrated monitoring programme for terrestrial mammals

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in Britain. Mammal Review, 34(1–2): 157–167. Hemami, M. R. & Dolman, P. M., 2005. The disappearance of muntjac (Muntiacus reevesi) and roe deer (Capreolus capreolus) pellet groups in a pine forest of lowland England. European Journal of Wildlife Research, 51(1): 19–24. Hlavac, V., 2005. Increasing permeability of the Czech road network for large mammals. Gaia– Ecological Perspectives for Science and Society, 14(2): 175–177. Kataev, G. D., 2005. The state of the mammal community of boreal forest ecosystems in the vicinity of a nickel–smelting plant. Russian Journal of Ecology, 36(6): 421–426. Kraemer, H. C. & Thiemann, S., 1987. How Many Subjects?: Statistical Power Analysis in Research SAGE Publications, Newbury Park. Lehman, E. L., 1975. Nonparametrics: Statistical Methods Based on Ranks Holden–Day, San Francisco, USA. Lurz, P. W. W., 1995. The ecology and conservation of the red squirrel (Sciurus vulgaris L.) in upland conifer plantations. Ph. D. Thesis, University of Newcastle. Lurz, P. W. W., Garson, P. J. & Ogilvie, J. F., 1998. Conifer species mixtures, cone crops and red squirrel conservation. Forestry, 71: 67–71. Lurz, P. W. W., Geddes, N., Lloyd, A. J., Shirley, M. D. F., Rushton, S. P. & Burlton, B., 2003. Planning a red squirrel conservation area: using a spatially explicit population dynamics model to predict the impact of felling and forest design plans. Forestry, 76: 95–108. Lurz, P. W. W., Hewitt, S. M., Shirley, M. D. F. & Bruce, J., 2005. Mammals in Cumbria: examples of what publicly collected records can tell us about the distribution and ecology of local species. Carlisle Naturalist, 13: 1–15. Macdonald, D. W., Mace, G. & Rushton, S., 1998. Proposals for future monitoring of British mammals. Department of the Environment, Transport and the Regions, London. Manley, P. N., Zielinski, W. J., Schlesinger, M. D. & Mori, S. R., 2004. Evaluation of a multiplespecies approach to monitoring species at the ecoregional scale. Ecological Applications, 14(1): 296–310. McInnes, C. J., Wood, A. R., Thomas, K., Sainsbury, A. W., Gurnell, J., Dein, J. & Nettleton, P. F., 2006. Genomic characterization of a novel poxvirus contributing to the decline of the red squirrel (Sciurus vulgaris) in the UK. Journal of General Virology, 87: 2115–2125. Myers, J. H. 1978. Selecting a measure of dispersion. Environmental Entomology, 7: 619–621. Philcox, C. K., Grogan, A. L. & Macdonald, D. W., 1999. Patterns of otter Lutra lutra road mortality in Britain. Journal of Applied Ecology, 36(5): 748–762. Sainsbury, A. W., Nettleton, P., Gilray, J. & Gurnell J., 2000. Grey squirrels have high seroprevalence to a parapoxvirus associated with deaths in red squirrels. Animal Conservation, 3: 229–233.

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Smith, C. C., 1968. The adaptive nature of social organization in the Genus of three squirrels Tamiasciurus. Ecological Monographs, 38: 31–63. – 1981. The indivisible niche of Tamiasciurus: an example of non–partitioning of resources. Ecological Monographs, 51: 343–363. Thompson, S. K., 2002. Sampling. Second Edition. Wiley, New York. Wauters, L. A. & Dhondt, A. A., 1988. The use of red squirrel (Sciurus vulgaris) dreys to estimate

population density. Journal of Zoology, London, 214: 179–187. Wauters, L., Swinnen, C. & Dhondt, A. A., 1992. Activity budget and foraging behaviour of red squirrels (Sciurus vulgaris) in coniferous and deciduous habitats. Journal of Zoology, 227: 71–86. Yoccoz, N. G., Nichols, J. D. & Boulinier, T., 2001. Monitoring of biological diversity in space and time. Trends in Ecology and Evolution, 16: 446–453.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 31.1 (2008)

Effects of temperature on embryonic and larval development and growth in the natterjack toad (Bufo calamita) in a semi–arid zone D. Sanuy, N. Oromí & A. Galofré

Sanuy, D., Oromí, N. & Galofré, A., 2008. Effects of temperature on embryonic and larval development and growth in the natterjack toad (Bufo calamita) in a semi–arid zone. Animal Biodiversity and Conservation, 31.1: 41–46. Abstract Effects of temperature on embryonic and larval development and growth in the natterjack toad (Bufo calamita) in a semi–arid zone.— Temperature affects the duration of embryonic and larval periods in amphibians. Plasticity in time to metamorphosis is especially important in amphibian populations of Mediterranean semi–arid zones where temperatures are high and precipitation is low, increasing the rate of pond desiccation. In order to test the influence of water temperature on the larval development and growth of the natterjack toad (Bufo calamita), we collected two spawns in a semi–arid zone at Balaguer (Lleida, NE Iberian peninsula). Approximately 50 (± 10) eggs (stage 14–16) were raised in the lab at different temperature conditions: 10, 15, 20, 22.5 and 25ºC with 12:12 photoperiod. The results show a lengthening of development time with decreasing temperatures and a better survival performance of B. calamita to high temperatures. However, mean size at metamorphosis was not different across treatments, thus, suggesting that this population of B. calamita requires a minimum size to complete the metamorphosis. This study is the first approach to examine the effects that climatic factors have on the growth and development of B. calamita in semi–arid zones. Key words: Amphibians, Development, Growth, Semi–arid zone, Temperature. Resumen Efectos de la temperatura sobre el desarrollo y crecimiento de embriones y larvas en el sapo corredor (Bufo calamita) en zonas semiáridas.— La temperatura afecta la duración de los períodos embrionarios y larvarios de los anfibios. La plasticidad en el momento de la metamorfosis es especialmente importante en las poblaciones de anfibios del Mediterráneo y de zonas semiáridas donde las temperaturas son elevadas y las precipitaciones son escasas, lo que incrementa la desecación de las charcas. Con el fin de comprobar la influencia de la temperatura del agua en el desarrollo de las larvas y crecimiento de la sapo corredor (Bufo calamita), se recolectaron huevos de dos puestas procedentes de una zona semiárida en Balaguer (Lleida, NE península ibérica). Aproximadamente unos 50 (± 10), huevos (etapa 14–16) se sometieron en el laboratorio a diferentes condiciones de temperatura: 10, 15, 20, 22,5 y 25ºC con un fotoperíodo 12:12. Los resultados muestran un alargamiento del tiempo de desarrollo con la disminución de las temperaturas y una mejor supervivencia de B. calamita a temperaturas mas altas. Sin embargo, el tamaño medio de los ejemplares metamórficos no fue diferente entre los tratamientos, lo que sugiere que esta población de B. calamita requiere un tamaño mínimo corporal para completar la metamorfosis. Este trabajo es un estudio preliminar para examinar los efectos que los factores climáticos tienen en el crecimiento y el desarrollo de B. calamita en las zonas semiáridas. Palabras clave: Anfibios, Desarrollo, Crecimiento, Zonas semiáridas, Temperatura. (Received: 5 VI 07; Conditional acceptance: 24 VII 07; Final acceptance: 24 IX 07) Delfí Sanuy, Neus Oromí & Aina Galofré, Escola Tècnica Superior d’Enginyeria Agrària, Dept. de Producció Animal (Fauna Silvestre), Univ. of Lleida, Av. Rovira Roure 177, 25188 Lleida, Catalonia, Spain. Corresponding author: D. Sanuy. E–mail: dsanuy@prodan.udl.es ISSN: 1578–665X

Sanuy et al.

Introduction

Material and methods

Populations of ectotherm animals have a strong dependence on ambient temperature because they do not have an efficient mechanism for physiological thermoregulation (Brattstrom, 1963). Climatic variation is an important selective factor for life history trait differentiation, so populations of ectotherms are expected to diverge in their thermal optima for development and growth if they are exposed to different temperature environments. Amphibians have been widely used as model systems for the study of physiological ecology and temperature adaptation due to the easy manipulation of tadpoles in control experiments (Feber & Burggren, 1992). In temporary ponds, time to metamorphosis is influenced by temperature and duration of the larval stage is highly plastic, especially in semi– arid environments where rainfall and pond duration are unpredictable (Newman 1989; Tejedo & Reques, 1994). In these environments, larvae need to accelerate metamorphosis when ponds dry out and delay the process when ponds dry later in the season. When pond duration is extremely short larvae should be the most adaptive strategy. It would be to express not a plastic but a quick canalized development (Tejedo & Reques, 1994). Predation and pond desiccation have been identified as major causes of larval mortality in permanent and transient aquatic environments, respectively (Brockelman, 1969; Calef, 1973; Smith, 1983; Newman, 1987). In anuran populations, larger metamorphs may exhibit higher terrestrial survival since they can cope with different stressors such as predators and desiccation (Reques & Tejedo, 1997; Altwegg & Reyer, 2003). Smith–Gill & Berven (1979) considered that low temperatures retard differentiation more than growth and increase the stage– specific size. Therefore, larvae growing at cold temperatures have prolonged developmental periods but they may increase their size at metamorphosis. This phenomenon is considered a general rule for ectotherms (Atkinson, 1994, 1996). This trade–off in fitness, mediated by the influence of temperature, largely conditions the expression of an optimal phenotype at metamorphosis in amphibians and other aquatic organisms with complex life cycles (Etkin, 1964; Smith–Gill & Berven, 1979; Semlitsch et al., 1988; Hayes et al., 1993). In this study, we examined the influence of temperature on the development and growth of the natterjack toad (Bufo calamita). The study area is a semi–arid zone with a marked deficit of precipitation and high temperatures. Previous studies of the species in the study zone suggest that B. calamita adults (Miaud et al., 2000) presents different terrestrial behaviour with respect to other natterjack populations in other areas of Europe. In this study we focus on the response of natterjack larvae to increasing temperatures and analyze their metamorphic response.

The study area (Balaguer, 41° 46' N, 0° 46' E) is a semi–arid zone (Conesa et al., 1994) located in an agricultural setting of winter cereal fields. Mean annual temperature is about 14.5°C (January = 0.2°C and July = 32.2°C) and the mean annual rainfall is 400 mm (Balaguer meteorological station). The soil is poor and contains a high proportion of clay and lime. The evapo–transpiration is 805 mm (Thornthwaite & Mather, 1955). All these factors determine a harsh terrestrial environment with a particular flora and fauna that can tolerate such conditions (Conesa et al., 1994). As suitable breeding habitats for natterjack are temporary, tadpoles have to develop in a few days to complete the metamorphosis. We examined the effects of temperature on size and time to metamorphosis in the natterjack toad, Bufo calamita (Epidalea calamita according to Frost et al., 2006), a common amphibian species in the study area. This species breeds in seasonal ponds. Breeding activity can occur throughout the year after rainfalls, except in the colder months, with an explosive peak in the periods of more intensive rains (Sanuy, unpublished data). Two egg clutches were collected (approximately 100 eggs/spawn) in a temporal pond in the study area. At the lab where they were placed in a controlled temperature chamber (with an error of ± 0.5ºC) and immediately exposed to five different temperatures under a constant 12 hours light / 12 hours dark photoperiod. The temperature treatments were: 10, 15, 20, 22.5 and 25ºC. At the start of the experiment eggs were near Gosner stage 16 of development (14–16; Gosner, 1960). Approximately 50 eggs (± 10 eggs) from each spawn were raised in plastic recipients containing 1.3 L of dechlorinated water. Each spawn was replicated twice per experimental temperature camera. Larvae were fed fish food and the excess was removed daily. Water was changed every three days. During the experiment the stage of development was checked and photographed every 12 hours. The total body length (BL) of each larva was estimated using the program corelDRAW 11. The stage of development and BL of larvae in each sample were measured on days 1, 5 and 19 of the experiment. Stage–size was measured for each spawn at each temperature condition, at stages: 16, 25 and 46 (Gosner, 1960). Due to development time differences between individuals of the same spawn, the developmental stage was considered to have changed when 70% of larvae in the same sample had reached a particular stage. After the experiment was completed (experimental time: 150 days), the surviving larvae were returned to the pond where they were collected. The relationship between the stage of development (dependent variable) and time at each temperature and for each spawn was analysed using two–way ANOVA (PROC GLM version 9 SAS). The same type of analysis was also used to measure stage–size and the relationship between size and

Animal Biodiversity and Conservation 31.1 (2008)

45 Development stage

40 35 30 25 20 15 10 5 0

10ºC

60 Time (days)

15ºC

20ºC

100

22.5ºC

120

25ºC

Fig. 1. Effect of temperature on Bufo calamita larval development (Gosner stages; Gosner, 1960). Fig. 1. Efecto de la temperatura en el desarrollo larvario de Bufo calamita (estadios de Gosner; Gosner, 1960).

time. The significance level was set at µ = 0.05. All data are expressed as mean ± SD. Results Development time and survival. Development time increased with decreasing temperature (fig. 1). Developmental stage differed for each temperature condition (5 day: F = 71.20; p < 0.001, 19 day: F = 339.5; p < 0.001) and spawn (only in the 5 first days; F = 0.20; p < 0.001). Similarities in development were only observed between 22.5ºC and 25ºC (post hoc Tukey test, 5 day = p = 0.99, 19 day = 0.99), with Individuals in both temperatures metamorphosing in 23 days (stage 42). The coldest temperature treatment (10ºC) had a negative effect on survival: tadpoles stopped development at stage 23 (55 days), dying in 10 days. In the 15ºC treatment tadpoles stopped developing at stage 35 (90 days) and they survived without further development until the last day of the experiment. The larval period of tadpoles reared at 20ºC was on average 88 days (stage 42). Size at development stage The size increased at each development stage. We found differences in the total size between temperatures at stage 25 (fig. 2, table 1). In stage

39 tadpoles attained the maximum body size and we found differences between 20, 22.5 and 20 and 25 temperature treatments but not between 22,5 and 25ºC (table 2). However, all individuals completed the metamorphosis with a similar size (7.6 ± 1.2 mm; F = 0.08; p = 0.92) across temperature treatments. Discussion Temperature affects development and growth and is an important factor for climate selection (Berven & Gill, 1983). As expected, in our study, development time increased with decreasing temperature. Development time is very important for Bufo calamita in the study area because the breeding sites are temporary ponds with a high risk of desiccation due to high water temperatures and shallowness. Pond temperature plays a major role in determining the duration of the larval period in amphibians (Loman, 2002). Our results support other laboratory studies along these lines that have shown the effects of lowered water level on anuran development, presumably an adaptation to survival in drying ponds (Tejedo & Reques, 1994; Loman, 1999; Ryan & Winne, 2001). If pond drying increases temperature, our findings could be considered the result of drying effects. However, the analysis of effects of pond drying is complicated

Total size (mm)

Sanuy et al.

24 22 20 18 16 14 12 10 8 6 4 2 0

10ºC

15 18 21 24 27 30 Development stage 15ºC

20ºC

33 36

22,5ºC

25ºC

Fig. 2. Effect of temperature on larval size variation across developmental stages in Bufo calamita. Fig. 2. Efecto de la temperatura sobre la variación del tamaño de las larvas, a través de todas las fases de desarrollo de Bufo calamita.

Table 1. Effect of temperature on the total size at stage 25 (Gosner, 1960). Two–way factorial ANOVA. Tabla 1. Efecto de la temperatura sobre el tamaño total del estadio 25 (Gosner, 1960). ANOVA factorial bidireccional.

Source

Temperature

10.11

0.0017

Spawn

0.87

0.3710

Table 2. Differences in maximum size reached due to temperature conditions at stage 39 (Gosner, 1960): PT. Post hoc Tukey test; T. Temperaure; P. Probability. Tabla 2. Diferencias en el tamaño máximo alcanzado en la fase 39, debido a las condiciones de la temperatura (Gosner, 1960): PT. Test post hoc de Tukey; T. Temperatura; P. Probabilidad.

PT T

because this factor interacts with others, such as pond temperature and tadpole density (Loman, 2002). Other authors, studying B. calamita, did not find evidence in the response to desiccation per se, suggesting that development may differ under physiological constraints in relation to habitat types (Brady & Griffiths, 2000). Laboratory studies have shown a pattern in which tadpoles develop and grow more slowly but metamorphose with a longer body size at low temperatures (Etkin, 1964; Smith–Gill & Berven, 1979; Hayes et al., 1993). This result was not found in our study. Individuals raised at different temperatures attained metamorphosis at different times but contrarily to expected, size at metamorphosis was similar for all the treatments.

LS mean

15 vs 20

0.3746

15 vs 22.5

0.0074*

8.7792

15 vs 25

0.0024*

9.7645

20 vs 22.5

0.1201

22.5

11.2080

20 vs 25

0.0372*

11.6255

22.5 vs 25

0.8891

Therefore, higher temperature treatments determined both higher developmental rates and higher growth rates. All individuals that reached metamorphosis had the same body size. These results suggest that the population of B. calamita in the study zone requires a minimum size to complete metamorphosis.

Animal Biodiversity and Conservation 31.1 (2008)

Metabolic enzyme systems present high temperature sensitivity in an optimal range so growth and development can only proceed within a thermal window (e.g. Randall et al., 1997). The optimal temperature seems to be the higher temperatures (25 and 22.5ºC) as tadpoles reached metamorphosis in a shorter time and with larger size, thus with potential higher fitness. The results of this study do not allow us to determine higher limits of temperature tolerance for the species. The air temperatures in the study area can reach maximums of about 40ºC in summer, considerably higher than the maximum temperature used in our experiments. We cannot therefore determine a critical thermal maximum (CTM). On other hand, the minimum temperature that tadpoles needed to reach metamorphosis was 20ºC, which is a higher minimum temperature compared to the temperature tolerance in other anuran species in Europe (for example: Rana arvali Loman, 2002; Rana temporaria Laugen et al., 2003a, 2003b). Tadpoles attained a maximum size at stage 39 and decreased thereafter due to metamorphosis. The different sizes of larvae between temperatures at this stage, larger at higher temperatures, could be explained by the fact that the metabolism of growth factors is affected by temperature (Álvarez & Nicieza, 2002). Higher temperatures are well known to accelerating larval growth and development (Hayes et al., 1993). Growth rate depends on development rate, and both are functions of circulating hormone levels, which are in turn dependent upon the stage of differentiation reached. Nevertheless, growth is related to the duration of larval development (e.g. Wilbur & Collin, 1973) because conditions that are favorable for differentiation often are also favorable for growth (Smiths–Gill & Berven, 1979). In conclusion, this study represents a first step towards determining the role of climatic factors in growth and development rates that are increased in response to the time constraint. One limitation of the study is that tadpoles can actively thermoregulate by moving between shallow and deep water, a fact that was not taken into consideration in this study. Nevertheless, the results suggest that temperatures below 20ºC are too low to allow normal tadpole development and growth, while higher temperatures could favour growth and developmental conditions. In further studies it would be interesting to examine the existence of adaptive plasticity in development and growth rates in response to pond drying, as well as investigate whether a process of local adaptation is emerging in the study area. Acknowledgements We thank the Departament de Producció Vegetal i Ciència Forestal of University of Lleida, and especially Matilde Eizaguirre.

References Altwegg, R. & Reyer, H. U., 2003. Patterns of natural selection on size at metamorphosis in water frogs. Evolution, 57: 872–882. Álvarez, D. & Nicieza, G., 2002. Effects of temperature and food quality on anuran larval growth and metamorphosis. Functional Ecology, 16: 640–648. Atkinson, D., 1994. Temperature and organism size – a biological law for ectotherms? Advances in Ecological Research, 25: 1–58. – 1996. Ectotherm life–history responses to developmental temperature. Animals and Temperature. Phenotypic and Evolutionary Adaptation: 183– 204 (I. A. Johnston & A. F. Benett, Eds.). Cambridge Univ. Press. Berven, K. A. & Gill, D. E., 1983. Interpreting geographic variation in life history traits. American Zoologist., 23: 85–97. Brady, L. D. & Griffiths, R. A., 2000. Development responses to pond desiccation in tadpoles of the British anuran amphibians (Bufo bufo, B. calamita & R. temporaria). Journal of Zoology, 252: 61–69. Brattstrom, B. H., 1963. A preliminary review of thermal requirements of amphibians. Ecology, 44: 238–255. Brockelman, W. Y., 1969. An analysis of density effects and predation in Bufo americanus tadpoles. Ecology, 50: 632–644. Calef, G. W., 1973. Natural mortality of tadpoles in a population of Rana aurora. Ecology, 54: 741–758. Conesa, J. A., Mayoral, A., Pedro, J. & Recasens, J., 1994. El paisatge vegetal dels espais d’interes naturals de Lleida: area meridional. I.E.I. Diputació de Lleida. Etkin, W., 1964. Metamorphosis. In: Physiology of the Amphibia: 427–468 (J. A. Moore, Ed.). New York Academic Press, New York. Feder, M. E. & Burggren W. W., 1992. Environmental physiology of the amphibians. Chicago, London, The Univ. of Chicago Press., Brockelman. Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De Sá, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P., Drewes, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. & Wheeler, W. C., 2006. The amphibian tree of life. Bulletin of American Museum Natural. History, 297: 1–370. Gosner, K. L., 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16: 183–190. Hayes, T., Chan & Licht, P., 1993. Interactions of temperature and steroid on larval growth, development, and metamorphosis in a toad (Bufo boreas). Journal of Experimental Zoology, 299: 206–215. Laugen, A. T., Laurila, A. & Merilä, J., 2003a. Latitudinal and temperature dependent variation in embryonic development and growth in Rana temporaria. Oecologia, 135: 548–554.

Laugen, A. T., Laurila, A., Räsänen, K. & Merilä, J., 2003b. Latitudinal countergradient variation in the common frog (Rana temporaria) development rates–evidence for local adaptation. Journal of Evolutionary Biology, 16: 996–1005. Loman, J., 1999. Early metamorphosis in common frog Rana temporaria tadpoles at risk of drying: an experimental demonstration. Amphibia.–Reptilia, 20: 421–430. – 2002. Temperature, genetic and hydroperiod effects on metamorphosis of brown frogs Rana arvalis and R. temporaria in the field. Journal of Zoology, 258: 115–129. Miaud, C., Sanuy, D. & Avrillier, J. N., 2000. Terrestrial movements of natterjack toad Bufo calamita (Amphibia, Anura) in semi–arid, agricultural landscape. Amphibia–Reptilia, 21: 357–144. Newman, R. A., 1987. Effects of density and predation on Scaphiopus couchii tadpoles in desert ponds. Oecologia, 71: 301–307. – 1989. Developmental plasticity of Scaphiopus couchii tadpoles in an unpredictable environment. Ecology, 70: 1775–1787. Randall, D., Burggren, W. & French, K., 1997. Eckert Animal Physiology: Mechanisms and Adaptations. W. H. Freeman and Go., New York. Reques, R. & Tejedo, M., 1997. Reaction norms for

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metamorphic traits in natterjack toads to larval density and pond duration. Journal of Evolutionary Biology, 10: 829–851. Ryan, T. J. & Winne, C. T., 2001. Effects of hydroperiod on metamorphosis in Rana sphenocephala. American Midlands Naturalist, 145: 46–53. Semlitsch, R. D., Scott, D. E. & Pechmann J. H. K., 1988. Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology, 69: 184–192. Smith, D. C., 1983. Factors controlling tadpole populations of the chorus frog (Pseudacris triseriata) on Isle Royale, Michigan. Ecology, 64: 501–510. Smith–Gill, S. J. & Berven, K. A., 1979. Predicting amphibian metamorphosis. American Naturalist, 113: 563–585. Tejedo, M. & Reques, R., 1994. Plasticity in metamorphic traits of natterjack tadpoles: the iteractive effects of density and pond duration. Oikos, 71: 295–304. Thornthwaite, C. W. & Mather, J. R., 1955.The water balance. Climatology, 8: 1–104. Wilbur, H. M. & Collins, J. P., 1973. Ecological aspects of amphibian metamorphosis. Science, 182: 1305–1314.

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Monitoring programs to assess reintroduction efforts: a critical component in recovery E. Muths & V. Dreitz

Muths, E. & Dreitz, V., 2008. Monitoring programs to assess reintroduction efforts: a critical component in recovery. Animal Biodiversity and Conservation, 31.1: 47–56. Abstract Monitoring programs to assess reintroduction efforts: a critical component in recovery.— Reintroduction is a powerful tool in our conservation toolbox. However, the necessary follow–up, i.e. long–term monitoring, is not commonplace and if instituted may lack rigor. We contend that valid monitoring is possible, even with sparse data. We present a means to monitor based on demographic data and a projection model using the Wyoming toad (Bufo baxteri) as an example. Using an iterative process, existing data is built upon gradually such that demographic estimates and subsequent inferences increase in reliability. Reintroduction and defensible monitoring may become increasingly relevant as the outlook for amphibians, especially in tropical regions, continues to deteriorate and emergency collection, captive breeding, and reintroduction become necessary. Rigorous use of appropriate modeling and an adaptive approach can validate the use of reintroduction and substantially increase its value to recovery programs. Key words: Reintroduction, Monitoring, Adaptive processes, Amphibians, Bufo baxteri. Resumen Programas de seguimiento para evaluar los esfuerzos de reintroducción: un componente crítico en la recuperación.— La reintroducción es un utensilio muy potente en nuestra caja de herramientas conservacionista. No obstante, el seguimiento necesario, es decir, el seguimiento a largo plazo, no es un hecho común, y si se da, puede ser poco rigurosa. Sostenemos que el seguimiento válido es posible, incluso cuando los datos son escasos o están dispersos. Presentamos aquí un medio de seguimiento basado en datos demográficos y un modelo de proyección utilizando al sapo de Wyoming (Bufo baxteri) como ejemplo. Usando un proceso repetitivo, se trabajan gradualmente los datos existentes de tal forma que aumente la fiabilidad de las estimas demográficas y sus subsecuentes deducciones. La reintroducción y el seguimiento defendible pueden hacerse cada vez más importantes, dada la problemática de los anfibios, especialmente en las regiones tropicales, donde continua deteriorándose, y se hacen necesarias la captura y la cría en cautividad para la reintroducción posterior. Un uso riguroso de la construcción de modelos apropiada y un punto de vista adaptativo pueden hacer válido el uso de la reintroducción y aumentar sustancialmente su valor en los programas de recuperación. Palabras clave: Reintroducción, Seguimiento, Procesos adaptativos, Anfibios, Bufo baxteri. (Received 30 VII 07; Conditional acceptance: 13 IX 07; Final acceptance: 16 X 07) Erin Muths, U. S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Bldg C, Fort Collins, Colorado 80526–8118, U.S.A.– Victoria Dreitz, Colorado State Univ., Colorado Natural Heritage Program, 8002 Campus Delivery, Fort Collins, Colorado 80523, U.S.A. Corresponding author: E. Muths. E–mail: erin_muths@usgs.gov Current address of V. Dreitz: Colorado Division of Wildlife, 317 W. Prospect Road, Fort Collins, Colorado 80526, U.S.A. E–mail: Victoria.Dreitz@state.co.us ISSN: 1578–665X

Introduction Species reintroductions have become an increasingly popular tool in wildlife management (Wolf et al., 1996; Stanley–Price, 1991; Griffith et al., 1989; Kleiman, 1989). Reintroductions were used initially to resolve human–animal conflicts, to augment game populations, and to establish populations of non– native species but as more species have become imperiled and required more intensive management, this tool has become an integral part of many endangered species programs (Fischer & Lindemayer, 2000; Griffith et al., 1989). As habitat fragmentation increases (Noss et al., 2006) and the effects of global climate change become more evident (e.g. Knowles et al., 2006), reintroductions are likely to become an increasingly important tool for maintenance of demographically and genetically viable populations (Bright & Morris, 1994; Griffith et al., 1989). This may be increasingly true for amphibian species given the current outlook especially in the tropics (e.g., Stuart et al., 2004). Importantly, long–term monitoring, which is rarely implemented, is a necessary follow–up to such programs (Dodd, 2005). We contend that monitoring is possible, even with sparse data. Using an iterative process, a data–poor project can evolve, such that each iteration produces more reliable data. Rigorous use of sound field methods, appropriate modeling, parameter estimation, and an adaptive approach can validate the use of reintroduction and substantially increase its value to recovery programs. Background Reintroduction programs for threatened and endangered species have various goals, including augmentation of population numbers, introduction of satellite populations to reduce risk of species extirpation, movement from a negatively impacted site to a mitigation site, or repatriation following extirpation by anthropogenic or natural causes. The overarching goal is to have a self–sustaining population of the target species at the site in perpetuity. There are a number of terms used for the movement of animals (by humans) from one place to another including translocation, introduction, supplementation, relocation, repatriation, and reintroduction; we use reintroduction throughout in the broadest sense. Some reintroduction programs have been successful, such as those for natterjack toad (Bufo calamita), black–footed ferret (Mustela nigripes) and peregrine falcon (Falco peregrinus anatum) (Denton et al., 1997; Stanley–Price, 1991; Cade & Weaver, 1983), but many reintroduction programs fail (Seigel & Dodd, 2002; Griffith et al., 1989). Reintroductions are fraught with challenge; reasons for failure vary and are attributable to a range of factors (Snyder et al., 1996; Short & Smith, 1994; Kleiman, 1989). Monitoring is often the most challenging portion of a reintroduction program because of the perceived

Muths & Dreitz

costs, but it is arguably the most critical. Boersma, et al. (2001) state, "one cannot possibly know whether management is working and whether it needs to be adaptively altered unless its effects are monitored". Gauging success Based on the goal of a viable population after reintroduction (Caughley & Gunn, 1996), the success of a program should be measured not only by the successful release of individuals, but by the ability of those animals to reproduce successfully and create a self–sustaining population (Dodd, 2005). Monitoring efforts can provide an assessment of program efficacy (Semlitsch, 2002) as well as a feedback mechanism among all aspects of recovery (e.g. captive breeding, habitat restoration) in an adaptive management framework (Bar–David et al., 2005). In some cases gauging success must be done in small increments. Adequate data may not be available in the short term to evaluate the entire program or make completely informed decisions. In spite of this, an iterative, yet quantitative approach will yield a more reliable assessment of the program in the long run. Monitoring–considerations Factors that contribute to the success or failure of reintroductions are estimated through the dynamics of the population (e.g. reproduction, dispersal, survival) but these data usually do not exist (Bar–David et al., 2005). In many cases where reintroduction is considered it is nearly impossible to collect these data because the population of interest has very few adult animals left, is restricted to a single location, is infected by disease, or is otherwise compromised (Dodd, 2005). For example, long–term data from amphibian populations are rare (but see, e.g., Daszak et al., 2005, Whitfield et al., 2007) and amphibian species, about which very little is known, are being lost at an unprecedented rate. In spite of these obstacles, simulations or traditional prospective power analyses can be conducted to produce a target sample size; that is, the number of reintroduced individuals needed to reliably estimate parameters of interest. Reasonable sample size targets can be based on an array of data: studies of natural populations of the species, empirical data on a similar species, biological insight from experts, or captive colonies. A priori sample size calculations are used in other types of biological studies (Eng, 2004), and should not be overlooked when implementing reintroduction programs. Traditional power analyses are often used to calculate sample sizes for experiments, but efforts to relocate are seldom purely experimental and changes in study design can invalidate power analyses (Eng, 2004). One alternative to power analyses is simulations. Another critical issue in monitoring is spatial variation and detectability (Pollock et al., 2002).

Animal Biodiversity and Conservation 31.1 (2008)

For example, few, if any, species are so conspicuous that they are always detected during field surveys when present (MacKenzie et al., 2004). Some monitored reintroductions of birds and mammals include an estimation of detection rate (e.g., Ostermann et al., 2001; Bar–David et al., 2005), but we know of no monitored reintroduction programs for amphibians that estimate detection rate or attempt to remove the effects of incomplete detectability. Assuming that count data represents population size in order to extract information on other demographic parameters such as survival and reproduction can lead to erroneous conclusions (Williams et al., 2002). Given these concerns, more rigorous attention to the adequacy and appropriateness of monitoring and sufficient documentation of the process is necessary (Mazerolle, 2006; Maunder, 1992; Oldham et al., 1991). Material and methods The Wyoming toad The Wyoming toad was first recorded in Wyoming in 1946 as the Canadian toad, Bufo hemiophrys (Baxter, 1947). Porter (1968) recognized the Wyoming populations as a distinct subspecies, (B. h. baxteri), and Smith et al. (1998) elevated these populations to the species level as B. baxteri. From their discovery to about 1970, Wyoming toads were considered common and abundant within their restricted range (Baxter & Stone, 1985). Rapid declines in the 1970s presaged the extinction of Wyoming toads in the wild. The Wyoming toad was listed as an endangered species in 1984 (USFWS, 1984) and is suggested to be one of the most endangered amphibians in North America (Odum & Corn, 2005). The proximate cause of decline in Wyoming toads is likely infection by the fungus Batrachochytrium dendrobatidis (Bd) with the resulting chytridiomycosis causing unsustainable mortality of adult toads (Odum & Corn, 2005). Other factors, such as pesticides, predation, or habitat alteration, have been proposed to contribute to the decline of this species, but little evidence supports these hypotheses (Odum & Corn, 2005). Currently, the Wyoming toad population is not self–sustaining and relies on annual supplementation with captive–reared animals (Odum & Corn, 2005). Between 1995 and 1999, over 9,500 Wyoming toads, mainly post–metamorphs (< 4 mos.) were reintroduced at Mortenson Lake National Wildlife Refuge (MLNWR, Albany County, Wyoming) where Wyoming toads were last known to occur in the wild (Odum &Corn, 2005). MLNWR is the site of recent reintroduction efforts (Jennings et al., 2001) and is described elsewhere (Parker & Anderson, 2003). Except for photographic capture–recapture work from 1990 to 1992 (Odum & Corn, 2005) and the release and monitoring study in 2002 (this study), monitoring of reintroduction efforts are limited to

visual encounter surveys (i.e., individual counts) during early spring and/or fall in a given year (Jennings et al., 2001). The individuals conducting the survey are mostly volunteers with varying experience in locating Wyoming toads. The bi–annual survey entails workers walking around the lakeshore in the putative preferred habitat (saturated soils) of Wyoming toads and counting the number of individuals encountered. These individual counts enumerate toads observed by life history stage; young– of–year, juveniles (1 yr old), and adults. Toads are not handled and no attempt is made to determine if a toad was previously counted during the survey (Dreitz, 2006). Study design The goal of this project was to determine whether or not a reintroduction and long–term monitoring program was feasible for the Wyoming toad. The project was financially constrained to a single field season. To address the goal, we needed to determine 1) the feasibility of releasing, recapturing and monitoring post–metamorphic toads and 2) the efficacy of sparse data in building a model that would yield useful information (e.g. how many individuals to release and survival estimates). Captive propagation of Wyoming toads has been successful (Jennings et al., 2001) so that locating a source population was not an issue. A priori simulations were conducted using the robust design framework (Pollock, 1982) and information based on the biology of the Wyoming toad and other bufonids (e.g. Odum & Corn, 2005). We used a conservative scenario to set survival and capture probability. Field sampling: marking and capture All post–metamorphs released in 2002 were marked by clipping the 2nd digit on the left forefoot. Post–metamorphs were held in captivity at least one additional day after marking then released at MLNWR. Captive rearing facilities included Saratoga National Fish Hatchery, Wyoming Game and Fish Department’s Sybille Wildlife Research Center and the Detroit Zoological Association. Post–metamorphic toads were staged and marked at the Saratoga Hatchery and the Sybille Research Center in Wyoming. The potential for disease was monitored at these facilities but individual animals were not tested prior to release. The release location was not tested for the presence of Bd because methods for testing water for this fungus were not yet available. We allowed at least one week acclimation period after release before initiating field sampling. An 82–section grid was established around Mortenson Lake. Each grid cell was approximately 25 m x 25 m, and extended from waters edge out towards upland habitat. Time–constrained (20 minute) visual encounter surveys (Crump & Scott, 1994) were conducted

Muths & Dreitz

in every third cell around the lake (= 28 cells) by trained surveyors. All equipment, including waders, was disinfected with bleach daily. The robust design (Pollock, 1982; Kendall et al., 1995, 1997) includes k primary sampling periods, each with li secondary sampling periods. Primary sampling periods are separated from each other by sufficient time to expect gains (birth and immigration) and losses (death and emigration), that is, the population is "open" to demographic and geographic changes. Further, each primary period includes li secondary periods separated from each other by sufficiently short time intervals for the population to be effectively "closed" to gains and losses (sensu Kendall et al., 1995). In our case, selected cells were sampled on 3 consecutive days (= secondary periods) in each of the summer months (June, July, and August = primary periods). Primary periods were approximately 4 weeks apart. For each survey occasion, a team of two observers was assigned to cells such that no team surveyed the same cells during the 3–day session. All toads observed were captured. At the conclusion of the 20 minute search, toads were inspected for marks. Additional toes were clipped to give each captured individual a unique number (Martof, 1953). Toads were released at the site of capture.

parameters followed Pollock et al. (1990), Lebreton et al. (1992), and Burnham & Anderson (2002). We first developed a list of covariates likely to influence one or more of the parameters, and developed a set of candidate models. We modeled over–summer survival as constant ( .) or varying between the primary sampling periods ( t). We assumed that there was no temporary emigration (i.e. '' = i' = 0), and set initial capture probability equal i to recapture probability (pij= cij, hereafter capture probability). We considered three different effects on capture probabilities: observers, micro–habitat within cells, and mean air temperature during secondary surveys compiled from data collected at the Laramie Regional Airport. The observers (obs) effect was based on probable variability in the abilities of survey teams to observe and capture post– metamorphs. The effect of cell in the survey grid (cell) was included because it is likely that the number of post–metamorphs in a cell varies due to micro–habitat differences among cells. The air temperature (temp) effect was based on amphibian physiology. We assumed that, to a point, post– metamorphs would be more active at warmer temperatures.

Analysis: robust design

Model selection and inference was based on information–theoretic methods using the small sample size correction to Akaike’s Information Criterion, AICc (Hurvich & Tsai, 1989; Burnham & Anderson, 2002). We did not correct for extra binomial variation because there is currently no standard approach to estimate this in the robust design model (Williams et al., 2002). Once AIC c values were computed for each model, we ranked the models based on the relative distances, DAICc, between the best approximating model and competing models. Normalized Akaike weights (wi), which provide a strength of evidence for each model, were then computed (Burnham & Anderson, 2002). Instead of using parameter estimates from a single "best" model, we model averaged parameter estimates across all models (Burnham & Anderson, 2002).

We used the robust design to estimate apparent over–summer survival of post–metamorphic Wyoming toads. The robust design incorporates features of both the open and closed mark–release– recapture models (see above), with the major advantage of being able to estimate survival and population size in a single study. Information from secondary periods is used to estimate conditional capture (pij) and recapture (cij) probabilities and the number of animals in the population (Ni). Our ability to detect an individual was measured by capture and recapture probabilities. The pooled capture probabilities for each primary period are used to estimate apparent survival (the product of true survival and fidelity; [ 1,..., 1k–1]). Recently metamorphosed individuals are unlikely to leave the sampling area until they hibernate for the winter (Odum & Corn, 2005). The assumptions of the robust design are summarized by Kendall et al. (1995) and are similar to assumptions of other capture–recapture models. Over–summer survival (of released post–metamorphic Wyoming toads) rather than population size, was our primary objective. We used an extension of the robust design, the Huggins estimator, which removes the estimates of population size from the likelihood and allows capture and recapture probabilities to be modeled as functions of individual covariates (Huggins, 1991, 1989). Population size, if needed, can be derived. Additional releases of captive bred post– metamorphs occurred between the primary periods. Our approach to modeling the demographic

Model selection criteria and parameter estimation

Population projection model The minimum number of animals to release to meet a recovery goal of a pre–defined number of breeding females is a common question for many recovery teams. To illustrate the potential of our approach in a reintroduction and monitoring program, we built a projection model based on a hypothetical target of 150 females. Using this value, the projection model provides the number of releases necessary over a 5 year period to reach that target. Projection models (e.g. Caswell, 2001) are flexible, such that a variety of parameters can be estimated or set to a target value. The number of adult females at a given time t, NAt, is calculated as:

Animal Biodiversity and Conservation 31.1 (2008)

Table 1. Number of captures and air temperatures (from Laramie Regional Airport) during each secondary survey at MLNWR in 2002. Tabla 1. Número de capturas y temperaturas del aire (del aeropuerto regional de Laramie) durante cada transecto secundario en el MLNWR en 2002.

Primary periods June Secondary surveys

July

August

June

July

August

Air temperatures (oC)

Captures

Day 1

19.4

17.1

15.8

Day 2

19.9

19.8

15.4

Day 3

20.7

15.8

13.6

NAt

NAt–1 SA + (NJt–1

JdA

where NJt is the number juveniles in the population at time t; SA is the probability of an adult surviving from time t to t+1; J d A is the probability a juvenile becoming an adult from time t to t+1; and r is the sex ratio of males to females in the adult population. And the number of juveniles in the population is: NJt = NJt–1 SJ (1 –

) + NAFASESPost + ISPost JdA

where SJ is the probability of a juvenile surviving at time t; SPost is the probability of a post–metamorph surviving; SE is the probability of an egg surviving to metamorphosis; FA is the fecundity of adult females in the population per year (defined as the number of reproducing females that a single female produces in one year); and I is the number of post– metamorphs released into the population per year. We used an optimization routine to get the least– sum–of–squares estimate for I. Any projection model needs information on population dynamics (i.e., survival, reproduction) and like many reintroduced species, information on the demography of Wyoming toads is limited (Jennings et al., 2001). We used values from a hypothetical life table (P. S. Corn, unpublished data) for our projection model including: SA = 0.20, SJ = 0.57, SE = 0.10, and r = 0.5. The values J d A = 0.19 and FA = 2 were based on information from herpetologists who have worked on Wyoming toads over the last 20 years (P. S. Corn, E. Muths). Results Releases Between June and August 2002, 8,124 post–metamorphic Wyoming toads were released with 74% released prior to the June sampling. We captured 459 post–metamorphs during field sampling; most

captures occurred in July with the fewest in August (table 1). None of the captured animals showed signs of disease and none were found dead. Air temperatures ranged from 13.6 to 20.7 o C (18.4 ± 1.9oC, mean ± SD), with June the warmest and August noticeably cooler (table 1). Model results The data were best explained by the model with constant over–summer survival and time–varying capture probabilities. Time variation in over–summer survival and capture probabilities was also a competitive model (table 2). The model–averaged estimate of the over–summer survival of post– metaphoric Wyoming toads was 0. 21 (table 3). The model–averaged estimate of the capture probabilities for the August primary period was low, 0.01, while June and July were somewhat higher, 0.09 and 0.07, respectively (table 3). Estimates of the number of post–metamorphs in the study area ranged from 594 to 1,304. Estimates for August were imprecise as a result of the low number of individuals captured. Population projection model The projection model predicted that a minimum of 5,000 post–metamorph releases each year are necessary to achieve our hypothetical goal of 150 adult females in the population after 5 years of releases. Discussion We determined that relocating post–metamorphic Wyoming toads is feasible. Our over–summer survival rate (0.21) was greater than our worst–case scenario expectation (0.10), but our capture rate (0.08) was substantially lower than our worst–case scenario expectation (0.15). While the capture probability during the last session was likely compro-

Muths & Dreitz

Table 2. Summary of model selection results for released post–metamorphic Wyoming toads at MLNWR in 2002 with models ranked by ascending DAICc. Tabla 2. Resumen de los resultados de la selección de modelos para las sueltas post–metamórficas de los sapos de Wyoming en el MLNWR en 2002, con los modelos ordenados según una CIAc ascendente.

Model

Deviance

AICc

'' = '' = 0 pt = ct

1235.9364

1254.3311

0.0000

0.7038

'' = '' = 0 pt = ct

1235.5861

1256.0696

1.7385

0.2951

'' = '' = 0 ptemp*t = ctemp*t

1261.4109

1267.4628

13.1317

0.0010

'' = '' = 0 ptemp*t = ctemp*t

1267.7440

1271.7699

17.4388

0.0001

'' = '' = 0 pobs+t = cobs+t

1223.7014

1276.6560

22.3249

0.0000

1223.6667

1278.8649

24.5338

0.0000

'' = '' = 0 pcell*t = ccell*t

1396.7434

1417.2269

162.8958

0.0000

'' = '' = 0 pcell*t = ccell*t

1407.1175

1425.5122

171.1811

0.0000

t t ·

'' =

'' = 0 pobs+t = cobs+t

Table 3. Modeled average results for oversummer survival and capture probabilities: Pm. Parameter; SE. Standard error; CI. 95% confidence interval. Tabla 3. Resultados promedio modelados para la supervivencia pasado el verano y para las probabilidades de captura: Pm. Parámetro; SE. Error estándar; CI: Intérvalo de confianza del 95%.

Estimate

Lower

Upper

0.2095

0.0884 0.0852 0.4302

p1. = c1.

0.0880

0.0246 0.0503 0.1495

p2. = c2.

0.0716

0.0183 0.0430

p3. = c3.

0.0080

0.0091 –0.0098 0.0257

0.1168

mised by cool weather, animals should have been larger and therefore easier to see. We do not expect metamorphic toads to emigrate at this time of the year (before hibernation, Parker & Anderson, 2003), therefore, the very low number of captures suggests high mortality between July and August. We cannot attribute mortality to Bd. There were no adult animals or carcasses from released animals to test for Bd. At the time of this study assays to test the environment (e.g. water, Kirshtein et al., 2007) were unavailable. Carey et al. (2006) report that duration of exposure and dosage influence

survival in boreal toads (Bufo boreas) and predict that there is a threshold level of infection that must be reached to cause death. Since our released animals came from Bd–free facilities and there was minimal opportunity for contact with other amphibians, it is unlikely that the threshold levels of Bd, if it was present, were met, at least within the short time–frame of this study. Capture probability is important as it is tied closely to the precision of the population size estimate (White et al., 1982). It is critical to increase capture rate by increasing the number of secondary periods and / or by increasing the number of primary periods (likely to increase precision). Effort (number of observers or search time per cell) could also be increased. Based only on technician costs, the cost of one season of monitoring was minimal. Technicians were a combination of students paid at an hourly wage, volunteers, and staff from various participating agencies. Depending on the source of technicians, increasing the number of secondary surveys should not be prohibitive. Projection models can evaluate an array of parameters, with a great deal of flexibility in the equations. These models can assist in evaluating the overall performance of a population and, importantly, recovery program success relative to predetermined criteria (e.g. Caswell, 2001). Such models (i.e. Population viability analyses) have been applied to Wyoming toads (Program VORTEX, Jennings et al., 2001). Our projection model has the small advantage of using additional data (this study) that was unavailable when Program VORTEX was applied to the Wyoming toad data, and illustrates the incremental nature of collecting information on critically endangered species. The demographic estimates we used were the only ones available; they are prelimi-

Animal Biodiversity and Conservation 31.1 (2008)

Estimates of the number of post–metamorphic toads

3,000 2,500 2,000 1,500 1,000 500 0

June

July

August

Fig. 1. Estimates of the number of post–metamorphic toads present at MLNWR. Fig. 1. Estimas del número de sapos post–metamórficos presentes en el MLNWR.

nary at best, with some data based on estimates made when the population was likely stressed by disease. In addition, our simple projection model was based on an assumption of constancy over time due to the limited data available, which is most likely not the case in most amphibian reproductive scenarios. Stochatiscity and density dependence are important considerations that can be added to the model as more data accumulate. While the results of our projection model should be viewed with caution, they are based on biologically authentic information and illustrate the functionality of such a model in our iterative and adaptive framework. There are a number of definitions of adaptive management. We use Salafsky et al. (2001) and Margoluis & Salafsky (1998) who define adaptive management as the incorporation of research into conservation action. We advocate such a process and submit that our preliminary monitoring lays the foundation for using such an approach on Wyoming toad reintroduction. Our estimates and projection model results are clearly the first iteration of what should be a long–term release and monitoring program. With each year, methods can be refined as the precision and accuracy of the data improve. For example, the over–summer survival rate can be used in the projection model to more reliably examine a suite of parameters that may be of interest to the project, specifically the number of animals to be released (as we calculated above), the number of adult females expected to survive and reproduce with a certain number of releases, or in sensitivity/ elasticity analyses. Although our projections were based on over–summer survival rather than the more informative annual survival probability, it is still an improvement over guesses alone and, if the

animals do not survive over–summer, it is clear that they will not survive until the next summer. As more data become available, a more detailed approach to adaptive resource management (e.g. Holling, 1978) could be applied where an explicit objective is defined, specific models are developed and assessed, and the results applied in determining the best conservation action to take. Reintroduction is an important component of conservation biology (Wolf et al., 1996; Griffith et al., 1989) although our ability to project the outcome of reintroduction programs, and to plan accordingly, is still limited (Dodd, 2005; Kleiman, 1989). The point we make is not a new one: Reintroductions, to be of any long–term use, must be monitored. We have shown that rigorous monitoring is possible if defensible information is gathered, built upon, and used to monitor the release of post–metamorphic Wyoming toads. By using appropriate simulations for initial sample size decisions, modeling to estimate parameter values, an AIC–based decision criterion to evaluate competing models, and a projection model to provide information for the next iteration of releases and monitoring, the approach is straightforward and adaptive. Basing a program on defensible methods allows managers to respond relatively quickly to modeled data that provide valuable inferences about biological changes in the system. Interestingly, more traditional metrics, such as indices that do not provide the opportunity to improve estimation efforts or to address changing circumstances, appear to be used more often in herpetology than for other taxa (Mazerolle, 2006, but see, for example; Scherer et al., 2005; Bailey et al., 2004a, 2004b). While our example is applicable

to a broad range of taxa and endangered species programs, it may be especially pertinent to amphibians. The current outlook for amphibians, especially those in tropical regions, is grim (Mendelson et al., 2006; Stuart et al., 2004), and drastic measures, such as collecting the remaining animals from the wild and using captive breeding programs have been advocated (Mendelson & Rabb, 2005). If amphibian declines continue at their current alarming rate (e.g., Mendelson et al., 2006; Lannoo, 2005) and large scale "ark" projects (Mendelson & Rabb, 2005) are used, the implementation of reintroduction projects that are accountable and amenable to adaptation will be pivotal. Acknowledgements Thanks to R. Beiswenger and P. S. Corn for discussions about the Wyoming toad. L. Bailey and K. R. Wilson provided helpful comments on earlier drafts of the manuscript. The research described herein was approved by the U. S. Geological Survey Animal Care and Use Committee and partially funded by the U. S. Fish and Wildlife Service. References Bailey, L. L., Kendall, W. L., Church, D. R. & Wilbur, H. M., 2004a. Estimating survival and breeding probability for pond–breeding amphibians: a modified robust design. Ecology, 8: 2456–2466. Bailey, L. L., Simons, T. R. & Pollock, K. H., 2004b. Estimating site occupancy and species detection probability parameters for terrestrial salamanders. Ecological Applications, 14: 692–702. Bar–David, S., Saltz, D., Dayan, T., Perelberg, A. & Dolev, A., 2005. Demographic models and reality in reintroductions: Persian fallow deer in Israel. Conservation Biology, 19: 131–138. Baxter, G. T., 1947. The amphibians and reptiles of Wyoming. Wyoming Wildlife, 11: 30–34. Baxter, G. T. & Stone, M. D., 1985. Amphibians and reptiles of Wyoming. Wyoming Game and Fish Department, Second Edition, Cheyenne, Wyoming, U.S.A. Boersma, P. D., Kareiva, P., Fagan, W. F., Clar, J. A. & Hoekstra, J. M., 2001. How good are endangered species recovery plans? BioScience, 51: 643–649. Bright, P. W. & Morris, P. A., 1994. Animal translocation for conservation: Performance of dormice in relation to release methods, origin, and season. Journal of Applied Ecology, 31: 699–708. Burnham, K. P. & Anderson, D. R., 2002. Model selection and multimodel inference: a practical information–theoretic approach. Second edition. Springer–Verlag, New York, NY, U.S.A. Cade, T. J. & Weaver, J. D., 1983. Falcon propagation: a manual on captive breeding: The Peregrine Fund, Ithaca, NY.

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Descripción de un nuevo limácido de Menorca (Islas Baleares): Gigantomilax (Vitrinoides) benjaminus sp. n. (Gastropoda, Pulmonata)

V. Borredà & A. Martínez–Ortí

Borredà, V. & Martínez–Ortí, A., 2008. Descripción de un nuevo limácido de Menorca (Islas Baleares): Gigantomilax (Vitrinoides) benjaminus sp. n. (Gastropoda, Pulmonata). Animal Biodiversity and Conservation, 31.1: 57–66. Abstract Description of a new limacid slug in Menorca (Balearic Islands, Spain) Gigantomilax (Vitrinoides) benjaminus n. sp. (Gastropoda, Pulmonata).— We describe a new endemic limacid slug, Gigantomilax (Vitrinoides) benjaminus n. sp. and we compare it with the nearest species, particularly with Gigantomilax (V.) majoricensis, another Balearic endemism. Characteristic features of this new species include its small size, translucid and smooth body, and totally grey dorsum with no bands or spots. The reproductive system shows a well developed vas deferens surrounded by the distal part of prostatic gland, a thin penial retractor muscle, swollen prostate and small distal genitalia. The recent redescription of Limax majoricensis by Wiktor et al. (2007) is discussed and we consider that these authors refer to G. benjaminus n. sp., and so we dessign the neotype of Gigantomilax (V.) majoricensis. Key words: Molluscs, Limacidae, Gigantomilax (Vitrinoides) benjaminus n. sp., Limax majoricensis, Minorca, Balearic Islands, Spain. Resumen Descripción de un nuevo limácido de Menorca (Islas Baleares): Gigantomilax (Vitrinoides) benjaminus sp. n. (Gastropoda, Pulmonata).— A partir de material recolectado en la isla de Menorca se describe una nueva babosa endémica de esta isla, Gigantomilax (Vitrinoides) benjaminus sp. n. y se compara con las especies más cercanas, en especial con el otro limácido endémico balear Gigantomilax (V.) majoricensis. Los caracteres más destacables son su pequeño tamaño y el tono gris uniforme sin bandas, manchas ni reticulado de su translúcida parte dorsal, y en el aparato reproductor la presencia de un bien desarrollado vaso deferente rodeado por la parte distal de la glándula prostática y la existencia de un delgado músculo retractor del pene, el aspecto hinchado de la próstata así como el reducido tamaño de la genitalia distal. Se discute la redescripción de Limax majoricensis recientemente publicada por Wiktor et al. (2007), que consideramos se refiere a G. benjaminus sp. n., por lo que designamos un neotipo de Gigantomilax (V.) majoricensis. Palabras clave: Molusco, Limacidae, Gigantomilax (Vitrinoides) benjaminus sp. n., Limax majoricensis, Menorca, Islas Baleares, España. (Received: 7 IX 07; Conditional acceptance: 12 XII 07; Final acceptance: 9 I 08) Vicent Borredà & Alberto Martínez–Ortí, Dept. de Zoologia, Fac. de Biologia, Univ. de València, Av. Dr. Moliner 50, 46100 Burjassot, València, España (Spain) y Museu Valencià d’Història Natural, Passeig de la Petxina 15, 46008 Valencia, España (Spain). Corresponding author: A. Martínez–Ortí. E–mail: alberto.martínez@uv.es

ISSN: 1578–665X

Introducción Se describe un nuevo limácido, Gigantomilax (Vitrinoides) benjaminus sp. n., procedente de la isla de Menorca (Islas Baleares), continuando así con nuestros estudios sobre el conocimiento de la diversidad malacológica española (Borredà, 1996; Martínez–Ortí, 1999, entre otros). Se detalla y figura su morfología externa, limacela, aparato reproductor, rádula y mandíbula y se compara con las especies más cercanas de los géneros Gigantomilax Boettger, 1883, Limax Linnaeus, 1758 y Lehmannia Heynemann, 1863. Hasta ahora el único limácido endémico balear conocido era Limax majoricensis Heynemann, 1862. Numerosos autores han hecho referencia a esta especie con distintas denominaciones genéricas y subgenéricas: Hidalgo (1875, 1879, 1916, 1918) en diversos estudios faunísticos sobre la malacofauna española cita L. majoricensis. Hesse (1926) sitúa a L. majoricensis en el subgénero Malacolimax. Waldén (1961) en un trabajo sobre Lehmannia valentiana (Férussac, 1821), se refiere a la especie balear como Limax cf. majoricensis. Jaeckel & Plate (1964) incluyen L. majoricensis entre los moluscos de Baleares. Gasull & Van Regteren Altena (1969) recolectan y citan L. majoricensis en varias localidades de Mallorca, Ibiza y Formentera, pero no de Menorca. Paul (1982) vuelve a nombrar L. majoricensis en la malacofauna balear. Gasull (1984) en su estudio sobre los gasterópodos de las Pitiusas comenta que L. majoricensis no se encuentra en Menorca. Castillejo & Rodríguez (1991) recogen las citas de L. majoricensis de los autores anteriores, todas ellas de Mallorca y las Pitiusas, sin ninguna otra información adicional. Castillejo & Garrido (1994, 1996) realizan un exhaustivo estudio morfo–anatómico de L. majoricensis por primera vez, a partir de material preservado procedente del Museo de Historia Natural de Göteborg (Suecia) consistente en los ejemplares recolectados por Gasull y Montaner en los años 60 del pasado siglo en Mallorca e Ibiza y de otro material procedente del Swedish Museum of Natural History de Estocolmo, recolectado por F. Söderlund en 1870 y 1871 en Ibiza y Formentera. Los incluyen en el subgénero Limacus Lehmann, 1864, al comprobar la existencia de ciego rectal. Además, y sin dar ninguna explicación, sugieren que probablemente la especie se encuentre también en Menorca. Anderson (2004) cita Lehmannia sp. de Menorca, concretamente del Barranc d’Algendar. Recientemente, Wiktor et al. (2007) redescriben Limax majoricensis Heynemann, 1862 reasignándola al género Gigantomilax, subgénero Vitrinoides Simroth, 1891, y designan un neotipo de esta especie procedente de Menorca, también del Barranc d’Algendar. En el presente estudio se discute esta adscripción específica del taxon menorquín y se muestra información suficiente para afirmar que éste, Gigantomilax benjaminus sp. n., presenta claras di-

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ferencias morfo–anatómicas con G. majoricensis, que habita en el resto de las islas Baleares, de acuerdo con los datos de recolección actuales. Resultados Familia Limacidae Rafinesque, 1815 Género Gigantomilax Boettger, 1883 Subgénero Vitrinoides Simroth, 1891 Gigantomilax (Vitrinoides) benjaminus sp. n. Descripción La longitud de los nueve ejemplares estudiados, todos adultos y conservados en alcohol de 70º, oscila entre 21 y 27 mm con una media de 24 mm. El holotipo muestra una longitud total de 24 mm con el escudo de 10 mm de longitud y 5 mm de anchura (figs. 1A, 1C). Su aspecto externo es similar a un Deroceras (Rafinesque, 1820), con mucus incoloro y tegumento gris–pardo translúcido, que nos permite observar la limacela en el interior del escudo. Los ejemplares conservados en alcohol son de color gris claro uniforme, sin ningún tipo de manchas, dibujo o reticulado, incluso sobre el escudo. Sólo un par de ejemplares presentan el extremo posterior algo pigmentado. A la lupa binocular se puede distinguir en algún individuo diminutas manchas apenas más oscuras, distribuidas sobre todo por el escudo. El tegumento es muy fino y casi transparente, siendo los tubérculos pequeños e igualmente finos. La cola es puntiaguda. El escudo mide algo más de un tercio de la longitud total, y presenta un halo claro alrededor del orificio respiratorio. Suela pedia tripartita y de tonalidad clara. El estudio de la anatomía interna se ha realizado sobre cinco ejemplares. Concha (figs. 1B, 3B) La limacela mide 4,5 x 3 mm. Es fina y algo convexa, de color blanco translúcido, con un pequeño halo membranoso del mismo color. Aparato digestivo El intestino da tres vueltas a la masa visceral, la última justo por encima de la glándula hermafrodita. Existe un ciego rectal que no llega al extremo apical de la masa visceral (fig. 2A), estando muy adherido al tegumento, por lo que no es fácil observarlo. En algunos ejemplares aparece dilatado. Aparato reproductor (fig. 2B) La glándula hermafrodita u ovotestis es redondeada, grande, de color claro, y con grandes acinos. Se encuentra situada exteriormente a la masa visceral sin estar parcialmente oculta por la misma, en la parte izquierda, y no llega al extremo de dicha masa. El conducto hermafrodita es más bien largo (12 mm), algo grueso y sin pigmentación alguna. Glándula del albumen triangular, alargada y de color crema, al-

Animal Biodiversity and Conservation 31.1 (2008)

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Fig. 1. A–C. Holotipo de Gigantomilax (Vitrinoides) benjaminus spec. nov. (MVHN nº 666–A). B. Limacela. D–F. Gigantomilax majoricensis: D. Neotipo de L. majoricensis, Puerto de San Antonio Abad, Ibiza, Islas Baleares (SNHM nº 90187); E. Limacela de otro ejemplar de G. majoricensis, Puerto de San Antonio Abab, Ibiza, Islas Baleares (SNHM nº 90187); F. Molán, Formentera, Islas Baleares (SNHM nº 90188). G. Lehmannia valentiana, Muntanyeta dels Sants, Sueca, Valencia (MVHN nº 1838). H. Limax flavus, Motilleja, Albacete (MVHN nº 1833). Fig. 1. A–C. Holotype of Gigantomilax (Vitrinoides) benjaminus n. sp. (MVHN nº 666–A). B. Limacella. D–F. Gigantomilax majoricensis: D. Neotype of L. majoricensis, Port of San Antonio Abad, Ibiza, Balearic Islands (SNHM nº 90187); E. Limacella of another specimen of G. majoricensis, Port of San Antonio Abab, Ibiza, Balearic Islands (SNHM nº 90187); F. Molán, Formentera, Balearic Islands (SNHM nº 90188). G. Lehmannia valentiana, Muntanyeta del Sants, Sueca, Valencia (MVHN nº 1838). H. Limax flavus, Motilleja, Albacete (MVHN nº 1833).

canzando 7 mm de largo. El espermoviducto es blanquecino y translúcido con una longitud similar a la de la glándula del albumen. La genitalia distal (figs. 2B, 2C, 2D) es de pequeño tamaño (alrededor de 3 mm) y presenta un vaso

deferente bien desarrollado rodeado por la parte distal de la próstata que alcanza el pene por una pequeña porción libre de masa glandular. El pene es entre globoso y cilíndrico, blanco y de superficie lisa, sin ningún apéndice ni glándula externa, y en su

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Fig. 2. A–D. Gigantomilax (Vitrinoides) benjaminus sp. n.: A. Detalle del ciego rectal; B. Aparato reproductor; C. Detalle de la lígula; D. Detalle de la bursa copulatrix de otro paratipo; E–G. Limax majoricensis (SNHM nº 90187) (E. Aparato reproductor; F. Detalle de la papila peneana; G. Detalle de la zona proximal de la papila peneana). Abreviaturas: ag. Atrio genital; bc. Bursa copulatrix; cr. Ciego rectal; eov. Espermoviducto; gh. Glándula hermafrodita; lg. Lígula; mr. Músculo retractor del pene; ovl. Oviducto libre; pe. Pene; vd. Vaso deferente. Fig. 2. A–D. Gigantomilax (Vitrinoides) benjaminus n. sp.: A. Detail of the rectal caecum; B. Reproductive system; C. Detail of the ligula; D. Detail of the bursa copulatrix of another paratype; E– G. Limax majoricensis (SNHM nº 90187) (E. Reproductive system; F. Detail of the penial papilla; G. Detail of the proximal area of penial papilla): Abbreviations: ag. Genital atrium; bc. Bursa copulatrix; cr. Rectal caecum; eov. Ovispermiduct; gh. Hermaphroditic gland; lg. Ligula; mr. Penial retractor muscle; ovl. Free oviduct; pe. Penis; vd. Vas deferens.

interior hay una lígula en forma de U o V con anchos brazos fuertemente estriados en sentido transversal (fig. 2C). Esta estriación continúa en parte en el fondo del saco peneano. En el atrio genital se inserta un oviducto libre tubular y largo, con un grosor inferior a la mitad de la del pene, y que se une por el extremo opuesto al espermoviducto. La glándula prostática aparece hinchada tanto en la

zona que rodea al vaso deferente como en una buena parte del espermoviducto. La bursa copulatrix (figs. 2B, 2D) es pequeña, de aspecto globoso, con el conducto que finaliza en la parte distal del pene, muy cerca del atrio, que es cilíndrico, corto, ancho y rodeado de finísimas fibras musculares. Presenta un pequeño músculo retractor peneano situado cerca de la zona de unión con el vaso deferente.

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Fig. 3. A. Limacela de G. majoricensis (SNHM nº 90187) (sin recubrimiento metálico). B–H. Gigantomilax (Vitrinoides) benjaminus sp. n.: B. Limacela; C. Mandíbula; D. Diente central y siete primeros dientes laterales; E. Diente central y primeros dientes laterales; F. Diente central y primer lateral; G. Transición entre dientes laterales y marginales; H. Dientes marginales. I–J. Detalle de algunos dientes marginales. Fig. 3. A. Limacella of G. majoricensis (SNHM nº 90187) (without a metal cover). B–H. Gigantomilax (Vitrinoides) benjaminus n. sp.: B. Limacella; C. Jaw; D. Central tooth and seven first lateral teeth; E. Central tooth and first lateral teeth; F. Central and first lateral teeth; G. Transition between the laterals and marginal teeth; H. Marginal teeth. I–J. Details of the marginal teeth.

Rádula y Mandíbula (figs. 3C–J) La rádula presenta dientes centrales y laterales tricúspides y la mandíbula es de tipo oxignato (fig. 3C), ambas características de la familia Limacidae. La rádula presenta 141 filas y su fórmula radular es 46L + C + 46L. El diente central es tricúspide, con el mesocono alargado y dos ectoconos más cortos situados simétricamente a ambos lados del mesocono (figs. 3D–F). Los dientes laterales son, inicialmente, también tricúspides aunque los ectoconos son ya asimétricos, y donde el endocono que es más alargado, se sitúa más cerca de la cúspide del mesocono y está más fusionado con él, mientras el ectocono permanece aproximadamente en la misma posición que en el diente central (figs. 3D–F). Los dientes laterales a medida que se aproximan al margen exterior de la rádula van cambiando de morfología (fig. 3G). A partir del L15, se puede considerar que comienzan los dientes marginales (31) ya que el endocono se fusiona totalmente con el mesocono (fig. 3G), y el ectocono se desplaza hacia abajo presentando el diente una morfología más estilizada, curvada hacia el interior de la rádula y dando un aspecto como de "navaja curva", pudiendo presentar dos o tres cúspides alineadas, dos de ellas laterales (figs. 3I–J). Sólo en las últimas dos o tres hileras de dientes marginales se puede encontrar algún diente con una sola cúspide, aunque no es lo más común (fig. 3H). Castillejo & Garrido (1994) señalan que la rádula de L. majoricensis presenta alrededor de 130 filas, y su fórmula radular es 52L + C + 52L, de los que considera 35 marginales a ambos lados; sin embargo el número de filas halladas en G. benjaminus sp. n. es de 141, 11 filas más, y el número de dientes laterales es menor, 46. También señalan que L. majoricensis presenta 17 dientes laterales, mientras que en G. benjaminus sp. n. solo hay 15.

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vas deferens surrounded by a swollen prostatic gland. The penis is short and thick without any appendix. Inside the penis there is a grooved U or V–shape ligula. Tubular free oviduct. The penial retractor muscle is very thin and is inserted close to the vas deferens. Material estudiado Holotipo depositado en el Museu Valencià d’Història Natural (MVHN nº 666–A) (figs. 1A–C; 5 paratipos depositados en el MVHN (nº 666–B); 1 paratipo en el Museo Nacional de Ciencias Naturales de Madrid (nº 15.05/44113); 1 paratipo en el Museu de Zoologia de Barcelona (nº 2001–0283); 1 paratipo en el Swedish Museum of Natural History de Estocolmo (nº 6955). Localidad tipo: Barranc d’Algendar (Ferreries, Menorca, Islas Baleares; UTM = 31TEE8223). (09/1998; B. Gómez y M. Conde leg.). Etimología El nombre específico hace alusión al pequeño tamaño de esta especie y además se aplica en honor del Dr. Benjamín Gómez Moliner, destacado malacólogo de la Universidad del País Vasco y recolector de los ejemplares. Distribución y hábitat Probable endemismo de Menorca, solo conocido con certeza en el Barranc d’Algendar. Se trata de un barranco de sustrato calizo y con un pequeño arroyo. La vegetación consiste en un bosque mixto mediterráneo, con encinas, higueras y olivos. Son zonas de umbría, con abundante humus, y los ejemplares se han recolectado bajo piedras y entre la hojarasca.

Diagnosis Comentarios Babosa de pequeño tamaño con el dorso de color gris, sin ornamentación alguna, todo lo más con una ligera pigmentación en el afilado extremo posterior. Tegumento muy delgado y casi transparente. Presenta un ciego rectal que no llega al fondo de la masa visceral. La genitalia distal es pequeña y presenta un vaso deferente bien desarrollado y rodeado por la parte distal de la próstata, que aparece hinchada. El pene es corto y grueso y sin apéndices. En el interior del mismo hay una lígula estriada transversalmente en forma de U o V. Oviducto libre tubular. Músculo retractor del pene muy delgado que se inserta junto al vaso deferente. Diagnose Slugs of small size. Dorsum grey, without any ornamentation, only with a slight pigmentation in the posterior sharp end. Tegument thin and almost transparent. There is a rectal caecum that does not reaches the bottom of the visceral mass. Distal genitalia is of small size and shows a well developed

Wiktor et al. (2007) en su apartado "Material" designan un neotipo de Gigantomilax (Vitrinoides) majoricensis también del Barranc d’Algendar, y además la citan en el Barranc de Binigaus, también en Menorca, y Cala Figuera y Costa de Canyamel, ambas en Mallorca. En nuestra opinión este neotipo y toda la redescripción efectuada corresponde a Gigantomilax (V.) benjaminus sp. n. En el trabajo citado en ningún momento se hace referencia a los ejemplares mallorquines, por lo que su presencia en Mallorca habría que confirmarla. Toda la "redescripción" se basa en ejemplares del Barranc d’Algendar. Igualmente en la figura 12 del mismo artículo presentan la distribución de G. majoricensis en la isla de Menorca, en la que añaden otras siete localidades en las que han hallado limacelas fósiles o subfósiles (del Plioceno Superior al Holoceno), que atribuyen a esta especie. Es conocida la poca fiabilidad de la limacela para determinar babosas a nivel específico (Quintana, 2001; Reuse, 1983; Wiktor, 2000), todo lo más a nivel de

Animal Biodiversity and Conservation 31.1 (2008)

Tabla 1. Diferencias morfo–anatómicas entre G. benjaminus sp. n. y G. majoricensis. Table 1. Morpho–anatomical differences between G. benjaminus n. sp. and G. majoricensis.

Caracteres

G. benjaminus sp. n.

G. majoricensis

Tamaño

Menor (20–36 mm)

Mayor (25–45mm). Posiblemente en vivo superen los 100 mm

Forma

Estilizada

Abombada en el escudo

Coloración del dorso

Gris claro

Pardo claro con bandas y puntos oscuros

Tegumento

Fino y translúcido

Grueso y opaco

Tubérculos dérmicos

Finos

Gruesos y resaltados

Limacela

Pequeña

Más grande

Ciego rectal

Corto

Largo

Glándula hermafrodita

Grandes acinos; claros

Acinos pequeños; más oscuros

Bursa copulatrix

Redondeada. Conducto estrecho

Alargada. Conducto ancho

Pene

Corto. Entre globoso y cilíndrico

Curvado. Dividido en dos porciones

Estructuras intrapeneanas

Lígula en V o U con estriación transversal

Pliegue sin estriación transversal

Vaso deferente

Bien desarrollado, rodeado por glándula prostática

Muy corto, sin aspecto glandular

Músculo retractor del pene

Presente

Ausente

Atrio genital

Corto y ancho

Largo y estrecho

Fórmula radular

46L + C + 46L

52L + C + 52L

Rádula: nº filas de dientes

141

l130

familia, y ya que en Menorca conviven también otros limácidos como Lehmannia valentiana y Limax flavus, consideramos muy dudosas estas determinaciones. Incluso se afirma (Wiktor et al., 2007: p. 192) que "estas limacelas pueden indicar el carácter autóctono de Gigantomilax (V.) algendari en Menorca", nomen nudum que tan solo se nombra y del que no se proporciona ni el autor ni la referencia de su descripción ni ningún otro dato. Discusión Wiktor et al. (2007) "redescriben Limax majoricensis", reasignan el género y realizan la nueva combinación Gigantomilax (Vitrinoides) majoricensis (Heynemann 1863), que figuran a partir de material reciente recolectado de Menorca. Para justificar la nueva adscripción genérica y subgenérica, la comparan con Gigantomilax (Vitrinoides) cecconi Simroth 1906, especie de Israel, y sugieren algunas explicaciones para justificar las áreas tan disjuntas de distribución de este género, con representantes en China, Cáucaso, Asia Menor y los Balcanes, pero que falta

en casi toda la región mediterránea para aparecer en las Islas Baleares. En su opinión se debe a la escasez de muestreos realizados en el Norte de África donde, posiblemente, aparecerán representantes de este género. En nuestra opinión, "la redescripción de Limax majoricensis" de Wiktor et al. (2007), en realidad se refiere a Gigantomilax (Vitrinoides) benjaminus sp. n., existiendo también otra especie en Baleares, probablemente no en Menorca, a la que se han referido desde Heynemann todos los autores mencionados en la introducción y que debe conservar la denominación propuesta por Wiktor et al. (2007) de Gigantomilax (Vitrinoides) majoricensis (Heynemann 1862). El aspecto exterior y el tamaño del nuevo taxon menorquín son radicalmente distintos a los de G. majoricensis pero el aparato reproductor presenta una cierta similitud, aunque con características diferenciales claras. Para la comparación (tabla 1) hemos utilizado los datos y figuras de G. majoricensis realizadas por Castillejo & Garrido (1994, 1996) y ejemplares de Ibiza y Formentera procedentes del Swedish Museum of Natural History de Estocolmo.

G. benjaminus sp. n. y G. majoricensis tienen tamaños diferentes: Castillejo & Garrido (1994), señalan que la longitud normal de los ejemplares conservados de G. majoricensis varía entre 25 y 45 mm, aunque en general no sobrepasan los 35 mm, habiendo estudiado un total de 54 individuos de los que solamente tres eran adultos. Castillejo & Garrido (1996) indican que posiblemente la longitud de los adultos en vivo sobrepasa los 100 mm. Nuestros nueve ejemplares conservados, todos adultos, miden entre 20 y 27 mm, [hasta 36 mm los ejemplares, también preservados en alcohol, de Wiktor et al. (2007)], por lo que se trata de una especie de tamaño menor, aunque los rangos de tamaño máximo y mínimo de ambas especies pueden solaparse. En cuanto al aspecto externo, G. majoricensis es de color pardo claro con dos bandas longitudinales oscuras formadas por puntos en el dorso que está también salpicado por manchas del mismo color, más abundantes en el escudo, lo que recuerda el aspecto de L. valentiana. G. benjaminus sp. n. tiene un dorso gris claro uniforme, con algunos ejemplares blanco–lechosos que Wiktor et al. (2007) sugieren como posibles casos de albinismo. El tegumento en G. benjaminus sp. n. es delgado y translúcido, casi transparente, dejando ver algunos órganos internos mientras que en G. majoricensis es más grueso y opaco, y con tubérculos mucho mas patentes. La zona media de los individuos de G. majoricensis está claramente más abombada, con anchura entre 7,4 y 5,7 mm mientras que en G. benjaminus sp. n. es más estilizada y mide alrededor de 4,5 mm de ancho. La limacela estudiada de G. majoricensis mide 6,2 mm de longitud y 4,3 mm de anchura (figs. 1E, 3A), mientras que en G. benjaminus sp. n. alcanza 3,8 mm y 2,25 mm respectivamente (figs. 1B, 3B). También se han encontrado ciertas diferencias en la rádula (véase en la descripción), tanto en la fórmula radular como el número de filas. Finalmente, G. benjaminus sp. n. presenta un ciego rectal más bien corto que sin embargo se aprecia mucho más largo en G. majoricensis, llegando casi al final de la masa visceral en esta última (Castillejo & Garrido, 1994: fig. 4; 1996: fig. 21; Wiktor et al., 2007: fig. 9b de un ejemplar juvenil de Mallorca, probablemente G. majoricensis). Atendiendo al aparato reproductor, se observan grandes similitudes que nos permiten considerar ambas especies congenéricas, pero existen diferencias considerables (fig. 2): 1. Glándula hermafrodita con grandes acinos en G. benjaminus sp. n. que son pequeños en G. majoricensis. 2. Castillejo & Garrido (1994, 1996) señalan la presencia de un corto vaso deferente en G. majoricensis, lo que coincide con nuestras observaciones (fig. 2E). Sin embargo, G. benjaminus sp. n. presenta un vaso deferente más desarrollado y rodeado proximalmente y en casi toda su extensión por la próstata. En nuestra opinión no se trata, en absoluto, de una estructura equivalente a la porción proximal del pene que describen Castillejo & Garrido (1994, 1996) en algunos ejemplares de G. majoricensis, en los que las dos porcio-

Borredà & Martínez–Ortí

nes están ajustadas por bandas musculares. Esta porción proximal del pene no es de aspecto glandular el cual, sin embargo, si aparece en la porción masculina del espermoviducto de esta especie. 3. La bursa copulatrix de G. benjaminus sp. n. es redondeada u ovalada con un conducto más estrecho mientras que la de G. majoricensis es más bien alargada y el conducto es difícil de diferenciar ya que presenta un grosor similar al de la bursa. 4. Existencia en G. benjaminus sp. n. de un delgado músculo retractor del pene, entre el mismo y el vaso deferente, que está ausente en G. majoricensis. 5. El pene en G. benjaminus sp. n. es corto, entre globoso y cilíndrico, y ni curvado ni dividido en dos regiones como en G. majoricensis. 6. Las estructuras intrapeneanas son totalmente diferentes en ambas especies (figs. 2C, 2F–G). G. benjaminus sp. n. presenta dos repliegues que forman una V o U estriados en sentido transversal que ocupan gran parte del interior del pene (fig. 2C). L. majoricensis también presenta estos repliegues aunque mucho menos desarrollados y con débil estriación longitudinal (fig. 2F), y ambos se unen en una papila redondeada de aspecto glanduloso plegada en espiral sobre sí misma y unida a un cordón que continúa hacia el espermoviducto (fig. 2G), lo que concuerda con la figura 22 de Castillejo & Garrido (1996: p. 142). 7. El atrio genital es corto y ancho en G. benjaminus sp. n., y más largo y estrecho en G. majoricensis. Se trata de uno de los limácidos más pequeños que se conocen, en cuanto a tamaño sólo comparable en la malacofauna ibérica a Malacolimax tenellus (Müller, 1774), que presenta distribución pirenaica y tiene una genitalia totalmente distinta (Outeiro et al., 1988). Se diferencia de Limax flavus Linneo, 1758 (fig. 1H), frecuente en la región mediterránea e Islas Baleares, por el tamaño mucho menor y por su coloración y ornamentación muy diferente, además de poseer un aparato reproductor muy distinto. En cuanto a las Lehmannia peninsulares, como L. valentiana también presente en la fauna balear (fig. 1G), L. marginata (Müller, 1774) y L. rupicola Lessona et Pollonera 1884, son todas de aspecto externo muy diferente de G. benjaminus sp. n. y además se pueden distinguir fácilmente por la presencia de un apéndice o glándula bien conspicua en el pene en las Lehmannia (Castillejo, 1982; Borredà & Collado, 1996). Lehmannia nyctelia (Bourguignat, 1861) es una especie norteafricana también presente en Italia (Cossignani & Cossignani, 1995), similar externamente a L. valentiana pero que carece del referido apéndice. Sin embargo presenta un largo y tubular conducto deferente no rodeado de glándula prostática que, entre otros caracteres, la diferencia de G. benjaminus sp. n. Selección del neotipo de Limax majoricensis Heynemann 1862 Tal como opinan Castillejo & Garrido (1994) y Witkor et al. (2007) la serie tipo de esta especie

Animal Biodiversity and Conservation 31.1 (2008)

probablemente ha desaparecido, idea que compartimos. Witkor et al. (2007) designan un neotipo para esta especie que en realidad corresponde a G. benjaminus sp. n. Para aclarar esta confusión consideramos necesario designar otro neotipo de G. majoricensis. Castillejo & Garrido (1994: figs. 11, 12) muestran dos fotografías de un mismo ejemplar, originarias de H. W. Waldén, depositado en el Swedish Museum of Natural History de Estocolmo (SMNH nº 90187; junto con cinco ejemplares más). Fue recolectado en 1870 en el Puerto de Sant Antoni Abad (Ibiza) (sic = Puerto Magno. 38º 59' N 01º 20' E. Fishing market) por F. Söderlund y determinado por él como Limax variegatus. Este ejemplar es el mismo que aparece en la figura 1D del presente trabajo y el cual designamos como neotipo de Limax majoricensis Heynemann, 1862 (= Gigantomilax (Vitrinoides) majoricensis). Sus medidas son de 22,0 mm de longitud y 6,5 mm de anchura. Wiktor et al. (2007: p. 188) señalan que los ejemplares depositados en el Museo de Estocolmo (por error indican que están depositados en el de Göteborg) son juveniles, basándose en las figuras de Castillejo & Garrido (1994). Sin embargo, tras la revisión que hemos realizado de dicha muestra (SMNH nº 90187) podemos afirmar que todos los individuos, excepto uno, son adultos. En cuanto al aspecto externo todos los ejemplares revisados, tanto los de esta muestra (SMNH nº 90187) como los de la de Formentera (SMNH nº 90188, 3 ejs., fig. 1F), presentan un patrón de bandas longitudinales y puntos, y con tubérculos gruesos en el dorso, que coincide con las observaciones de Castillejo & Garrido (1994: p. 219) y Castillejo & Garrido (1996: p. 141) que se hacen extensivas a todos los ejemplares depositados en el museo de Göteborg (Castillejo & Garrido, 1994: figs. 1–2, p. 220). Agradecimientos Este estudio ha sido financiado en parte por el proyecto de investigación Fauna Ibérica (DGICYT PB95–0235). A la Sección de Microscopía Electrónica del S.C.S.I.E. de la Universitat de València por su ayuda en la utilización del microscopio electrónico de barrido Hitachi S–4100. A Karin Sindemark del Department of Invertebrate Zoology del Swedish Museum of Natural History de Estocolmo por la cesión de las muestras de Limax majoricensis. Referencias Anderson, R., 2004. Pseudosuccinea columella (Say) and other additions to the fauna of Menorca. Journal of Conchology, 38: 323. Borredà, V., 1996. Pulmonados desnudos (Mollusca: Gastropoda: Pulmonata) del este de la Península Ibérica. Tesis doctoral (inédita). Univ. de València. Borredà, V. & Collado, M. A., 1996. Pulmonados

desnudos (Gastropoda, Pulmonata) de la provincia de Castellón (E España). Iberus, 14 (2): 9–24. Castillejo, J., 1982. Los Pulmonados desnudos de Galicia II. Género Lehmannia Heynemann, 1862 (Pulmonata: Limacidae). Iberus, 2: 19–28. Castillejo, J. & Garrido, C., 1994. Morphology and anatomy of Limax (Limacus) majoricensis Heynemann, 1862, from the Balearic Islands (Spain, western Mediterranean) (Gastropoda: Pulmonata: Limacidae). Basteria, 58: 217–224. – 1996. Las babosas de la familia Limacidae Rafinesque, 1815 (Gastropoda: Pulmonata: Terrestria nuda) de la Península Ibérica e Islas Baleares. Morfología y distribución. Nova Acta Científica Compostelana (Bioloxía), 6: 131–143. Castillejo, J. & Rodríguez, T., 1991. Babosas de la Península Ibérica y Baleares. Monografías da Universidade de Santiago de Compostela, 162: 1–211. Cossignani, T. & Cossignani, V., 1995. Atlante delle conchiglie terrestri e dulciacquicole italiane. L’Informatore Piceno, Ancona. Gasull, L., 1984. Terrestrial and fresh–water gastropods of the Pityusics (Eivissa and Formentera), excluding Trochoidea (Xerocrassa) Monterosato 1892. En: Biogeography and Ecology of the Pityusic Islands, 11: 231–241 (H. Kuhbier, J. A. Alcover & G. D’Arellano Tur, Eds.). Dr. W. Junk Publisher, The Hague, Boston & Lancaster. Gasull, L. & Van Regteren Altena, C. O., 1969. Pulmonados desnudos de las Baleares (Mollusca: Gastropoda). Boletín de la Sociedad de Historia Natural de Baleares, 15: 121–134. Hesse, P., 1926. Die Nacktschnecken der palearkstichen Region. Abhandlungen Archive Molluskenkunde, 2: 1–152. Hidalgo, J. G., 1875. Catálogo iconográfico y descriptivo de los Moluscos terrestres de España, Portugal y las Baleares, 1–224(1A), 1–16(2A). Imprenta Segundo Martínez, Madrid. – 1879. Catálogo de los Moluscos terrestres de las Islas Baleares. Revista de los Progresos de las Ciencias Exactas, Físicas y Naturales, 20: 429–452. – 1916. Datos para la fauna española (Moluscos y Braquiópodos). Boletín de la Real Sociedad Española de Historia Natural, 16: 235–246. – 1918. Suplementos a la bibliografía crítica malacológica. Memorias de la Real Academia de Ciencias. Madrid. 15: 1–41. Jaeckel, S. H. & Plate, H. P., 1964. Beitráge zur Kenntnis der Molluskenfauna der Insel Mallorca. Malakologische Abhandlungen. Dresden, 1: 53–164. Martínez–Ortí, A., 1999. Moluscos terrestres testáceos de la Comunidad Valenciana. Tesis doctoral (inédita). Univ. de València. Outeiro, A., Rodríguez, T. & Castillejo, J., 1988. Malacolimax tenellus (Müller, 1774) (Mollusca: Gastropoda: Limacidae) en España. Morfología y distribución. Miscelánea Zoológica, 12: 41–46.

Paul, C. R. C., 1982. An annoted check–list of the non–marine mollusca of the Pityuse Islands, Spain. Journal of Conchology, 31: 79–86. Quintana, J., 2001. Fauna malacológica presente en los sedimentos holocénicos del Barranc d’Algendar (Ferreries, Menorca). Spira, 33–40. Reuse, C., 1983. On the taxonomic significance of the internal shell in the identification of european slugs of the families Limacidae and Milacidae (Gastropoda: Pulmonata). Biologische Jahrbuch, 51: 180–200. Waldén, H. W., 1961. On the variation, nomenclature, distribution and taxonomical position of Limax

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(Lehmannia) valentiana Ferussac (Gastropoda, Pulmonata). Arkiv för Zoologi, Estocolmo, 2: 15(3): 71–96. Wiktor, A., 2000. Agriolimacidae (Gastropoda, Pulmonata). A systematic monograph. Annales zoologici Warszawa, 49(3): 347–590. Wiktor, A., Quintana, J. & Beckmann, K. H., 2007. Redescription of Limax majoricensis (Heynemann 1863) (Gastropoda: Pulmonata: Limacidae) from the Balearic Island. En: Die Land und Süsswassermollusken der Balearischen Inseln, CLECOM–Projekt: 187–197 (K. H. Beckmann, Ed.). ConchBooks Ed., Hackenheim.

Animal Biodiversity and Conservation 31.1 (2008)

Hemibrycon rafaelense n. sp. (Characiformes, Characidae), a new species from the upper Cauca River, with keys to Colombian species

C. Román–Valencia & D. K. Arcila–Mesa

Román–Valencia, C. & Arcila–Mesa, D. K., 2008. Hemibrycon rafaelense n. sp. (Characiformes, Characidae), a new species from the upper Cauca River, with keys to Colombian species. Animal Biodiversity and Conservation, 31.1: 67–75. Abstract Hemibrycon rafaelense n. sp. (Characiformes, Characidae), a new species from the upper Cauca River, with keys to Colombian species.— A new fish species of Hemibrycon is described from the San Rafael River, upper Cauca River, Colombia. H. rafaelense can be distinguished from other species of the genus by the number of cusps on the teeth in the internal premaxilla row (3–5 vs. 5–7 except H. surinamensis), by the number of predorsal scales (10–12 vs. 12–17, except H. jelskii and H. orcesi), and by poscleithrum 1 (much closer to postcleithrum 2 vs. postcleithrum 1 and 2 clearly separated). Ecological data of the aquatic habitat of the new taxon are presented and keys to help identify known Colombian species are included. Key words: Hemibrycon, Tropical fish, South America. Resumen Hemibrycon rafaelense sp. n. (Characiformes, Characidae), una nueva especie del alto Cauca, con claves de identificación para las especies colombianas.— Se describe una nueva especie de Hemibrycon para el río San Rafael, alto Cauca, Colombia. H. rafaelense se diferencia de sus congéneres por el número de cúspides de la fila interna de dientes del premaxilar (3–5 vs. 5–7 excepto H. surinamensis), por el número de escamas predorsales (10–12 vs.12–17, excepto H. jelskii y H. orcesi), y por el postcleitrum 1 (mucho más próximo al postcleitrum 2 vs. postcleitrum 1 y 2 bien separados). Se incluyen datos ecológicos del hábitat propio del nuevo taxón y las claves para la identificación de las especies conocidas de Colombia. Palabras clave: Hemibrycon, Pez tropical, Sudamérica. (Received 2 VIII 06; Conditional acceptance: 16 X 07; Final acceptance: 18 II 08) C. Román–Valencia & D. K. Arcila–Mesa, Lab. de ictiología, Univ. del Quindío, A. A. 2639, Armenia, Quindío, Colombia. Corresponding author: C. Román–Valencia. E–mail: ceroman@uniquindio.edu.co

ISSN: 1578–665X

Introduction Previous studies of Hemibrycon Günther in Colombia and adjacent localities focused on the taxonomy and description of new species (Eigenmann, 1913; Eigenmann et al., 1914; Eigenmann, 1922, 1927; Géry, 1977; Meek & Hildebrand, 1916; Schultz, 1944; Dahl, 1960, 1971; Dahl & Medem, 1964; Miles, 1971; Taphorn, 1992; Román–Valencia, 2001, 2004; Román–Valencia et al., 2006; Román–Valencia & Ruiz–C., 2007; Román–Valencia et al., 2007; Bertaco et al., 2007). Román– Valencia (2004) considered Hemibrycon tolimae a synonym of Bryconamericus tolimae, while Román– Valencia (2001) distinguished Hemibrycon boquiae from Bryconamericus caucanus and discussed the validity of traditional diagnostic characters for Hemibrycon. There is no modern phylogenetic hypothesis of relationships for this genus, and the characters used to define it have not proven significant in determining its monophyly. Most of these characters are little or non–informative and some coincide with those for other Characidae genera. When no hypothesis is available, it is not possible to reconstruct a spatial model to explain the current geographic distribution (Román–Valencia et al., 2007). The genus lives in secondary creeks between 41 to 1,910 m a.s.l., with crystalline waters flowing over substrates of stones, rocks, sand, or leaf litter in decomposition, with high dissolved oxygen (mean 8 ppm). Their diet is mainly aquatic and terrestrial insects of autochthonous and allochthonous origin (Román–Valencia & Botero, 2006). The purpose of this paper is to describe a new species of Hemibrycon from Colombia, as a further contribution to the ongoing revision of the genus. Material and methods Fishes were captured using a seine, preserved with 10% formalin and later stored in 70% ethanol. Measurements were made with digital calipers to 0.01–mm precision, and expressed as percentages of standard (SL) and head lengths (HL) (table 1). Measurements and counts were taken on the left side, except if this was damaged. Counts and measurements were recorded following the methodology described in Vari & Siebert (1990). We performed principal component analysis (PCA) on the correlation matrix of morphometric and meristic characters; for meristic characters we used the Mann–Whitney non–parametric rank–sum test for species in biogeographically proximity; bar graphs of 99% confidence were used to provide more information in the differentiation of species. Observations of cartilage and bone were made on two cleared and stained specimens (C. and S.) following the modifications by Song & Parenti (1995) of the method outlined in Taylor & Van Dyke (1985). Bone nomenclature follows Weitzman (1962), Vari (1995) and Ruiz–C. & Román–Valencia (2006).

Román–Valencia & Arcila–Mesa

Specimens were compared with material housed in the Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Bogotá (ICNMNH); Field Museum of Natural History, Chicago (FMNH); Laboratorio de Ictiología, Departamento de Biología, Universidad del Quindío, Armenia, Colombia (IUQ); Museo de Biología, Instituto de Zoología Tropical, Universidad Central de Venezuela, Caracas (MBUCV); Museo de Ciencias Naturales de la UNELLEZ–Guanare, Venezuela (MCNG); Museo de Historia Natural La Salle, Caracas, Venezuela (MHNLS); California Academy of Sciences, Department of Ichthyology, San Francisco, USA (CAS); Instituto de Investigación de Recursos Biológicos "Alexander Von Humboldt'', Villa de Leyva, Boyacá, Colombia (IAvH); Staatliches Museum für Tierkunde, Dresden, Fischsammlung, Germany (MTD F); Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Perú (MNH–UNMSM) and National Museum of Natural History, Washington D.C., USA (USNM). In the material examined and comparative sections, the number of specimens is given in parentheses after the catalog number, for example: FMNH 56258 (4), means there were (4) in that lot. Comparative material Bryconamericus tolimae: FMNH 56258 (4 paratype), Colombia, Ibagué; IUQ 484 (48), Colombia, Tolima, Ibagué, Pastales, 100 m before Pastales Ibagué– Juntas Road, Combeima, Magdalena River system (4º 30' 19'' N, 75º 17' 46'' W) 1,586 m a.s.l. Bryconamericus guaytarae: CAS 40844 (1 paratype); Colombia, Nariño, Patia Basin, Guaitara River on the mouth of the Patia River. Bryconamericus lassorum: MHNLS 8889 (12), Venezuela, Monagas, Aragua River (bridge on the Becerros Creek), Maturin–Quiriquire Road, ca. 10 km Aragua–Maturin. Hemibrycon boquiae: IUQ 301a (3), (C. and S.), Colombia, Quindío, Boquia Creek (4° 38' 35'' N, 75° 75' 11'' O) 1,819 m a.s.l; IUQ 754 (104), Colombia, Quindío, Boquia Creek (4° 38' 35'' N, 75° 75' 11'' O) 1,819 m a.s.l; IUQ 871 (15), Colombia, Quindío, Boquia Creek (4° 38' 35'' N, 75° 75' 11'' O) 1,819 m a.s.l. Hemibrycon colombianus: IAvH 3130 (28), Colombia, Santander, Moniquira and Suárez Rivers. Hemibrycon jelskii: IUQ 1141 (2), (C. and S.), Divino River, 1,600 m before Chontayacu; USNM 361171 (3), Perú Cusco La Convención, Echarate, Peruanita, Igoripato Creek. Hemibrycon dariensis: USNM 260697 (1), Colombia, Creek Bernal, tributary of Río Negua, 17 III 1967; USNM 293218 (2), Panamá, locality of Kuna Yala, Río Madinga between Río Pingandi, and Mandinga (Atlántico) (09° 28´ N, 70° 06´ W), 3 III 1985; USNM 293234 (1), Panamá, Darién, Río Pirre ca 1/2 km above el Real (Río Tuira), Pacifico, 19 II 1985; USNM 293245 (28), Panamá, Darien, Río Tuira, Darién Province, Pucuro River about 3– 4 km above the confluence of the Río Tuira Pacifico,

Animal Biodiversity and Conservation 31.1 (2008)

Table 1. Morphometric and meristic data of H. rafaelense n. sp. (Standard and total lengths in mm, mean values in parenthesis.) Tabla 1. Datos morfométricos y merísticos de H. rafaelense sp. n. (Longitud estándar y total en mm, medias entre paréntesis.)

H. rafaelense Morphometrics

Paratype

Holotype

Standard length (mm)

22.73–89.95 (40.91)

49.35

Total length

28.29–105.6 (50.26)

61.02

Percentages of SL Body depth

23.27–29.87 (26.22)

26.55

Snout–dorsal fin origin distance

48.33–54.24 (51.31)

51.04

Snout–pectoral fin insertion distance

21.26–25.84 (23.81)

23.32

Snout–pelvic fin insertion distance

42.00–46.74 (44.52)

42.7

Dorsal–fin origin–pectoral–fin distance

35.21–41.26 (38.23)

37.28

Snout–anal fin origin distance

54.74–59.92 (56.99)

55.91

Dorsal fin origin–hypurals plate length

46.33–55.49 (52.20)

53.41

Dorsal fin origin–anal fin origin length

23.78–30.75 (28.00)

27.62

Dorsal fin length

17.39–23.76 (21.68)

19.78

Pectoral fin length

17.75–22.18 (19.66)

19.47

Pelvic fin length

11.06–16.06 (12.41)

13.47

Anal fin length

11.00–19.23 (15.10)

14.77

Caudal peduncle depth

8.28–11.88 (10.48)

10.46

Caudal peduncle length

7.25–13.31 (9.94)

11.21

18.17–23.14 (22.06)

21.56

Snout length

20.29–29.07 (24.48)

23.87

Orbital diameter

36.65–43.58 (40.18)

36.37

Postorbital distance

31.21–39.9 (35.44)

35.81

Maxilla length

28.00–37.76 (32.35)

33.74

Interorbital distance

34.74–41.55 (37.83)

33.83

Upper jaw length

24.49–35.53 (29.85)

26.79

Head length Percentages of HL

Meristic Lateral–line scales

40–43

Scale rows between dorsal–fin origin and lateral line

5–8

Scale rows between anal–fin origin and lateral line

4–6

Scale rows between pelvic–fin insertion and lateral line

4–7

Predorsal median scales Dorsal–fin rays Anal–fin rays Pelvic–fin rays Pectoral–fin rays

17 II 1985; IUQ 523 (26), Colombia, Departamento de Antioquia, Río Zungo highway, Río León system, 17 XII 1990; IUQ 524 (2), Colombia, Antioquia, Creek

10–13

ii–iii,7–8

ii,8

iii–iv,24–28

iv,27

ii,6

ii,9–11

ii,10

km 25 road Mutatá–Chigorodo, XII 1990. IUQ 525 (26), Colombia, Antioquia, Río León drainage, Río Villarteaga, XII 1990.

Hemibrycon metae: IAvH 3122 (10), Colombia, Casanare, Aguazul, Cachiza River, Chichaca Creek; III 1995. Hemibrycon taeniurus: MHNLS 8046 (2), Venezuela, Monagas, Punceres River, to 15 km of Quiriquire (63º 53' 30'' N, 63º 9' W); MHNLS 8070 (119), Venezuela, Monagas River, Aragua (bridge on the Becerros Creek), Maturin–Quiriquire Road, ca. 10 km Aragua– Maturin (63º 25' W, 63º 55' N) 100 m a.s.l; MHNLS 8091 (72), Venezuela, Monagas, Aragua River (bridge on the Becerros Creek, Maturin–Quiriquire road, ca. 10 km Aragua–Maturin (63º 25' W, 63º 55' N) 100 m a.s.l; MHNLS 8157 (52), Venezuela, Sucre, Parare River, at road 5 km from Grande River, Quiriquire– Cariaco Road (63º 17' W, 10º 19' N), 15 II 1991; MHNLS 8888 (191), Venezuela, Monagas, Aragua River (bridge on the Becerros Creek), Maturin– Quiriquire road, ca. 10 km Aragua–Maturin (63º 25' W, 63º 55' N) 100 m a.s.l; MHNLS 8891 (6), Venezuela, Monagas, Aragua River (bridge on the Becerros Creek), Maturin–Quiriquire Road, ca. 10 km Aragua– Maturin (63º 25' W, 63º 55' N) 100 m a.s.l. Hemibrycon microformaa: IUQ 512 (1 paratype), (C. and S.), Colombia, Atrato River Basin, Chintado River, 100 m bridge on the Yuto–Certegui; IUQ 1204 (1 paratype), (C. and S.), Atrato River Basin, Chintado River, 100 m bridge on the Yuto–Certegui. Hemibrycon pautensis: IUQ 533 (2 paratypes), (C. and S.), Ecuador, Paute River, on the mouth of the Namangoza River. Hemibrycon polyodon: IUQ 1142 (2), (C. and S.), Ecuador, Antonio–Guadalupe Creek. Results Hemibrycon rafaelense n. sp. (table 1, figs. 1–7) Holotype: ICNMHN 6703, 43.24 mm SL; Colombia, Risaralda, Apia, San Rafael Creek, Apia River system, on the Santuario–Apia road, 12 April 1991. Paratype: ICNMHN 3505 (50) collected with holotype; IUQ 499 (2) (C. and S.) collected with holotype. IUQ 509 (27); Colombia, Risaralda, Apia, San Rafael Creek in mouth of Apia River, at 100 m of Santuario–Apia Road (5° 04' 54'' N, 75° 56' 36'' W) 1,253 m a.s.l., 8 VII 2003; MCNG 54101 (5); Colombia, Risaralda, Apia, San Rafael Creek at mouth of Apia River, 100 m from Santuario–Apia Road (5° 04' 54'' N, 75° 56' 36'' W) 1,253 m a.s.l., 8 VII 2003; MTD F 27623–27624 (2); Colombia, Risaralda, Apia, San Rafael Creek at mouth of Apia River, 100 m from Santuario–Apia Road (5° 04' 54'' N, 75° 56' 36'' W) 1,253 m a.s.l., 8 VII 2003. Diagnosis The new taxon can be distinguished from all congeners by the number of cusps on the row of internal premaxilla teeth (fig. 2) (3–5 vs. 5–7 except H. surinamensis, by the number of predorsal scales (10–12 vs.12–17, except H. jelskii and H. orcesi) by poscleitrum 1 (fig. 3) (much closer to postcleitrum 2 vs. postcleitrum 1 and 2 clearly separated).

Román–Valencia & Arcila–Mesa

Description Morphometric in table 1. Body elongate, anteriorly robust, dorsal profile of head convex; area above orbits convex. Dorsal profile of body curved from supraoccipital to dorsal–fin origin, oblique from last dorsal–fin ray to caudal–fin base. Ventral profile of body convex from snout to anal–fin base, convexity more pronounced beyond posterior portion of pectoral fins. Caudal peduncle laterally compressed in all specimens. Head and snout short; jaws equal, mouth terminal; lips soft and flexible, not covering external tooth row of premaxilla; ventral border of upper jaw slightly concave; opening of posterior nostrils vertically ovoid; opening of anterior nostrils with posterior membranous flap. Six infraorbitals present, all with laterosensory canal; third infraorbital long, wide, with ventral and posterior borders in contact with preopercle. Supraorbital absent. Premaxilla with short lateral process, and two rows of teeth; outer row with 3– 5 tricuspid teeth arranged in straight line. Inner row with 3–5 teeth, with central cusp larger. Maxilla short with posterior tip not reaching anterior border of third infraorbital. Maxilla with 8 to 12 teeth, with 1 to 3 cusps, along anterior and ventral border in some specimens (< 40 mm SL). Dentary with 2 to 3 large pentacuspid teeth followed by 8 small teeth with one to three cusps. Rhinosphenoid cartilaginous and ossified, separated posteriorly from orbitosphenoid by mesethmoid cartilage. Orbitosphenoid with short, narrow apophysis present. Parasphenoid elongate and undivided posteriorly. Mesethmoid cartilage contacting dorsal and lateral margins of rhinosphenoid and extending to anterior extreme of parasphenoid. Anterior portion of parasphenoid covering posterodorsal surface of vomer cartilaginous; posterior portion of parasphenoid in contact with prootic and basioccipital. Nasal bones elongate, the anterior end of the nasal bone lies lateral and dorsal to the external surface of the premaxilar. Seven supraneurals between head and anterior dorsal fin. Four branchiosegal rays. One to two epurals. 32–34 epineural, 23–24 epipleural, 11–13/12– 13 procurrent rays. Dorsal–fin margin oblique, second ray unbranched and first two branched rays longest. Pectoral girdle with sharp dorsal process on cleithrum reaching one–third length of supracleithrum. Cleithrum short. Pelvic–fin short, with tip of fin falling short of anal–fin origin. Pelvic bone elongate, short, straight and pointed; ischiatic process short, curved, with foramen in part upper and without apophysis. Caudal–fin unscaled, bifurcate with short lobe and pointed tips. Caudal–fin rays 10/9. Pored lateral line scales 40–43, extending from supracleithrum to hypural joint. Lateral line pores forming slight curve in ventral direction between first and eighth scales with rest in straight line. Total vertebrae 40–41.

Animal Biodiversity and Conservation 31.1 (2008)

Fig. 1. Hemibrycon rafaelense, paratype: MTD F 27623–27624; Colombia, Risaralda, Apia, San Rafael Creek at Apia River mouth, at 100 m of Santuario–Apia Road (5° 04' 54'' N; 75° 56' 36'' W). Fig. 1. Hemibrycon rafaelense, paratipo: MTD F 27623–27624; Colombia, Risaralda, Apia, arroyo de San Rafael en la desembocadura del río Apia, a 100 m de Santuario–carretera de Apia (5° 04' 54'' N; 75° 56' 36'' W).

Color in alcohol Body maroon. Lateral body stripe gray and broad. Dark humeral spot vertically elongate centered on second to fourth scale of scale row just dorsal to lateral line. Distal border of anal and dorsal fins dark. Pectoral and pelvic fins without pigmentation. Chromatophores on middle of caudal fin more intense.

very, more so ventrally. Pectoral and caudal–fins light brown, other fins hyaline. Humeral spot obscure, dark rounded. Middle caudal–fin rays with narrow dark pigmentation, a red spot on ventral portion of caudal fin base.

Color in life Dorsal region greenish–dark, lateral surface sil-

1 mm

pc1

pc2 ctm

Fig. 2. Premaxillar of Hemibrycon rafaelense, lateral view. Fig. 2. Premaxilar de Hemibrycon rafaelense, vista lateral.

pc3

Fig. 3. Left pectoral girdle and fin of Hemibrycon rafaelense, lateral view: ctm. Cleithrum; pc. Postcleithrum; sc. Supracleithrum. Fig. 3. Cintura pectoral y aleta izquierdos de Hemibrycon rafaelense, vista lateral: ctm. Cleitro; pc. Postcleitro; sc. Supracleitro.

Román–Valencia & Arcila–Mesa

8º

4º

78º Mar Caribe

74º

Río Cauca

12º

C. San Rafael

2000 0

2000 km

0 100 200 300 km 0º

Fig. 4. Distribution of Hemibrycon rafaelense (S means type locality), Colombia, Risaralda, Apia, San Rafael Creek at Apia River mouth, 100 m from Santuario–Apia Road (5° 04' 54'' N; 75° 56' 36'' W). Fig. 4. Distribución de Hemibrycon rafaelense (S significa localidad tipo), Colombia, Risaralda, Apia, arroyo de San Rafael en la desembocadura del río Apia, a 100 m de la carretera Santuario– Apia (5° 04' 54'' N; 75° 56' 36'' W).

Sexual dimorphism The males of H. rafaelense presented very small hooks on all except the caudal fin. Hooks were observed on anal–fin rays on the distal end of all branched rays. Distribution (fig. 4) San Rafael Creek and Apia Rriver in the Risaralda River system, upper Cauca.

Habitat Surface temperature 17.7°C, air temperature 17.8°C, dissolved oxygen 8.4 mg/l and 102% saturation, width 1–4 m, substrate stone and sand, water color clear. Etymology The specific epithet refers to San Rafael Creek, the drainage system where the new species was collected.

3.6 3 2.4 1.8 1.2

Component 2 –3.6

0.6 –3 –2.4 –1.8 –1.2 –0.6 –0.6 –1.2 –1.8 –2.4 –3 –3.6

0.6 1.2 1.8 2.4

3.6

Component 1

Fig. 5. Principal Component Analysis (PCA) of variation in five meristic data. Circles are the confidence limits exceeding 95% of species H. boquiae (+) and H. rafaelense (X). Fig. 5. Análisis de componentes principales (ACP) de la variación de cinco datos merísticos. Los círculos son los límites de confianza que exceden del 95%, de las especies H. boquiae (+) y H. rafaelense (X).

Animal Biodiversity and Conservation 31.1 (2008)

11.38

n = 47

n = 34

11.00

13.56

n = 34

12.00 13.00 14.00 Predorsal median scales

n = 47

41.15

42.38

41.00 41.50 42.00 42.50 43.00 Lateral line scales

Fig. 6. Bar graphs represent of 99% confidence levels for numbers of predorsal scales between H. boquiae (Hb) and H. rafaelense (Hr).

Fig. 7. Bar graphs represent of 99% confidence levels for numbers of lateral line scales with pores between H. boquiae (Hb) and H. rafaelense (Hr).

Fig. 6. Los gráficos de barras representan el 99% de nivel de confianza para el número de escamas predorsales comparando a H. boquiae (Hb) y H. rafaelense (Hr).

Fig. 7. Los gráficos de barras representan el 99% de nivel de confianza para número de escamas de la línea lateral con poros comparando a H. boquiae (Hb) y H. rafaelense (Hr).

Comments The morphometric characters provided little information to differentiate H. rafaelense from other Rio Magdalena Basin species and populations. Morphological differences between these similar forms are subtle. The first component of the PCA accounted for 40.24% (eigenvalue 2.81) of variability and the second 16.79% (1.17). Only a few specimens of H. rafaelense n. sp. overlapped

with individuals of H. boquiae (fig. 5 ). Meristic characters such as predorsal scales number (P [ 0001) (fig. 6) and the number of pored lateral line scales (P [ 0001) (fig. 7) allow the differentiation of H. rafaelense from H. boquiae. Males of both H. rafaelense and H. boquiae have very small hooks on all fins, except the caudal fin. This sexually dimorphic character was also reported in H. divisorensis (Bertaco et al., 2007).

Key to the species of Hemibrycon from the Magdalena River Basin. Clave para las especies de Hemibrycon de la cuenca del río Magdalena.

19–25 branched anal–fin rays; males with hooks only on anal and pelvic fins 24–28 branched anal–fin rays; males with a few hooks on all fins except caudal 13–14 predorsal scales; 42–44 line lateral scales; three unbranched anal–fin rays; scales from lateral line to dorsal fin base 5–6 10–12 predorsal scales; 40–42 line lateral scales; four unbranched anal–fin rays; scales from lateral line to dorsal fin base 6–8

H. colombianus 2

H. boquiae

H. rafaelense n. sp.

Román–Valencia & Arcila–Mesa

Key to the species of Hemibrycon from Atrato River Basin, Pacific drainage, Orinoco River and Amazon Basin. Clave para las especies de Hemibrycon de la cuenca del río Atrato, la vertiente del Pacífico, el río Orinoco y la cuenca del Amazonas.

Mature adults less than 40 mm standard length; mandibles unequal in length: superior longer than inferior; mouth subterminal; 14–16 anal fin rays; dentary with two large and two average sized teeth; caudal peduncle lacks dot; five supraneurals; humeral spot on first and second lateral line scales Mature adults larger than 45 mm standard length; mandibles equal, mouth terminal; 19–28 anal fin rays; dentary with one average–sized and three–four large teeth; caudal peduncle with dot; 6–8 supraneurals; humeral spot on third to fifth lateral line scales Lateral line rarely incomplete; caudal lobe base with small scales that extend 1/4 of length of caudal fin; caudal peduncle with small round black dot Lateral line complete; caudal lobe base with large scales that extend 1/4–1/2 of length of caudal fin; caudal peduncle with elongate black dot Tips of caudal fin lobes not dotted; medial band on caudal fins extends to the edge of the ventral caudal lobes; dorsal surface of metapterigoid without undulations; 23–26 branched anal–fin rays; 11–13 predorsal scales Tips of caudal fin lobes dotted; medial band on caudal fins does not extend to the edge ventral caudal lobes; dorsal surface of metapterigoide with two undulations; 26–31 branched anal–fin rays; 12–16 predorsal scales

H. microformaa

H. fredcochui

H. dariensis

H. metae

Phylogenetic analysis of Hemibrycon species is currently underway and is expected to support autapomorphy or diagnostic characters by description of new species from Colombia (Magdalena River) and Ecuador (Amazonian). In the present study we found that the number of teeth on the maxilla is not useful as either a taxonomic or a systematic character.

car–Lasso Alcalá (MHNLS), Hernan Ortega (MNH– UNMSM) Barry Chernoff and Mary Anne Rogers (FMNH), Yaneth Muñoz–S and Germán Galvis (ICNMNH), W. N. Eschmeyer and Jon Fong (CAS), José E. Castillo and Fabio Quevedo A. (IAvH), Richard P. Vari and Susan L. Jewett (USNM). Carlos García (IUQ) prepared fig. 1, Raquel I. Ruiz–C. (IUQ) figs. 2 and 3.

Acknowledgements

References

The Fundación para la Promoción de la Investigación y la Tecnología del Banco de la República of Colombia and University of Quindío (grant 212) financed the study; IDEA WILD provided field equipment. We further thank Richard P. Vari, Donald C. Taphorn (MCNG), Francisco Langeani, Axel Zarske, Raquel I. Ruiz C., Ignacio Doadrio, Rocio Rodiles– Hernández and Salvador Contreras–Balderas for suggestions and corrections. We also thank the following persons and museums for the loan of material under their care: Carlos Lasso and Os-

Bertaco, V. A., Malabarba, L. R., Hidalgo, M. & Ortega, H., 2007. A new species of Hemibrycon (Teleostei: Characiformes: Characidae) from the río Ucayali drainage, Sierra del Divisor, Peru. Neotropical Icthyology, 5(3): 251–257. Dahl, G., 1960. New fresh–water fishes from western Colombia. Caldasia, 8: 451–484. – 1971. Los peces del norte de Colombia. Inderena, Bogotá. Cundinamarca, Colombia. Dahl, G. & Medem, F., 1964. Informe sobre la fauna acuática del river Sinú. CVM, Monteria, Cordoba,

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Colombia. Eigenmann, C. H., 1913. Some results from an ichthyological reconnaissance of Colombia, South America. Part II. Ind. Univ. Stud., 131: 1–31. – 1922. The fishes of the northwestern South America. Mem. Carnegie Mus., 10: 1–348. – 1927. The American Characidae. Mem. Mus. Comp. Zool., 43: 311–428 + twenty–four plates. Eigenmann, C. H, Henn, A. &.Wilson, Ch., 1914. New Fishes from Western Colombia, Ecuador, and Peru. Ind. Univ. Stud., 19: 1–15. Géry, J., 1977. Characoids of the world. T. F. H. Publ. Inc. Ltd, Neptune city, New Jersey, U.S.A. Meek, E. S. & Hildebrand, S. F., 1916. The fishes of the freshwaters of Panama. Field. Mus. Nat. Hist., 10: 216–374. Miles, C., 1971. Los peces del Río Magdalena. U.T. Edic. Ibagué, Tolima, Colombia (Reprint). Román–Valencia, C., 2001. Redescripción de Hemibrycon boquiae, especie endémica de la quebrada Boquía en Alto Cauca, Colombia. Dahlia (Rev. Asoc. Colomb. Ictiol.), 4: 27–32. – 2004. Redescripción de Bryconamericus tolimae (Pisces: Characidae), endémica del Río Combeima, cuenca Río Magdalena, Colombia. Dahlia (Rev. Asoc. Colomb. Ictiol.), 7: 23–27. Román–Valencia, C. & Botero, A., 2006. Trophic and reproductive ecology of a species of Hemibrycon (Pisces: Characidae) in Tinajas creek, Quindio River drainage, upper Cauca basin, Colombia. Rev. Mus. Argentino Cienc. Nat., n. s., 8: 1–8. Román–Valencia, C. & Ruiz–C., R I., 2007. Una nueva especie de pez del género Hemibrycon (Characiformes: Characidae) del Alto Río Atrato, noroccidente de Colombia. Caldasia, 29: 121–131. Román–Valencia, C., Ruiz–C., R. I. & Barriga, R., 2006. Una nueva especie de pez del género Hemibrycon (Characiformes: Characidae). Int.

J. Trop. Biol., 54: 209–217. – 2007. Redescripción de Hemibrycon orcesi Böhlke 1958 y H. polyodon (Günther 1864) (Teleostei: Characidae), incluye clave para las especies de Hemibrycon en Ecuador. Animal Biodiversity and Conservation, 30.2: 179–187. Ruiz–C., R. I. & Román–Valencia, C., 2006. Osteología de Astyanax aurocaudatus Eigenmann, 1913 (Pisces, Characidae), con notas sobre la validez de Carlastyanax Géry, 1972. Animal Biodiversity and Conservation, 29: 49–64. Schultz, L. P., 1944. The fishes of the family characinidae from Venezuela, with description of seventeen new forms. Proc. U. S. Nat. Mus., 95: 235–367. Song, J. & Parenti, L. R., 1995. Clearing and staining whole fish specimens for simultaneous demostration of bone, cartilage and nerves. Copeia, 1995: 114–118. Taphorn, D. C., 1992. The characiform fishes of the Apure Río drainage, Venezuela. Biollania (edic. especial), 4: 1–534. Taylor, W. R. & Van Dyke, G. C., 1985. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9: 107–119. Vari, P. R., 1995. The neotropical fish family Ctenolucidae (Teleosti: Ostariophysi: Characiformes) supra and intrafamilial phylogenetic relationships, with a revisionary study. Smith. Contr. (Zool.), 564: 1–96. Vari, P. R. & Siebert, D. J., 1990. A new, unusually sexually dimorphic species of Bryconamericus (Pisces: Ostariophysi: Characidae) from the Peruvian Amazon. Proc. Biol. Soc. Wash., 103: 516–524. Weitzman, S. H., 1962. The osteology of Brycon meeki, a generalized characid fish, with an osteological definition of the family. Stanford Icthyol. Bull., 8: 1–50.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 31.1 (2008)

Revisión taxonómica de Helix zapateri Hidalgo, 1870 (Pulmonata, Trissexodontidae) y su nuevo estatus en la malacofauna ibérica A. Martínez–Ortí, J. R. Arrébola & A. Ruiz

Martínez–Ortí, A., Arrébola, J. R. & Ruiz, A., 2008. Revisión taxonómica de Helix zapateri Hidalgo, 1870 (Pulmonata, Trissexodontidae) y su nuevo estatus en la malacofauna ibérica. Animal Biodiversity and Conservation, 31.1: 77–81. Abstract Taxonomical revision of Helix zapateri Hidalgo, 1870 (Pulmonata, Trissexodontidae) and its new status in the Iberian malacofauna.— A taxonomic revision is made and the new generic assignation of the Iberian taxon Helix zapateri is discussed; its conchological features are compared with the most similar species, Hatumia pseudogasulli and Gasullia gasulli, both trissexodontids. Conchological studies allow us to conclude that Helix zapateri should be considered as a valid species and designated Hatumia zapateri, while H. pseudogasulli is a junior synonym of H. zapateri. Key words: Helix zapateri, Hatumia pseudogasulli, Trissexodontidae, Synonymy, Taxonomy, Revision, Iberian peninsula. Resumen Revisión taxonómica de Helix zapateri Hidalgo, 1870 (Pulmonata, Trissexodontidae) y su nuevo estatus en la malacofauna ibérica.— Se realiza la revisión taxonómica y se discute la nueva asignación genérica del taxon ibérico Helix zapateri, mediante la comparación de caracteres conquiológicos con las especies más similares, Hatumia pseudogasulli y Gasullia gasulli, ambas trissexodóntidos. Los estudios conquiológicos nos permiten concluir que Helix zapateri debe ser considerada como una especie válida y designarse como Hatumia zapateri, y que Hatumia pseudogasulli corresponde a un sinónimo posterior de H. zapateri. Palabras clave: Helix zapateri, Hatumia pseudogasulli, Trissexodontidae, Sinonimia, Taxonomía, Revisión, Península ibérica. (Received: 18 XII 07; Conditional acceptance: 8 II 08; Final acceptance: 18 II 08) A. Martínez–Ortí, Depto. de Zoología, Fac. de Biología, Univ. de València, Av. Dr. Moliner 50, E–46100 Burjassot, Valencia, España (Spain) y Museu Valencià d’Història Natural, Valencia, España (Spain).– J. R. Arrébola & A. Ruiz, Depto. de Fisiología y Zoología, Fac. de Biología, Univ. de Sevilla, Av. Reina Mercedes 6, E–41012 Sevilla, España (Spain). Corresponding author: A. Martínez–Ortí. E–mail: alberto.martinez@uv.es

ISSN: 1578–665X

Martínez–Ortí et al.

Introducción Durante los últimos años varios táxones ibéricos, que fueron descritos en el siglo XIX y XX, se han considerado, tras su revisión taxonómica, sinónimos posteriores de otras especies como por ejemplo Helix semipicta Hidalgo, 1870 de Helicella cistorum (Morelet, 1845) (Martínez–Ortí & Aparicio, 2003), Oestophora kuiperi Gasull, 1966 de Suboestophora boscae (Hidalgo, 1869) (Martínez– Ortí & Robles, 2002) y Trochoidea llopisi Gasull, 1981 de Xerocrassa geyeri (Soós, 1926) (Martínez– Ortí et al., 2000), mientras que otras se consideraron especies válidas, como Hohenwartiana disparata (Westerlund, 1892) (Martínez–Ortí, 2002). Helix zapateri Hidalgo, 1870 es otro de esos táxones ibéricos del que al no haber sido estudiado con profundidad y carecerse por ello de datos morfo– anatómicos, principalmente del aparato reproductor, no se conoce con exactitud su validez taxonómica y es considerado en la actualidad, respecto a su asignación genérica, como incertae sedis (Templado et al., 1993; Puente, 1994). Este taxon fue descrito por Hidalgo (1870) de la localidad cordobesa de Belalcazar (UTM: 30SUH1172) y dedicado a Bernardo Zapater, naturalista turolense contemporáneo suyo. La serie tipo está formada por tres ejemplares: el lectotipo depositado en el Museo Nacional de Ciencias Naturales de Madrid (MNCN nº 15.05/ 2754) (Templado et al., 1993) (fig. 5); un paralectotipo depositado en el Museum National d’Histoire Naturelle de París (Templado et al., 1993); y otro paralectotipo procedente de la colección Eduardo Boscá, que a su vez provenía de la colección Paz y Membiela, y que se encuentra depositado en la colección Siro de Fez en el Museu Valencià d’Història Natural de Valencia (MVHN) (Martínez–Ortí, 2001; Martínez–Ortí & Uribe, 2008) (figs. 6–10). Recientemente Arrébola et al. (2006) realizan un estudio sobre diversas especies de trissexodóntidos del sur de la península ibérica y del norte de África, y describen el nuevo género Hatumia [especie tipo Oestophora (Gasullia) riffensis Ortiz de Zárate, 1962], y una nueva especie, H. pseudogasulli Arrébola, Prieto et al., 2006, cuya

localidad típica es "Sierra Padrona, ctra. SE–179, km 10–11" (Sevilla; UTM: 29SQC5906). Se caracteriza por presentar la concha de color marrón pálido y brillante con la última vuelta redondeada, sin quilla, abertura sin labio interno, la teloconcha con la superficie granulosa tenue y la protoconcha provista de crestas espirales (Arrébola et al., 2006) (figs. 1–4). El aparato reproductor posee un flagelo corto, papila penial pequeña y ancha, siendo más delgada en el ápice, dos glándulas mucosas con digitaciones y un conducto de la bursa copulatrix corto y ancho e igual que el epifalo (Arrébola et al., 2006). Estos autores señalan diferencias con Gasullia gasulli (Ortiz de Zárate & Ortiz de Zárate, 1961), especie similar a H. pseudogasulli, tales como: (1) presencia de unas finas crestas espirales en la protoconcha de H. pseudogasulli; (2) una tenue granulación dispersa por el resto de la concha de H. pseudogasulli; (3) diferencias en la estructura del aparato estimulador; y (4) áreas de distribución separadas, aunque puede hallarse una pequeña zona de contacto entre las provincias de Sevilla y Huelva, donde llegan a convivir. Con las otras dos especies de Hatumia, H. riffensis y H. cobosi (Ortiz de Zárate, 1962), H. pseudogasulli puede diferenciarse fácilmente usando caracteres conquiológicos y/o del aparato reproductor (Arrébola et al., 2006). Con el fin de comprobar si Helix zapateri y Hatumia pseudogasulli corresponden o no a la misma especie, se comparan características conquiológicas, suficientes para su confirmación, como son la forma, las dimensiones, la coloración y la ornamentación de la protoconcha y de la teloconcha, entre otras. Además se presenta un mapa de distribución de ambos táxones. Material y métodos Material tipo estudiado Hatumia pseudogasulli (figs. 1–4): serie tipo depositada en el Departamento de Fisiología y Zoología de la Universidad de Sevilla (figs. 2–3)

Figs. 1–10. 1–4. Paratipos de Hatumia pseudogasulli Arrébola et al., 2006: 1. Ctra. J500 km 1 a 2 del Parque Natural de la Sierra de Andújar (Andujar, Jaén) (MVHN nº 1478) ( = 9,9 mm); 2–3. Ctra. CO– 142, Cerro del Olivo (PN Sierra de Hornachuelos) ( = 8,8 mm); 4. Detalle de la ornamentación de la protoconcha (Locus typicus). 5–10. Dos ejemplares de la serie tipo de Helix zapateri Hidalgo, 1870 (Belalcazar, Córdoba): 5. Lectotipo (MNCNM, nº 15.05/2754) ( = 10 mm); 6–7. Paralectotipo (MVHN nº 600) ( = 9,5 mm); 8–10. Detalle de la ornamentación de la protoconcha del paralectotipo. Figs. 1–10. 1–4. Paratypes of Hatumia pseudogaulli Arrébola et al., 2006: 1. Road J500 km 1–2, Sierra de Andújar Natural Park (Andujar, Jaén) (MVHN nº 1478) ( = 9.9 mm); 2–3. Road CO–142, Cerro del Olivo (Sierra de Hornachuelos Natural Park) ( = 8.8 mm); 4. Detail of the protoconch sculpture (Locus typicus). 5–10. Two specimens of the type series of Helix zapateri Hidalgo, 1870 (Belalcazar, Córdoba): 5. Lectotype (MNCNM nº 15.05/2754) ( = 10 mm); 6–7. Paralectotype (MVHN nº 600) ( = 9.5 mm); 8–10. Detail of the protoconch sculpture of the paralectotype.

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Fig. 11. Distribución geográfica de Hatumia zapateri Hidalgo 1870: O Locus typicus de Hatumia pseudogasulli; G Locus typicus de Helix zapateri; M Otras localidades de H. zapateri (como H. pseudogasulli en Arrébola et al., 2006). Fig. 11. Geographical distribution of Hatumia zapateri Hidalgo 1870: O Locus typicus of Hatumia pseudogasulli; G locus typicus of Helix zapateri; M Other localities of Hatumia zapateri (as H. pseudogasulli in Arrébola et al., 2006).

(Arrébola et al., 2006) y dos paratipos depositados en el MVHN (nº 1478) (fig. 1) [J500 km 1 a 2 del Parque Natural de la Sierra de Andújar, Andújar (Jaén; UTM = 30SVH0928)] (Martínez– Ortí & Uribe, 2008: p. 56). Helix zapateri (figs. 5–10): El lectotipo depositado en el MNCN (nº 15.05/2754) (fig. 5) y un paralectotipo depositado en el MVHN (nº 600) (fig. 6–7) (Martínez–Ortí, 2001; Martínez–Ortí & Uribe, 2008), y las fotografías del lectotipo (MNCN nº 15.05/2754) realizadas por Hidalgo (1875–1884: lám. 26: figs. 282–284) y por Templado et al. (1993: lám. XI, figs. 3a–c). En las microfotografías del paralectotipo de H. zapateri (figs. 8–10), realizadas en el microscopio electrónico de barrido HITACHI S–4100, no se utilizó el recubrimiento habitual con oro–paladio para no alterar las características propias de la concha. Resultados y discusión Templado et al. (1993) designan como lectotipo de Helix zapateri el ejemplar figurado por Hidalgo (1975– 1884, lám. 26, figs. 282–284) y cuyas medidas son 10 mm de diámetro mayor, 8,5 mm de diámetro menor y 4,6 mm de altura (fig. 5). Hidalgo (1870) indica las siguientes medidas para la especie: 10 mm diámetro máximo, 9 diámetro mínimo y 4,5 mm de altura. El paralectotipo depositado en MVHN mide 9,5 mm de diámetro máximo y 4,7 mm de altura. Por otra parte Arrébola et al. (2006) indican para

Hatumia pseudogasulli unas medidas entre 6,7 y 9,3 mm de diámetro y únicamente 5,0 mm de altura, sin indicar el rango de variación de la altura. Las dimensiones de las conchas de ambos taxones, publicadas por los diversos autores que los han estudiado, indican que todas las conchas de H. pseudogasulli y H. zapateri, estudiadas hasta el momento, presentan unas dimensiones similares. Se puede observar que la morfología de la concha del lectotipo de Helix zapateri (fig. 5) presenta una espira más alta que el paralectotipo depositado en el MVHN (fig. 6) y que a su vez corresponde a una forma más alta que el paratipo de Hatumia pseudogasulli (fig. 1) (Martínez– Ortí & Uribe, 2008: p. 56) y similar a la que presenta otro paratipo de H. pseudogasulli (fig.. 2), lo cual refuerza nuestra opinión. Además, el estudio de la ornamentación de la protoconcha y de la teloconcha ha sido otro factor determinante, y el más relevante, para conocer el estatus taxonómico de H. zapateri. La presencia de crestas espirales en las protoconchas (figs. 4, 8– 10) así como la granulación (figs. 4, 8–9), formada por pequeños y numerosos nódulos, distribuida por toda la superficie de la teloconcha, en ambos táxones, nos permite concluir que se trata en realidad de la misma especie, cuyo nombre, por ser descrito con anterioridad y por lo tanto tener prioridad según el CINZ, debe corresponder a Helix zapateri Hidalgo, 1870, con la nueva combinación Hatumia zapateri (Hidalgo, 1870), correspondiendo Hatumia pseudogasulli Arrébola et al., 2006, a un sinónimo posterior del primero. La anatomía del aparato reproductor y de la

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rádula de Hatumia zapateri son descritas y figuradas por Arrébola et al. (2006). Su distribución geográfica abarca las provincias de Córdoba (locus typicus), Jaén y Sevilla (fig. 11), sin descartar su posible presencia en otras provincias limítrofes. Agradecimientos Al Dr. Oscar Soriano, conservador de moluscos del Museo Nacional de Ciencias Naturales, por la cesión del lectotipo de Helix zapateri. También a la Sección de Microscopía Electrónica del S.C.S.I.E. de la Universitat de València por su ayuda en la utilización del microscopio electrónico de barrido. Trabajo subvencionado por el proyecto de investigación CGL–2005–01966 del Ministerio de Educación y Ciencia. Referencias Arrébola, J. R., Prieto, C. E., Puente, A. I. & Ruiz, A., 2006. Hatumia, a new genus for Oestophora riffensis Ortiz de Zárate, 1962, Oestophora cobosi Ortiz de Zárate, 1962 and Hatumia pseudogasulli (Pulmonata: Helicoidea: Trissexodontidae). Journal of Conchology, 39(2): 119–134. Hidalgo, J. G. B., 1870. Description de trois espèces nouvelles d’Helix d’Espagne. Journal de Conchyliologie, 19: 309–312. – 1875–84. Catálogo Iconográfico y descriptivo de los moluscos terrestres de España, Portugal y las Baleares. Ed. S. Martínez, Madrid. Martínez–Ortí, A., 2001. The mollucs type specimen’s preliminary study of the Museu Valencià d’Història Natural (Valencia, Spain). En:

Abstracts World Congress of Malacology. Unitas Malacologica: 209 (L. von Salvini–Plawen, J. Voltzow, H. Sattmann & G. Steiner, Eds.). Vienna. – 2002. Revisión taxonómica de Cionella (Hohenwartia) disparata Westerlund, 1892 (Gastropoda Pulmonata: Ferussaciidae). Iberus, 20(2): 1–9. Martínez–Ortí, A. & Aparicio, M. T., 2003. Taxonomical clarification of Helix semipicta Hidalgo, 1870 (Gastropoda Pulmonata: Hygromiidae). Journal of Conchology, 38(2): 1–5. Martínez–Ortí, A., Faci, G. & Robles, F., 2000. Taxonomical revision of Trochoidea (Xerocrassa) llopisi Gasull, 1981 (Gastropoda, Pulmonata, Hygromiidae, Geomitrinae), from the province of Castellón, Spain. Basteria (Leiden), 64: 7–14. Martínez–Ortí, A. & Robles, F., 2002. First anatomic data and taxonomical clarification of Suboestophora kuiperi (Gasull, 1966) (Mollusca, Gastropoda: Hygromiidae). Journal of Conchology, 37: 355–362. Martínez–Ortí A. & Uribe, F., 2008. Los ejemplares tipo de las colecciones malacológicas del Museu de Ciències Naturals de Barcelona y del Museu Valencià d’Història Natural. Arxius de Miscel·lànea Zoológica, 6: 1–156. Puente, A. I., 1994. Estudio taxonómico y biogeográfico de la superfamilia Helicoidea Rafinesque, 1815 (Gastropoda: Pulmonata: Stylommatophora) de la Península Ibérica e Islas Baleares. Tesis doctoral (inédita). Univ. del País Vasco, Bilbao. Templado, J., Baratech, L., Calvo, M., Villena, M. & Aparicio, M. T., 1993. Los “Ejemplares Tipo” de las colecciones malacológicas del Museo Nacional de Ciencias Naturales. C.S.I.C. Monografía, 9, Madrid.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 31.1 (2008)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (abans Miscel·lània Zoològica) és una revista inter disciplinària publicada, des de 1958, pel Museu de Ciències Naturals de Barcelona. Inclou articles d'investigació empírica i teòrica en totes les àrees de la zoologia (sistemàtica, taxonomia, morfologia, biogeografia, ecologia, etologia, fisiologia i genètica) procedents de totes les regions del món amb especial énfasis als estudis que d'una manera o altre tinguin relevància en la biología de la conservació. La revista no publica compilacions bibliogràfiques, catàlegs, llistes d'espècies o cites puntuals. Els estudis realit zats amb espècies rares o protegides poden no ser acceptats tret que els autors disposin dels permisos corresponents. Cada volum anual consta de dos fascicles. Animal Biodiversity and Conservation es troba registrada en la majoria de les bases de dades més importants i està disponible gratuitament a internet a http://www.bcn.cat/ABC, de manera que permet una difusió mundial dels seus articles. Tots els manuscrits són revisats per l'editor execu tiu, un editor i dos revisors independents, triats d'una llista internacional, a fi de garantir–ne la qualitat. El procés de revisió és ràpid i constructiu. La publicació dels treballs acceptats es fa normalment dintre dels 12 mesos posteriors a la recepció. Una vegada hagin estat acceptats passaran a ser propietat de la revista. Aquesta es reserva els drets d’autor, i cap part dels treballs no podrà ser reproduïda sense citar–ne la procedència.

Normes de publicació Els treballs s'enviaran preferentment de forma electrònica (abc@bcn.cat). El format preferit és un document Rich Text Format (RTF) o DOC que inclogui les figures i les taules. Les figures s'hauran d'enviar també en arxius apart en format TIFF, EPS o JPEG. Si s'opta per la versió impresa, s'han d'enviar quatre còpies del treball juntament amb una còpia en disquet a la Secretaria de Redacció. Cal incloure, juntament amb l'article, una carta on es faci constar que el treball està basat en investigacions originals no publicades anteriorment i que està sotmès a Animal Biodiversity and Conservation en exclusiva. A la carta també ha de constar, per a aquells treballs en que calgui manipular animals, que els autors disposen dels permisos necessaris i que compleixen la normativa de protecció animal vigent. També es poden suggerir possibles assessors. Quan l'article sigui acceptat, els autors hauran d'enviar a la Redacció una còpia impresa de la versió final acompanyada d'un disquet indicant el progra ma utilitzat (preferiblement en Word). Les proves d'impremta enviades a l'autor per a la correcció, seran retornades al Consell Editor en el termini de 10 dies. Aniran a càrrec dels autors les despeses degudes a modificacions substancials introduïdes ISSN: 1578–665X

per ells en el text original acceptat. El primer autor rebrà 50 separates del treball sense càrrec a més d'una separata electrònica en format PDF. Manuscrits Els treballs seran presentats en format DIN A–4 (30 línies de 70 espais cada una) a doble espai i amb totes les pàgines numerades. Els manuscrits han de ser complets, amb taules i figures. No s'han d'enviar les figures originals fins que l'article no hagi estat acceptat. El text es podrà redactar en anglès, castellà o català. Se suggereix als autors que enviïn els seus treballs en anglès. La revista els ofereix, sense cap càrrec, un servei de correcció per part d'una persona especialitzada en revistes científiques. En tots els casos, els textos hauran de ser redactats correctament i amb un llenguatge clar i concís. La redacció del text serà impersonal, i s'evitarà sempre la primera persona. Els caràcters cursius s’empraran per als noms científics de gèneres i d’espècies i per als neologis mes intraduïbles; les cites textuals, independentment de la llengua, seran consignades en lletra rodona i entre cometes i els noms d’autor que segueixin un tàxon aniran en rodona. Quan se citi una espècie per primera vegada en el text, es ressenyarà, sempre que sigui possible, el seu nom comú. Els topònims s’escriuran o bé en la forma original o bé en la llengua en què estigui escrit el treball, seguint sempre el mateix criteri. Els nombres de l’u al nou, sempre que estiguin en el text, s’escriuran amb lletres, excepte quan precedeixin una unitat de mesura. Els nombres més grans s'escriuran amb xifres excepte quan comencin una frase. Les dates s’indicaran de la forma següent: 28 VI 99 (un únic dia); 28, 30 VI 99 (dies 28 i 30); 28–30 VI 99 (dies 28 a 30). S’evitaran sempre les notes a peu de pàgina. Format dels articles Títol. Serà concís, però suficientment indicador del contingut. Els títols amb designacions de sèries numèriques (I, II, III, etc.) seran acceptats previ acord amb l'editor. Nom de l’autor o els autors. Abstract en anglès que no ultrapassi les 12 línies mecanografiades (860 espais) i que mostri l’essència del manuscrit (introducció, material, mètodes, resultats i discussió). S'evitaran les especulacions i les cites bibliogràfiques. Estarà encapçalat pel títol del treball en cursiva. Key words en anglès (sis com a màxim), que orientin sobre el contingut del treball en ordre d’importància. Resumen en castellà, traducció de l'Abstract. De la traducció se'n farà càrrec la revista per a aquells autors que no siguin castellanoparlants. Palabras clave en castellà. © 2008 Museu de Ciències Naturals

Adreça postal de l’autor o autors. (Títol, Nom, Abstract, Key words, Resumen, Pala bras clave i Adreça postal, conformaran la primera pàgina.) Introducción. S'hi donarà una idea dels antecedents del tema tractat, així com dels objectius del treball. Material y métodos. Inclourà la informació pertinent de les espècies estudiades, aparells emprats, mèto des d’estudi i d’anàlisi de les dades i zona d’estudi. Resultados. En aquesta secció es presentaran úni cament les dades obtingudes que no hagin estat publicades prèviament. Discusión. Es discutiran els resultats i es compa raran amb treballs relacionats. Els suggeriments de recerques futures es podran incloure al final d’aquest apartat. Agradecimientos (optatiu). Referencias. Cada treball haurà d’anar acompanyat de les referències bibliogràfiques citades en el text. Les referències han de presentar–se segons els models següents (mètode Harvard): * Articles de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Llibres o altres publicacions no periòdiques: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Treballs de contribució en llibres: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorals: Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Tesis doctoral, Uppsala University. * Els treballs en premsa només han d’ésser citats si han estat acceptats per a la publicació: Ripoll, M. (in press). The relevance of population

studies to conservation biology: a review. Anim. Biodivers. Conserv. La relació de referències bibliogràfiques d’un tre ball serà establerta i s’ordenarà alfabèticament per autors i cronològicament per a un mateix autor, afegint les lletres a, b, c,... als treballs del mateix any. En el text, s’indicaran en la forma usual: "... segons Wemmer (1998)...", "...ha estat definit per Robinson & Redford (1991)...", "...les prospeccions realitzades (Begon et al., 1999)..." Taules. Es numeraran 1, 2, 3, etc. i han de ser sempre ressenyades en el text. Les taules grans seran més estretes i llargues que amples i curtes ja que s'han d'encaixar en l'amplada de la caixa de la revista. Figures. Tota classe d’il·lustracions (gràfics, figures o fotografies) entraran amb el nom de figura i es numeraran 1, 2, 3, etc. i han de ser sempre ressen yades en el text. Es podran incloure fotografies si són imprescindibles. Si les fotografies són en color, el cost de la seva publicació anirà a càrrec dels au tors. La mida màxima de les figures és de 15,5 cm d'amplada per 24 cm d'alçada. S'evitaran les figures tridimensionals. Tant els mapes com els dibuixos han d'incloure l'escala. Els ombreigs preferibles són blanc, negre o trama. S'evitaran els punteigs ja que no es reprodueixen bé. Peus de figura i capçaleres de taula. Seran clars, concisos i bilingües en la llengua de l’article i en anglès. Els títols dels apartats generals de l’article (Intro ducción, Material y métodos, Resultados, Discusión, Conclusiones, Agradecimientos y Referencias) no aniran numerats. No es poden utilitzar més de tres nivells de títols. Els autors procuraran que els seus treballs originals no passin de 20 pàgines (incloent–hi figures i taules). Si a l'article es descriuen nous tàxons, caldrà que els tipus estiguin dipositats en una institució pública. Es recomana als autors la consulta de fascicles recents de la revista per tenir en compte les seves normes.

Animal Biodiversity and Conservation 31.1 (2008)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (antes Miscel·lània Zoològica) es una revista inter disciplinar, publicada desde 1958 por el Museo Ciencias Naturales de Barcelona. Incluye artículos de investigación empírica y teórica en todas las áreas de la zoología (sistemática, taxonomía, morfología, biogeografía, ecología, etología, fisiología y genéti ca) procedentes de todas las regiones del mundo, con especial énfasis en los estudios que de una manera u otra tengan relevancia en la biología de la conservación. La revista no publica compilaciones bibliográficas, catálogos, listas de especies sin más o citas puntuales. Los estudios realizados con es pecies raras o protegidas pueden no ser aceptados a no ser que los autores dispongan de los permisos correspondientes. Cada volumen anual consta de dos fascículos. Animal Biodiversity and Conservation está re gistrada en todas las bases de datos importantes y además está disponible gratuitamente en internet en http://www.bcn.cat/ABC, lo que permite una difusión mundial de sus artículos. Todos los manuscritos son revisados por el editor ejecutivo, un editor y dos revisores independientes, elegidos de una lista internacional, a fin de garan tizar su calidad. El proceso de revisión es rápido y constructivo, y se realiza vía correo electrónico siem pre que es posible. La publicación de los trabajos aceptados se realiza con la mayor rapidez posible, normalmente dentro de los 12 meses siguientes a la recepción del trabajo. Una vez aceptado, el trabajo pasará a ser propie dad de la revista. Ésta se reserva los derechos de autor, y ninguna parte del trabajo podrá ser reprodu cida sin citar su procedencia.

Normas de publicación Los trabajos se enviarán preferentemente de forma electrónica (abc@bcn.cat). El formato preferido es un documento Rich Text Format (RTF) o DOC, que incluya las figuras y las tablas. Las figuras deberán enviarse también en archivos separados en formato TIFF, EPS o JPEG. Si se opta por la versión impresa, deberán remitirse cuatro copias juntamente con una copia en disquete a la Secretaría de Redacción. Debe incluirse, con el artículo, una carta donde conste que el trabajo versa sobre investigaciones originales no publicadas anteriormente y que se somete en ex clusiva a Animal Biodiversity and Conservation. En dicha carta también debe constar, para trabajos donde sea necesaria la manipulación de animales, que los autores disponen de los permisos necesa rios y que han cumplido la normativa de protección animal vigente. Los autores pueden enviar también sugerencias para asesores. Cuando el trabajo sea aceptado los autores de berán enviar a la Redacción una copia impresa de la versión final junto con un disquete del manuscrito ISSN: 1578–665X

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preparado con un procesador de textos e indicando el programa utilizado (preferiblemente Word). Las pruebas de imprenta enviadas a los autores deberán remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Los gastos debidos a modifica ciones sustanciales en las pruebas de imprenta, intro ducidas por los autores, irán a cargo de los mismos. El primer autor recibirá 50 separatas del trabajo sin cargo alguno y una copia electrónica en for mato PDF. Manuscritos Los trabajos se presentarán en formato DIN A–4 (30 líneas de 70 espacios cada una) a doble espacio y con las páginas numeradas. Los manuscritos deben estar completos, con tablas y figuras. No enviar las figuras originales hasta que el artículo haya sido aceptado. El texto podrá redactarse en inglés, castellano o catalán. Se sugiere a los autores que envíen sus trabajos en inglés. La revista ofrece, sin cargo ningu no, un servicio de corrección por parte de una persona especializada en revistas científicas. En cualquier caso debe presentarse siempre de forma correcta y con un lenguaje claro y conciso. La redacción del texto deberá ser impersonal, evitándose siempre la primera persona. Los caracteres en cursiva se utilizarán para los nombres científicos de géneros y especies y para los neologismos que no tengan traducción; las citas textuales, independientemente de la lengua en que estén, irán en letra redonda y entre comillas; el nombre del autor que sigue a un taxón se escribirá también en redonda. Al citar por primera vez una especie en el trabajo, deberá especificarse siempre que sea posible su nombre común. Los topónimos se escribirán bien en su forma original o bien en la lengua en que esté redactado el trabajo, siguiendo el mismo criterio a lo largo de todo el artículo. Los números del uno al nueve se escribirán con letras, a excepción de cuando precedan una unidad de medida. Los números mayores de nueve se escribirán con cifras excepto al empezar una frase. Las fechas se indicarán de la siguiente forma: 28 VI 99 (un único día); 28, 30 VI 99 (días 28 y 30); 28–30 VI 99 (días 28 al 30). Se evitarán siempre las notas a pie de página. Formato de los artículos Título. Será conciso pero suficientemente explicativo del contenido del trabajo. Los títulos con designacio nes de series numéricas (I, II, III, etc.) serán aceptados excepcionalmente previo consentimiento del editor. Nombre del autor o autores. Abstract en inglés de 12 líneas mecanografiadas (860 espacios como máximo) y que exprese la esencia del manuscrito (introducción, material, métodos, resulta dos y discusión). Se evitarán las especulaciones y las citas bibliográficas. Irá encabezado por el título del trabajo en cursiva. © 2008 Museu de Ciències Naturals

Key words en inglés (un máximo de seis) que especifiquen el contenido del trabajo por orden de importancia. Resumen en castellano, traducción del abstract. Su traducción puede ser solicitada a la revista en el caso de autores que no sean castellano hablantes. Palabras clave en castellano. Dirección postal del autor o autores. (Título, Nombre, Abstract, Key words, Resumen, Palabras clave y Dirección postal conformarán la primera página.) Introducción. En ella se dará una idea de los ante cedentes del tema tratado, así como de los objetivos del trabajo. Material y métodos. Incluirá la información referente a las especies estudiadas, aparatos utilizados, me todología de estudio y análisis de los datos y zona de estudio. Resultados. En esta sección se presentarán úni camente los datos obtenidos que no hayan sido publicados previamente. Discusión. Se discutirán los resultados y se compara rán con otros trabajos relacionados. Las sugerencias sobre investigaciones futuras se podrán incluir al final de este apartado. Agradecimientos (optativo). Referencias. Cada trabajo irá acompañado de una bibliografía que incluirá únicamente las publicaciones citadas en el texto. Las referencias deben presentarse según los modelos siguientes (método Harvard): * Artículos de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773 * Libros y otras publicaciones no periódicas: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Trabajos de contribución en libros: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorales:

Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Tesis doctoral, Uppsala University. * Los trabajos en prensa sólo se citarán si han sido aceptados para su publicación: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. Las referencias se ordenarán alfabéticamente por autores, cronológicamente para un mismo autor y con las letras a, b, c,... para los trabajos de un mismo autor y año. En el texto las referencias bibliográficas se indicarán en la forma usual: "... según Wemmer (1998)...", "...ha sido definido por Robinson & Redford (1991)...", "...las prospecciones realizadas (Begon et al., 1999)..." Tablas. Se numerarán 1, 2, 3, etc. y se reseñarán todas en el texto. Las tablas grandes deben ser más estrechas y largas que anchas y cortas ya que deben ajustarse a la caja de la revista. Figuras. Toda clase de ilustraciones (gráficas, figuras o fotografías) se considerarán figuras, se numerarán 1, 2, 3, etc. y se citarán todas en el texto. Pueden incluirse fotografías si son imprescindibles. Si las fotografías son en color, el coste de su publicación irá a cargo de los autores. El tamaño máximo de las figuras es de 15,5 cm de ancho y 24 cm de alto. Deben evitarse las figuras tridimensionales. Tanto los mapas como los dibujos deben incluir la escala. Los sombreados preferibles son blanco, negro o trama. Deben evitarse los punteados ya que no se reproducen bien. Pies de figura y cabeceras de tabla. Serán claros, concisos y bilingües en castellano e inglés. Los títulos de los apartados generales del artículo (Introducción, Material y métodos, Resultados, Discusión, Agradecimientos y Referencias) no se numerarán. No utilizar más de tres niveles de títulos. Los autores procurarán que sus trabajos originales no excedan las 20 páginas incluidas figuras y tablas. Si en el artículo se describen nuevos taxones, es imprescindible que los tipos estén depositados en alguna institución pública. Se recomienda a los autores la consulta de fascícu los recientes de la revista para seguir sus directrices.

Animal Biodiversity and Conservation 31.1 (2008)

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an interdisciplinary journal published by the Natural Science Museum of Barcelona since 1958. It includes empirical and theoretical research from around the world that examines any aspect of Zool ogy (Systematics, Taxonomy, Morphology, Biogeography, Ecology, Ethology, Physiology and Genetics). It gives spe cial emphasis to studies related to Conservation Biology. The journal does not publish bibliographic compilations, listings, catalogues or collections of species, or isolated descriptions of a single specimens. Studies concerning rare or protected species will not be accepted unless the authors have been granted the relevant permits or authorisation. Each annual volume consists of two issues. Animal Biodiversity and Conservation is regis tered in all principal data bases and is freely available online at http://www.bcn.cat/ABC, assuring world–wide access to articles published therein. All manuscripts are screened by the Executive Editor, an Editor and two independent reviewers so as to guarantee the quality of the papers. The review process aims to be rapid and constructive. Once accepted, papers are published as soon as is practicable. This is usually within 12 months of initial submission. Upon acceptance, manuscripts become the prop erty of the journal, which reserves copyright, and no published material may be reproduced or cited without acknowledging the source of information.

Manuscripts must be presented in DIN A–4 format, 30 lines, 70 keystrokes per page. Maintain double spacing throughout. Number all pages. Manuscripts should be complete with figures and tables. Do not send original figures until the paper has been ac cepted. The text may be written in English, Spanish or Catalan, though English is preferred. The journal provides linguistic revision by an author’s editor. Care must be taken to use correct wording and the text should be written concisely and clearly. Scientific names of genera and species as well as untrans latable neologisms must be in italics. Quotations in whatever language used must be typed in ordinary print between quotation marks. The name of the author following a taxon should also be written in lower case letters. When referring to a species for the first time in the text, both common and scientific names should be given when possible. Do not capitalize common names of species unless they proper nouns (e.g. Iberian rock lizard). Place names may appear ei ther in their original form or in the langua ge of the manuscript, but care should be taken to use the same criteria throughout the text. Numbers one to nine should be written in full within the text except when preceding a measure. Higher numbers should be written in numerals except at the beginning of a sentence. Specify dates as follows: 28 VI 99 (for a single day); 28, 30 VI 99 (referring to two days, e.g. 28th and 30th), 28–30 VI 99 (for more than two consecu tive days, e.g. 28th to 30th). Footnotes should not be used.

Information for authors Electronic submission of papers is encouraged (abc@ bcn.cat). The preferred format is DOC or RTF. All figures must be readable by Word, embedded at the end of the manuscript and submitted together in a separate attachment in a TIFF, EPS or JPEG file. Tables should be placed at the end of the docu ment. If a printed version is sent, four copies should be forwarded to the Editorial Office, together with a copy on computer disc. A cover letter stating that the article reports original research that has not been published elsewhere and has been submitted exclusively for consideration in Animal Biodiversity and Conservation is also necessary. When animal manipulation has been necessary, the cover letter should also specify that the authors follow current norms on the protection of animal species and that they have obtained all relevant permits and authorisa tions. Authors may suggest referees for their papers. Once an article has been accepted, authors should send a paper copy and an electronic copy of the final version. Please identify software (preferably Word). Proofs sent to the authors for correction should be returned to the Editorial Board within 10 days. Expenses due to any substantial alterations of the proofs will be charged to the authors. The first author will receive 50 reprints free of charge and an electronic version of the article in PDF format. ISSN: 1578–665X

Formatting of articles Title. Must be concise but as informative as possible. Numbering of parts (I, II, III, etc.) should be avoided and will be subject to the Editor’s consent. Name of author or authors. Abstract in English, no longer than 12 typewritten lines (840 spaces), covering the contents of the article (introduction, material, methods, results and discussion). Speculation and literature citation should be avoided. The abstract should begin with the title in italics. Key words in English (no more than six) should express the precise contents of the manuscript in order of relevance. . Resumen in Spanish, translation of the Abstract. Summaries of articles by non–Spanish speaking authors will be translated by the journal on request. Palabras clave in Spanish. Address of the author or authors. (Title, Name, Abstract, Key words, Resumen, Palabras clave and Address should constitute the first page.) Introduction. Should include the historical back ground of the subject as well as the aims of the paper. © 2008 Museu de Ciències Naturals

Material and methods. This section should provide relevant information on the species studied, materi als, methods for collecting and analysing data, and the study area. Results. Report only previously unpublished results from the present study. Discussion. The results and their comparison with related studies should be discussed. Suggestions for future research may be given at the end of this section. Acknowledgements (optional). References. All manuscripts must include a bibliog raphy of the publications cited in the text. References should be presented as in the following examples (Harvard method): * Journal articles: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Books or other non–periodical publications: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Contributions or chapters of books: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Ph. D. Thesis: Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Ph. D. Thesis, Uppsala University. * Works in press should only be cited if they have been accepted for publication: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. References must be set out in alphabetical and

chronological order for each author, adding the letters a, b, c,... to papers of the same year. Bibliographic citations in the text must appear in the usual way: "... according to Wemmer (1998)...", "...has been defined by Robinson & Redford (1991)...", "...the prospections that have been carried out (Begon et al., 1999)..." Tables. Must be numbered in Arabic numerals with reference in the text. Large tables should be narrow (across the page) and long (down the page) rather than wide and short, so that they can be fitted into the column width of the journal. Figures. All illustrations (graphs, drawings, photo graphs) should be termed as figures, and numbered consecutively in Arabic numerals (1, 2, 3, etc.) with reference in the text. Glossy print photographs, if essential, may be included. The Journal will publish colour photographs but the author will be charged for the cost. Figures have a maximum size of 15.5 cm wide by 24 cm long. Figures should not be tridimen sional. Any maps or drawings should include a scale. Shadings should be kept to a minimum and preferably with black, white or bold hatching. Stippling should be avoided as it may be lost in reproduction. Legends of tables and figures. Legends of tables and figures should be clear, concise, and written both in English and Spanish. Main headings (Introduction, Material and methods, Results, Discussion, Acknowledgements and Refer ences) should not be numbered. Do not use more than three levels of headings. Manuscripts should not exceed 20 pages including figures and tables. If the article describes new taxa, type material must be deposited in a public institution. Authors are advised to consult recent issues of the journal and follow its conventions.

Animal Biodiversity and Conservation 31.1 (2008)

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Animal Biodiversity and Conservation 31.1 (2008)

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Animal Biodiversity and Conservation 31.1 (2008)

Arxius de Miscel·lània Zoològica vol. 5 (2007) 2008 Museu de Ciències Naturals ISSN: 1698–0476

Índex/Índice/Contents Del Pilar Ruso, Y. & Bayle Sempere, J. T., 2007. Ictioplancton asociado a praderas de Posidonia oceanica durante la época estival en la reserva marina de Tabarca. Arxius de Miscel·lània Zoològica, vol. 5: 1–11. Abstract Ichthyoplankton associated with P. oceanica meadows during the summer season in the Tabarca marine reserve.— Habitat complexity plays a key role in survival in early stages of fish larvae. We investigated fish larvae assemblage and its relation with P. oceanicaseagrass at the Tabarca Island Marine Reserve. Samples were taken using moored plankton nets at two depths (0 and 2 m from P. oceanica meadow) over five consecutive days in July 2000. Three hundred and fifty–three larvae were captured. The mostabundant families were Clupeidae (31%), Sparidae (27%), Engraulidae (11%) and Gobiidae (6%). We observed that small fish larvae were able to select nursery areas. We conclude that the P. oceanica leaf canopy is a major factor in structuring the larval fish assemblages of some demersal species. Key words: Fish larvae, Seagrasses, Habitat shelter, Moored plankton nets. Sanuy Castells, D., 2007. Fauna vertebrada de les zones semiàrides protegides de Catalunya. Arxius de Miscel·lània Zoològica, vol 5: 12–42. Abstract Vertebrate fauna of the protected semiarid zones in the south west of Catalonia.— This work describes fauna and habitats within the semiarid zones in the south west of Catalonia, bordering with Monegros. The fauna in the Peins area is studied and an approximation of the vertebrate species therein is given. As parts of the area surveyed are legally protected, their future is considered stable. The eight areas studied include steppe zones, chalky mountain ranges bordering the pre–Pyrenean region, Pinus halepensis forest and a dam. Key words: Biodiversity, Vertebrates, Semiarid zones, Catalonia.

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Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Les cites o els abstracts dels articles d’Animal Biodiversity and Conservation es resenyen a / Las citas o los abstracts de los artículos de Animal Biodiversity and Conservation se mencionan en / Animal Biodiversity and Conservation is cited or abstracted in: Abstracts of Entomology, Agrindex, Animal Behaviour Abstracts, Anthropos, Aquatic Sciences and Fisheries Abstracts, Behavioural Biology Abstracts, Biological Abstracts, Biological and Agricultural Abstracts, Current Primate References, DIALNET (Difusión de Alertas en la Red), DOAJ (Directory of Open Access Journals), Ecological Abstracts, Ecology Abstracts, Entomology Abstracts, Environmental Abstracts, Environmental Periodical Bibliography, Genetic Abstracts, Geographical Abstracts, Índice Español de Ciencia y Tecnología, International Abstracts of Biological Sciences, International Bibliography of Periodical Literature, International Developmental Abstracts, Marine Sciences Contents Tables, Oceanic Abstracts, RACO (Revistes Catalanes amb Accés Obert), Recent Ornithological Literature, Referatirnyi Zhurnal, Science Abstracts, Scientific Commons, Serials Directory, Ulrich’s International Periodical Directory, Zoological Records.

Índex / Índice / Contents Animal Biodiversity and Conservation 31.1 (2008) ISSN 1578–665X

1–13 X. Chen Topological properties in the spatial distri bution of amphibians in Alabama USA for the use of large scale conservation

47–56 E. Muths & V. Dreitz Monitoring programs to assess reintroduc tion efforts: a critical component in reco very

15–27 C. Román–Valencia, D. C. Taphorn B. & R. I. Ruiz–C. Two new Bryconamericus: B. cinarucoense n. sp. and B. singularis n. sp. (Characi formes, Characidae) from the Cinaruco River, Orinoco Basin, with keys to all Ve nezuelan species

57–66 V. Borredà & A. Martínez–Ortí Descripción de un nuevo limácido de Me norca (Islas Baleares): Gigantomilax (Vitrinoides) benjaminus sp. n. (Gastropoda, Pulmonata)

29–39 P. W. W. Lurz, M. D. F. Shirley & N. Geddes Monitoring low density populations: a pers pective on what level of population decline we can truly detect

67–75 C. Román–Valencia & D. K. Arcila–Mesa Hemibrycon rafaelense n. sp. (Characi formes, Characidae), a new species from the upper Cauca River, with keys to Colom bian species

41–46 D. Sanuy, N. Oromí & A. Galofré Effects of temperature on embryonic and larval development and growth in the nat terjack toad (Bufo calamita) in a semi–arid zone

77–81 A. Martínez–Ortí, J. R. Arrébola & A. Ruiz Revisión taxonómica de Helix zapateri Hidalgo, 1870 (Pulmonata, Trissexodon tidae) y su nuevo estatus en la malacofauna ibérica