ABC 44-1 (2021)

en J. Hatchwell, Univ. of Sheffield, UK

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Animal Biodiversity and Conservation 44.1, 2021 © 2021 Museu de Ciències Naturals de Barcelona, Consorci format per l'Ajuntament de Barcelona i la Generalitat de Catalunya Autoedició: Montserrat Ferrer Fotomecànica i impressió: CEVAGRAF SCCL ISSN: 1578–665 X eISSN: 2014–928 X Dipòsit legal: B. 5357–2013

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Animal Biodiversity and Conservation 44.1 (2021)

Editor en cap / Editor responsable / Editor in Chief Joan Carles Senar Museu de Ciències Naturals de Barcelona, Barcelona, Spain Editors temàtics / Editores temáticos / Thematic Editors Ecologia / Ecología / Ecology: Mario Díaz (Asociación Española de Ecología Terrestre – AEET) Comportament / Comportamiento / Behaviour: Adolfo Cordero (Sociedad Española de Etología y Ecología Evolutiva – SEEEE) Biologia Evolutiva / Biología Evolutiva / Evolutionary Biology: Santiago Merino (Sociedad Española de Biología Evolutiva – SESBE) Editors / Editores / Editors Pere Abelló Institut de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Pelayo Acevedo Instituto de Investigación en Recursos Cinegéticos IREC–UCLM–CSIC–JCCM, Ciudad Real, Spain Javier Alba–Tercedor Universidad de Granada, Granada, Spain Russell Alpizar–Jara University of Évora, Évora, Portugal Marco Apollonio Università degli Studi di Sassari, Sassari, Italy Pedro Aragón Universidad Complutense de Madrid, Madrid, Spain Miquel Arnedo Universitat de Barcelona, Barcelona, Spain Xavier Bellés Institut de Biología Evolutiva UPF–CSIC, Barcelona, Spain Agustín Camacho Instituto de Biociências–USP, São Paulo, Brasil David Canal MTA Centre for Ecological Research, Vácrátót, Hungary Gonçalo C. Cardoso CIBIO–InBIO, Universidade do Porto, Portugal Salvador Carranza Institut de Biologia Evolutiva UPF–CSIC, Barcelona, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Martina Carrete Universidad Pablo de Olavide, Sevilla, Spain Pablo Castillo Institute for Sustainable Agriculture–CSIC, Córdoba, Spain Adolfo Cordero Universidad de Vigo, Vigo, Spain Mario Díaz Museo Nacional de Ciencias Naturales MNCN–CSIC, Madrid, Spain Darí o Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain José A. Donazar Estación Biológica de Doñana EBD–CSIC, Sevilla, Spain Arnaud Faille Museum National histoire naturelle, Paris, France Jordi Figuerola Estación Biológica de Doñana EBD–CSIC, Sevilla, Spain Gonzalo Giribet Museum of Comparative Zoology, Harvard University, Cambridge, USA Susana González Universidad de la República–UdelaR, Montivideo, Uruguay Jacob González–Solís Universitat de Barcelona, Barcelona, Spain Sidney F. Gouveia Universidad Federal de Sergipe, Sergipe, Brasil Gary D. Grossman University of Georgia, Athens, USA Ben J. Hatchwell University of Sheffield, Sheffield, UK Joaquín Hortal Museo Nacional de Ciencias Naturales MNCN–CSIC, Madrid, Spain Jacob Höglund Uppsala University, Uppsala, Sweden Damià Jaume IMEDEA–CSIC, Universitat de les Illes Balears, Esporles, Spain Miguel A. Jiménez–Clavero Centro de Investigación en Sanidad Animal–INIA, Madrid, Spain Jennifer A. Leonard Estación Biológica de Doñana EBD–CSIC, Sevilla, Spain Andras Liker University of Pannonia, Veszprém, Hungary Jordi Lleonart Institut de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Josep Lloret Universitat de Girona, Girona, Spain Jorge Mª Lobo Museo Nacional de Ciencias Naturales MNCN–CSIC, Madrid, Spain Pablo J. López–González Universidad de Sevilla, Sevilla, Spain Ian MacGregor–Fors University of Helsinki, Lahti, Finland Jose Martin Museo Nacional de Ciencias Naturales MNCN–CSIC, Madrid, Spain Juan F. Masello Justus Liebig University Giessen, Giessen, Germany Santiago Merino Museo Nacional de Ciencias Naturales MNCN–CSIC, Madrid, Spain Manuel B. Morales CIBC–Universidad Autónoma de Madrid, Madrid Spain Juan J. Negro Estación Biológica de Doñana EBD–CSIC, Sevilla, Spain Daniel Oro Centre d’Estudis Avançats de Blanes CEAB–CSIC, Girona, Spain Vicente M. Ortuño Universidad de Alcalá de Henares, Alcalá de Henares, Spain Miquel Palmer IMEDEA–CSIC, Universitaat de les Illes Balears, Esporles, Spain Per Jakob Palsbøll University of Groningen, Groningen, The Netherlands Reyes Peña Universidad de Jaén, Jaén, Spain Javier Perez–Barberia Estación Biológica de Doñana EBD–CSIC, Sevilla, Spain Juan M. Pleguezuelos Universidad de Granada, Granada, Spain Oscar Ramírez Institut de Biologia Evolutiva UPF–CSIC, Barcelona, Spain Montserrat Ramón Institut de Ciències del Mar CMIMA­–CSIC, Barcelona, Spain Alex Richter–Boix CREAF, Univ. Autònoma de Barcelona, Bellaterra, Spain Diego San Mauro Universidad Complutense de Madrid, Madrid, Spain Ana Sanz–Aguilar IMEDEA, CSIC-UIB, Illes Balears, Spain Rafael Sardà Centre d’Estudis Avançats de Blanes CEAB–CSIC, Girona, Spain Ramón C. Soriguer Estación Biológica de Doñana EBD–CSIC, Sevilla, Spain Constantí Stefanescu Museu de Ciències Naturals de Granollers, Granollers, Spain Diederik Strubbe University of Antwerp, Antwerp, Belgium Miguel Tejedo Madueño Estación Biológica de Doñana–CSIC, Sevilla, Spain José L. Tellería Universidad Complutense de Madrid, Madrid, Spain Simone Tenan Institute of Marine Sciences (CNR–ISMAR), National Research Council, Venezia, Italy Francesc Uribe Museu de Ciències Naturals de Barcelona, Barcelona, Spain José Ramón Verdú CIBIO, Universidad de Alicante, Alicante, Spain Carles Vilà Estación Biológica de Doñana EBD–CSIC, Sevilla, Spain Rafael Villafuerte Inst.ituto de Estudios Sociales Avanzados IESA–CSIC, Cordoba, Spain Rafael Zardoya Museo Nacional de Ciencias Naturales MNCN–CSIC, Madrid, Spain

Animal Biodiversity and Conservation 44.1 (2021)

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The names of southwestern European goats: is Iberian ibex the best common name for Capra pyrenaica?

R. García–González, J. Herrero, C. Nores

García–González, R., Herrero, J., Nores, C., 2021. The names of southwestern European goats: is Iberian ibex the best common name for Capra pyrenaica? Animal Biodiversity and Conservation, 44.1: 1–16, Doi: https://doi.org/10.32800/abc.2021.44.0001 Abstract The names of southwestern European goats: is Iberian ibex the best common name for Capra pyrenaica? The common name designated to a species is important because it connects specialists with non–experts. The matter of the correct common name is relevant to the conservation and management of conspicuous or flag species.

The English name 'Spanish ibex' to designate Capra pyrenaica is extensive in the scientific literature, and some have defended its appropriateness. However, in our opinion, it is not the best term to designate this species.

We propose that 'Iberian wild goat' should be used. Herein, we review the etymology, history, taxonomy and public use of the names used to designate goats (domestic and wild) in southwestern Europe during the last two millennia. Used first by Pliny the Elder, the name 'ibex' has been applied most often for the Alpine wild goat (C. ibex), and few authors applied this name to C. pyrenaica until the 20th century when some influential works extended its use in the scientific literature. Adult males of C. pyrenaica have lyre–shaped, and typically smooth horns that do not match the ibex morphotype, which has scimitar–shaped knotted horns. Although C. pyrenaica and C. ibex are probably phylogenetically close, their common names do not necessarily have to match. The rules of common names differ from those of scientific names. Cabra montés or cabra brava (wild goat) is the common name used by most authors in the Iberian peninsula. This name is deeply entrenched in the Iberian languages and has been used since the earliest references to the species in mediaeval times. We propose the adoption of 'Iberian wild goat' for legal and scientific communication and when interacting with the media.

Key words: Caprinae, Wild goat, Spanish ibex, Conservation value, Historical taxonomy, Capra ibex.

Resumen Los nombres de las cabras del sudoeste de Europa: ¿"Iberian ibex" es el nombre común más adecuado para designar a Capra pyrenaica? El nombre común asociado a una especie es importante porque sirve de nexo entre los especialistas y las personas no expertas. El uso correcto del nombre común es importante para la conservación y gestión de las especies clave o emblemáticas. En las publicaciones científicas en inglés es muy frecuente denominar "Spanish ibex" a Capra pyrenaica y algunos autores defienden la idoneidad de esta opción, pero en nuestra opinión no es el mejor término para designar a esta especie. En este artículo proponemos el término "Iberian wild goat" y revisamos la etimología, la historia, la taxonomía y el uso del público en general de los nombres usados para designar a las cabras (domésticas y salvajes) en el sudoeste de Europa durante los dos últimos milenios. Utilizado por primera vez por Plinio el Viejo, el nombre "íbice" se ha aplicado en la mayor parte de los casos a la cabra salvaje de los Alpes (C. ibex) y son pocos los autores que lo aplicaron a C. pyrenaica hasta el siglo XX, cuando algunas obras influyentes extendieron su uso en las publicaciones científicas. Los machos adultos de C. pyrenaica tienen cuernos lisos en forma de lira, que no se corresponden con el morfotipo de ibex, que tiene cuernos con nudosidades en forma de cimitarra. Aunque C. pyrenaica y C. ibex probablemente sean dos especies próximas desde el punto de vista filogenético, sus nombres comunes no necesariamente tienen que coincidir. Los nombres comunes siguen reglas diferentes a las de los nombres científicos.

"Cabra montés" o "cabra brava" (wild goat en inglés) son los nombres comunes utilizados mayoritariamente por los autores de la península ibérica. Estos nombres están profundamente arraigados en las lenguas ibéricas y se han utilizado desde las primeras referencias a la especie en la Edad Media. Proponemos que se adopte el término "Iberian wild goat" en textos jurídicos y científicos y en la interacción con los medios de comunicación.

ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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García–González et al.

Palabras clave: Caprinae, Cabra montés, Íbice ibérico, Valor de conservación, Taxonomía histórica, Capra ibex.

Received: 07 II 20; Conditional acceptance: 21 IV 20; Final acceptance: 17 VII 20 Ricardo García–González, Instituto Pirenaico de Ecología IPE–CSIC, Avda. Nuestra Señora de la Victoria 16, 22700 Jaca, Spain.– Juan Herrero, Area of Ecology. Department of Agrarian and Environmental Sciences, Technical School, University of Zaragoza, 22718 Huesca, Spain.– Carlos Nores, INDUROT, University of Oviedo, 33600 Mieres, Spain.

Corresponding author: Ricardo García–González. E–mail: rgarciag@ipe.csic.es ORCID ID: R. García–González: 0000-0001-5625-8690

Animal Biodiversity and Conservation 44.1 (2021)

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Introduction

Methods

As elements of animal production, hunting and mythology objects, goats (Capra genus) have attracted much attention throughout human history.

The naming, description and classification of goats in southwestern Europe can be traced back to the first books of natural history by the Greek and Roman classics (Aristotle and Pliny the Elder, among others). The nomenclature and scientific classification of goats has been varied and controversial over the past two millennia (Ellerman and Morrison–Scott, 1951; appendix 1). Until Linnaeus and even later, the nomenclature was confusing, with common and pseudoscientific names being used interchangeably (Jonston, 1650; Pennant, 1793). Recently, with the generalization of molecular techniques, great advances have been made in the phylogeny of the genus, even though this is not completely resolved (Groves and Grubb, 2011).

The common name associated with a given taxon is important from scientific, conservation, and legislative perspectives. Common names have biological and practical importance given that they allow everyone from researchers to scientific popularisers and the general public to easily understand which species others are referring to. Usually, these names are recognizable, easy to pronounce and stable over time. The common names of the species should link the scientific world with lay people to increase the species conservation value (Stevens et al., 2014). Conversely, scientific names follow binomial nomenclature and are based on phylogenetic relationships, but they are written in Latin and are difficult to remember.

Capra pyrenaica is a conspicuous and endemic species of the Iberian peninsula, iconic for many nature enthusiasts, conservationists, and hunters.

The matter of the correct common name is relevant to its conservation and management. The common name 'Spanish' or 'Iberian ibex' designating the species C. pyrenaica is widespread in contemporary English–language publications. However, a significant number of publications also use the term 'Iberian or Spanish wild goat' (appendix 2).

In this work we provide arguments to support this latter option.

This work is divided into four sections. In the first two sections we conduct a detailed review of the names that goats have received in southwestern Europe, as well as the history of their taxonomic classification. In the third section we discuss the usefulness of using morphological and molecular criteria in establishing phylogenies, and in the last section we discuss the conservation value of common names regardless of the phylogenetic classification of the taxa.

We provide arguments to demonstrate that 'Iberian wild goat' is a more suitable common name than Iberian ibex for C. pyrenaica, and given the importance of common names for conservation and management, we suggest that the first term be adopted or used preferably over the second.

We searched the scientific literature for the origin, meaning, and use of the common names for C. pyrenaica.

The search was restricted to the wild goats of southwestern Europe. The search went back to the time prior to modern Zoology (Gessner, 1551; Linnaeus, 1758), including the classical Natural History texts of the Greeks and Romans, which influenced the early modern scientists. We searched classic pre–Linnaean texts and their translations from Greek and Latin in free–open bibliographic databases including biodiversitylibrery.org, thelatinlibrary.com, archive.org, penelope.uchicago.edu, remacle.org, perseus.tufts.edu, bibdigital.rjb.csic.es, reader.digitale–sammlungen.de, es.scribd.com, books.google. es, en.wikipedia.org, gallica.bnf.fr, bl.uk, e–codices. unifr.ch, and private libraries including getty.edu, linnean–online.org, merriam–webester.com, themorgan. org. For some classical texts in Spanish, especially hunting treatises, we used open–free databases such as aic.uva.es, bvpb.mcu.es, datos.bne.es, and especially the diacronic database of the Royal Spanish Academy (corpus.rae.es). Within classical texts, to determine their etymology and historical use, the words associated with wild goats (e.g., ibex, capra, hircus, tragus, goat, Steinbock, bouquetin) were searched.

In addition, we sought the opinions of historians and etymologists who were familiar with Iberian fauna, particularly, C. pyrenaica.

Among post–Linnaean documents, we reviewed the history of the taxonomy of Capra ibex and C. pyrenaica based on original scientific descriptions. We also searched for the use of their common names in subsequent catalogs and reference treaties (Pallas, 1776; Erxleben, 1777; Pennant, 1793; Saint–Hilaire and Cuvier, 1824–1842; Cuvier et al., 1827–1835; Gray, 1850–1852; Lydekker, 1898; Ellerman and Morrison–Scott, 1951; Heptner et al., 1989; Pidancier et al., 2006; Groves and Grubb, 2011). We synthesized the information to identify the most frequently used common names for C. pyrenaica and to determine how the name 'Spanish ibex' had come into use in contemporary scientific literature. Recent studies (e.g., paleontological, morphological, molecular) on the phylogenetic relationships among species (C. aegagrus, C. ibex, C. pyrenaica) were evaluated.

In this paper, we followed Shackleton's (1997) taxonomic nomenclature for the C. pyrenaica subspecies, although their taxonomic status remains under debate (García–González, 2011; Angelone–Alassad et al., 2017; Ureña et al., 2018). The Alpine ibex is considered as a single species: C. ibex, and not as a subspecies (Aulagnier et al., 2008).

Nomenclature of bezoars and domestic goats Domestic goats (C. hircus) and their attributed wild ancestors (C. aegagrus or bezoars) share a significant proportion of their genetic pools (Naderi et al., 2008; Colli et al., 2015), and hybridization between them is common (Couturier, 1962, p. 527). The genetic similarity is most pronounced in the goats of some

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Mediterranean islands where they were introduced in the early stages of domestication (between 10,000 to 8,000 years BP) and are currently considered to be subspecies of C. aegagrus (Horwitz and Bar–Gal, 2006; Masseti, 2009; Geskos, 2013).

If it is assumed that C. aegagrus and C. hircus are the same species, the specific name for both should be C. aegagrus based on the Opinion 2027 of the International Commission of Zoological Nomenclature (ICZN, 2003), which, if applicable, assigns to each variety (wild or domestic) the category of subspecies. Although, some refer to the domestic goat as C. aegagrus hircus and the wild goat as C. aegagrus aegagrus, most refer to them as C. hircus and C. aegagrus, respectively. Until a consensus on the specific identity of bezoars and domestic goats is reached, we prefer to use the classical nomenclature for reasons of clarity and simplification.

term is derived from the ancient tradition of paying Greek actors (tragedians, tragoedus) with a domestic goat. In addition, Greek texts use the word aie (αιε) which is equivalent to caper in Latin (Oppian, 215 AD in Graells, 1897; van Oppenraaij, 1998).

The origin of the term Capra is uncertain. For some (Barcia, 1902), it derives from the Greek word Kápros (κάπρος), which was used to designate the males of some wild species such as wild boar Sus scrofa (Coromines and Pascual, 1984). Thereafter, it evolved into the Latin terms Capra and Caper (De Funes y Mendoza, 1621). In early modern Zoology texts, it was used to describe domestic goats (Gessner, 1551; Jonston, 1650). Apparently, over time, the use of the term became restricted to females, and the terms used for males were tragos (of Greek origin), hircus (of Latin origin), or buck (of Germanic origin).

For instance, in Spanish, the term cabra is used to designate females of Capra and chamois Rupicapra.

Etymology of the common names of Capra spp. in Western Europe

Words of Latin origin (caper, hircus, ibex)

Words of Greek origin (aegagrus, tragos, capra?)

In classical natural history texts, most descriptions of goats refer to domestic goats (Pliny the Elder, 77 AD; Gessner, 1551; Jonston, 1650; Aristotle and Thompson, 2004; Voultsiadou and Tatolas, 2005). However, wild goats were mentioned as early as in the 8th century (C.) BC by Homer in the Iliad and the Odyssey. Both texts indicate that wild goats were abundant on the islands in the Aegean Sea (Buxton, 1892, p. 193). The primary classical Greek authors who mentioned wild goats referred to them as αἶγας ἀγρίας (transliterated aiga agrios), which means 'wild goat'. The contraction of those terms resulted in αίγαγρος (aigagros), which became aegagrus, used to scientifically name Capra aegagrus Erxleben, 1777 (as early as the 5th C. Boe­ thius explained that two separate terms did not have the same meaning after they had been combined into a single term (Migne, 1874); for example, a hippo­ potamus is not a 'river horse', and a blackbird Turdus merula is not any black bird; rather, it is a specific species). Today, the common name for C. aegagrus is agrimi, bezoar, or pasang, and some authors (Groves and Grubb, 2011) have argued that it is the 'true' wild goat, as opposed to the domestic goat Capra hircus.

One of the several observations about wild goats in Aristotle's 'History of Animals' is a description of their capacity to cure their own arrow wounds (Barthélemy–Saint–Hilaire, 1883), which was derived from their habit of feeding on dictame (Dictamnus sp.). On that account, this was perpetuated by others (De Funes y Mendoza, 1621; Pennant, 1793; Lindsay, 1911), reflecting the strong influence of classical authors on subsequent natural history texts.

Tragos (τράγος) is another Greek term associated with the common name of Capra which was used as a synonym of Capra in the early modern Zoology texts (Klein, 1751) and also to designate the male goat (De Funes y Mendoza, 1621; De la Huerta, 1624; Graells, 1897). Barney et al. (2006, p. 180) suggested that the

Caper is equivalent to the Latin word Capra and the Greek aie (αιε) (van Oppenraaij, 1998). De Funes y Mendoza (1621) stated that it is derived from the Latin word carpere because of the goat’s habit of browsing (Barney et al., 2006, p. 247). Some attribute caper to the same origin as Capra; e.g., Kapro from the Indo– European languages (Coromines and Pascual, 1984).

The term caper was reserved for domestic goats (Linnaeus 1756) and also for castrated males (Klein, 1751). For example, in Spanish, capar is the verb to castrate, and capado means castrated (De la Huerta, 1624; Ray, 1693). In early modern Zoology texts, caper was a synonym of wild goat (capra silvestris or caper montanus or ibex (Gessner, 1551), and to name Capra pyrenaica (i.e. Caper hispanica, Jonston, 1650; Charleton, 1677).

Hircus is a word of Latin origin that originally meant male goat (Gessner, 1551; De la Huerta, 1624; Ray, 1693; Lindsay, 1911). Barcia (1902) suggested that it might have derived from the Sabine word fircus, a pre–Roman Italic people in the 4th C. In addition, some classical authors (Suetonius cited in Barney et al., 2006) stated that the word derived from hirqui, which means 'eye corner', because 'his eyes look side–ways on account of wantonness'. This was also noted by Oroz and Marcos (2004) and by Martinez de Espinar (1644). The latter stated "they have rapid view, able to see on their sides or in front, they have highly slanted eyes". That and other descriptions (e.g., 'dictame', above) were repeated for centuries in natural history texts until about the 18th C., demonstrating that many of the definitions and descriptions of animal species were replicated by one author after another in ancient texts, regardless of their veracity.

Later, in peri–Linnaean texts, the word hircus was used to designate both domestic goats and bezoars (Charleton, 1677; Erxleben, 1777; Cuvier, 1798). After being adopted as a genus name for some goat species (Gessner, 1602; Gray, 1850–1852), its use was restricted to domestic goats; i.e. Capra hircus (Klein, 1751; Cuvier, 1817; Ellerman and Morrison–Scott, 1951).

Animal Biodiversity and Conservation 44.1 (2021)

Although Charleton (1677) suggested that the term ibex is of Greek origin, the consensus is that it is of Latin origin (Klein, 1751; Barcia, 1902). For instance, Gessner (1551) did not doubt its Latin origin ('quod nomen a Latino deductum non dubito') and assigned to it a meaning similar to that of Capricornus ('Ibex, vulgo Capricornus'; Gessner, 1602, p. 304). After the description of Alpine ibex by Pliny (Bostock and Riley, 1855) (see below), in his famous book Etymologiae, Isidore of Seville (c. 556–636) was the first to apply the term ibex to wild goats (Lindsay, 1911). His sources were classic texts, specifically those of Aristotle, Suetonius, and Pliny (Oroz and Marcos, 2004). From the latter, he repeated the description of its habitat (the highest peaks) and the legend that describes that when it flees it lets itself fall on its horns, unharmed (Barney et al., 2006; Lib. I, cap. XII, epígr. 16). Isidore of Seville associated the etymology of ibex with avex (birds) and with Nile's ibis because they also live on cliffs, far from human settlements (Oroz and Marcos, 2004; Barney et al., 2006). That peculiar interpretation was repeated in several pre–Linnaean Natural History texts (Gessner, 1602; Topsell et al., 1658). The texts of Isidore of Seville were extremely influential in the Middle Ages and during the Renaissance, and the errors have been replicated by one author after another until today.

Words of Ancient Germanic origin (goat, stein–bock, bouquetin, ibex?)

The Modern English word goat comes from the Old English gāt 'she–goat, goat in general', which in turn was derived from the Proto–Germanic gaitaz (cf. Dutch/ Icelandic geit, German Geiß, and Gothic gaits) and, ultimately, from the Proto–Indo–European ǵ'aidos, which means 'young goat' (cf. Latin haedus 'kid'). In Old English, the male was referred to as bucca (giving rise to the modern term buck), and was replaced by hegote, hegoote in the late 12th C. (Watkins et al., 1975).

Steinbock derives from the Germanic Bock or bod meaning male goat and from the Latin prefix stein meaning rock. The term designates male goats from rocky places, that is, wild goats. In addition to being the current name in Germanic languages, other names have derived from this root; e.g., bouquetin in French (Couturier, 1962), which is derived from Stein–bock through a term permutation. The Italian stambecco has the same origin, as does the term bucardo, which is one of the common names for the Pyrenean wild goat in the Aragonese language (Kuhn, 2008). In his Historia animalum, Gessner (1551) indicated that, in the anglica language, the word Capra is equivalent to gote and the male gote bucke. In Old–English, the term ibex was not used to name the she–goat or the he–goat; rather, the terms were Geiss for females and bucca for males. The English word buck (used also for the male goat) originates from the ancient German word bock. Use of the term ibex came later as a result of the Latin description of the species (Ray, 1693; Linnaeus, 1756).

Couturier (1962, p. 7), in the chapter dedicated to the etymology and lexicology in his exhaustive book

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on the Alpine ibex (C. ibex), investigated the origin of the common name bouquetin and included, among several meanings, the following: "... on trouve encore dans le vieil allemand Ybschen et Krencke; en allemand ancien usité en Autriche ... Stolz (1570) appelait le jeune mâle de 4 à 5 ans Zapfen, le femelle Ybsch et le chevreau de l’année Stökl. En Suisse et dans le Tirol Ibsch, Ibschn, Ybsch, Ybschgeiss (Stumpf, 1548) et Eibsch–Geiss (Wagner, 1680), qui évoquent le mot ibex, désignent la femelle. ...Rappelons quelques appellations anciennes.

En latin de moyen âge: ibex, hibix, bix, boch, estagnus, stambechus." (Couturier, 1962, p. 7).

It is difficult to know whether the Latin term ibex derives from Old German or vice versa. The term Ibsch (hence, ibex) might have come from an onomatopoeia of the alarm whistle of the female wild goat. Early settlers in the Alps might have used this term, and it was adopted by Latin Romans. New studies on the etymology of the term ibex might resolve that question.

In summary, 1) in the last 2,000 years multiple terms have been used to designate goats in Europe.

Many synonymous terms have been used to designate the genus; e.g. Caper (Jonston, 1650), Tragus (Klein, 1751), Hircus (Charleton, 1677), Ibex (Pallas, 1776; Gervais, 1854). Finally, the Latin name Capra was adopted as the genus of all goats, wild or domestic (Linnaeus, 1758); 2) a few classical natural history texts (Aristotle, Pliny, Isidore of Seville, Gessner, Ray) had great influence on later texts until the 18th C. Some authors, almost up until the present day replicated the legends, with their hits and misses.

Etymology of the common name of Capra p. pyrenaica The Pyrenean wild goat (C. pyrenaica pyrenaica), which was declared extinct in 2000 (García–González and Herrero, 1999), was the nominotypical subspecies of C. pyrenaica (Schinz, 1838). In Catalan and Spanish, the common names for the male are erc (erg, herx) and bucardo (appendix 3). Trutat (1878) asserted that Spaniards call the Pyrenean wild goat herx, which derives from the Latin term hircus. Asso (1784) stated that, in the Gistau Valley (Spanish Pyrenees), it was called hircus. The female goat is called craba (Vidaller, 2016).

Erc might have derived from the Latin term hircus or from the Occitan language. Old Occitan coexisted with Latin between the 1st and the 3rd C. (Nuñez, 2003). Cabrera (1911) affirmed that, in the Pyrenees, the wild goat was called yerp, and Rohlfs (1970 in Dendaletche, 1971) asserted that the Pyrenean name for the Pyrenean wild goat was erc, which derives from Gascon, a variant of Occitan. According to Nuñez (2003), the Proto–Basque language is closely related to Old Occitan. In the modern Basque language, the male goat is called aker.

Bucardo is the widely used current common name for the Pyrenean wild goat in the Central and Western Spanish Pyrenees (Vidaller, 2016). It derives from the root buck (male goat) and the suffix –ardo, a

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disparaging augmentative related to their condition of wild (or non–domestic) animal and their big size (Kuhn, 2008).

In the French Pyrenees, the name bouquetin des Pyrénées (Saint–Hilaire and Cuvier, 1824–1842) was used. In Livre de la Chasse, the Count of Bearn (Phoebus, 1387) translated what might be the first description of the bucardo. He called it 'bouc sauvage' (wild male goat) and stated that it is "as big as a red deer and its horns as thick as a man's leg". Apparently, in the Middle Ages, they were so highly abundant in the Pyrenees that 'their hunt had no merit' (Labarère, 1985). The excellent drawings in that manuscript are probably the first representations of the Pyrenean wild goat in various hunting scenes, which show the lyre horns of the Pyrenean morphotype (fig. 1).

In the earliest scientific descriptions of the species, Saint–Hilaire and Cuvier (1824–1842) and Schinz (1838) quoted extensively from Livre de la Chasse.

In conclusion, the local common names of the Pyrenean wild goat (the nominate subspecies of C. pyrenaica) were derivations of 'goat' or 'wild goat', and none included the name ibex.

History of the common and scientific names of Capra ibex and their use in English texts Classical and early modern texts In his Naturalis Historia (77 AD), Pliny the Elder was the first to describe, or at least disseminate, the term ibex to refer to the wild goats that lived in the Alps.

From the details in his work (Holland, 1601; De la Huerta, 1624; Brotier, 1779), it is clear that he refers to the wild goats in the 7th book only, and the meaning of the terms used are imprecise, probably leading to confusion throughout history. The paragraph in chapter 88 (this chapter number differs among translators) of the 7th book in the Karl Friedrich Theodor Mayhoff edition, reads as follows: "... Caprae tamen in plurimas similitudines transfigurantur. Sunt caprae, sunt rupicaprae, sunt ibices pernicitatis mirandae, quamquam onerato capite vastis cornibus gladiorum ceu vaginis ... Sunt et oryges, soli quibusdam dicti contrario pilo vestiri et ad caput verso.

Sunt et dammae et pygargi et strepsicerotes multaque alia haut dissimilia. Sed illa Alpes, haec transmarini situs mittunt." (Pliny the Elder and Mayhoff, 1906).

Bostock and Riley (1855, p. 346) translated the text as follows: "There is no kind of animal, however, that is divided into a greater number of varieties than the goat.

There are the capraea, the rupicapra or rock–goat, and the ibex, an animal of wonderful swiftness, although its head is loaded with immense horns, which bear a strong resemblance to the sheath of a sword. ...

There are the oryges also, which are said to be the only animals that have the hair the contrary way, the points being turned towards the head. There are the dama also, the pygargus, and the strepsiceros, besides many others, which strongly resemble them. The first mentioned of these animals, however, dwell in the Alps;

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all the others are sent to us from the parts beyond sea."

Their 18th note states: "It is not easy to determine what animals Pliny intended to designate. Cuvier employs the terms chevreuils, chamois, and bouquetins as the corresponding words in the French. In English we have no names to express these varieties; we may, however, regard them generally, as different species of wild goats" (Bostock and Riley, 1855).

In summary, Pliny used the terms caprae, rupicaprae, and ibices for the 'close' wild goats (particularly, those in the Alps), and oryges, dammae, pygargi, and strepsicerotes for the wild goats from beyond the sea (likely from Africa and the Middle East). These terms have been ascribed to various species depending on the translator (appendix 4).

Historia animalium by Gessner (1551) is considered the beginning of Modern Zoology. Like other pre–Linnaean works, it was strongly influenced by Pliny's Naturalis Historia (Findlen, 2006). Gessner applied the name ibex to the wild goats that lived in the Alps, following the description by Pliny, as follows: "Caprae (sylvestres) in plurimas similitudines transfigurantur. Sunt capreae, rupicapre, ibices; Sunt & oryges, damae, pygargi, strepsicerotes, multae alia haud dissimilia. Sed illa alpes, haec transmarini situs mittunt, Plinius 8:53" (Gessner, 1551, p. 319).

When referring to synonyms of the term ibex in various languages, he stated that Germans call it Steinbock and Transalpine Gallics call it bouc estain (Gessner, 1602, p. 304), which match the current common names for C. ibex, of Germanic origin. Swiss highlanders call female ibex ybschen or ybschgeiss ('whose name I do not doubt comes from Latin', Gessner, 1551, p. 331).

In the description of the animal, Gessner stated that they are abundant in the Alp peaks and that males have heavy horns that are curved backwards (scimitar type), harsh, and knotted: 'Magni ponderis cornua ei reclinantur ad dorsum, aspera & nodosa' (Gessner, 1602, p. 305). The knots in the horns are distinct in the drawings in the book, which are probably among the first drawings of C. ibex (fig. 2).

That same morphological description, more or less verbatim, was repeated by Ray (1693) and by Linnaeus (1756, 1758) in what is considered the official description of the species: "Capra cornibus nodosis in dorsum reclinatis. le Bouc–étain. Ibex. Raj. quadr.

79". Linnaeus was influenced by or copied the description of C. ibex from Ray (appendix 4) and used the French common name Bouc–etain (Linnaeus, 1756), and Ray (1693) followed Pliny, who is quoted in the description. The description was repeated in other Latin texts of the 18th C. (Klein, 1751; Erxleben, 1777; Asso, 1784).

The earliest English texts that mention wild goats From the 16th C. until the mid–19th C., few zoology books were written in English. Most were written in French or German, as Cuvier et al. (1827–1835) indicated in the foreword of The Animal Kingdom. The History of Four–footed Beasts and Serpents (Topsell, 1658) was, perhaps, one of the first Modern Zoology

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Fig. 1. Scene showing some 13 'bouquetins des Pyrénées' in a Pyrenean landscape; three are albinos.

From Le Livre de la chasse, 1407 (Gaston Phoebus, MS M. 1044, fol. 12–detail), with permission of © The Morgan Library & Museum, New York.

Fig. 1. Imagen en la que se muestran 13 cabras monteses en un paisaje pirenaico; tres de ellas son albinas. De Le Livre de la chasse, 1407 (Gaston Phoebus, MS M. 1044, detalle fol. 12), con permiso de © The Morgan Library & Museum, New York.

books written in Old English. Topsell used the term ibex to designate Alpine wilde goats, possibly, because of the influence of Isidore of Seville, from whom he extracted the origin of the term ibex, which associates it with the Nile ibis.

Another of the early English texts mentioning C. ibex is the Catalogue of the Museum Leveriani by George Shaw (1791), in which Linnaean nomenclature is already used. This bilingual Latin–English edition includes a brief description of Capra ibex from Linnaeus (1758) (Capra cornibus supra nodosis in dorsum reclinatis), which is translated as "The Ibex.

Dark–brown Goat, with large knotted horns reclining backwards". Shaw (1791) refers to Ibex and steinbock equivalently as the common name in English. Both terms are used synonymously in The Animal Kingdom

by Cuvier et al. (1827–1835) and in Gray (1850–1852).

In summary, in Old English, the word ibex was not used to designate the female or the male goat; rather, geit and buck were used, respectively. The term ibex came later through the Latin influence by Linnaeus (1758), being copied from Ray (1693), who was influenced by Pliny (77 AD). Until the 19th C., ibex, Steinbock, and bouc–etain were used interchangeably as the common name for the Alpine ibex (C. ibex) in English. In the earliest descriptions and use in English

of the term ibex, there is no indication that suggests it included Iberian wild goat. Therefore, none of the interpretations based on the texts of Pliny justify the use of ibex as the common name for the Iberian wild goat.

History of the common name of Capra pyrenaica ('cabra montés') Pre–Linnaean texts Isidore of Seville was the first to apply the term ibex to Iberian wild goats, connecting its etymology to Nile's bird ibis (Barney et al., 2006, p. 248). Isidore of Seville (an ecclesiastical scholar) may not have had direct knowledge of Iberian wild goats and was limited to copying classical texts for its description, adding strange interpretations the origin of the term ibex.

Based on the Hispanic origin of Isidore of Seville, on the supposed Latin–Iberian origin of the term, and on the renowned Diccionario etimológico de la lengua hispánica by Coromines and Pascual (1984), Sarasa et al. (2012) justified the use of the term ibex as a common name for the Iberian wild goat. There are several reasons why that was unjustified: (a) Isidore of Seville mentions wild goats and ibex, but he does

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Fig. 2. Alpine ibex or Steinbock (Capra ibex) from Gessner (1560). Probably one of the first illustrations of Capra ibex in a modern zoological text. Conrad Gessner (1516–1565) noted the typical character of the knots in the anterior face of the horn sheath, differentiating it from the Iberian wild goat (C. pyrenaica). www. biodiversitylibrary.org/item/131297, public domain (holding institution: Smithsonian Libraries, sponsored by: Biodiversity Heritage Library).

Fig. 2. Cabra salvaje de los Alpes (Capra ibex) de Gessner (1560). Probablemente una de las primeras ilustraciones de Capra ibex en un texto zoológico moderno. Conrad Gessner (1516–1565) señaló el carácter típico de las nudosidades de la cara anterior del estuche de los cuernos, lo que la diferencia de la cabra montés (C. pyrenaica). www.biodiversitylibrary.org/item/131297, dominio público (institución depositaria: Smithsonian Libraries, patrocinado por: Biodiversity Heritage Library).

not refer to Iberian species specifically; rather, he refers to wild goats in general. Furthermore, Gessner (1602, p. 304) felt that Isidore of Seville confused both terms ('Isidorus dorcades, capreas & ibices imperitissime confundit'). (b) Isidore of Seville gathered most of his information from Pliny the Elder (Barney et al., 2006, p. 14), who referred to ibex as the wild goat that lives in the Alps (see above). (c) In their book, Coromines and Pascual (1984, p. 553) confuse the current species of Southern chamois (Rupicapra pyrenaica) and wild goat (Capra p. hispanica). They created a hybrid Latin name Rupicapra hispanica, and state that ibex only occurs in Spain and not in the Alps. This is a significant error as Pliny (77 AD), Gessner (1602), Klein (1751), and Linnaeus (1758) (among others) make it clear that the ibex is restricted to the Alps. Consequently, given the limited taxonomic and biological background of Coromines and Pascual, their argument should be considered invalid. Contrary to what Sarasa et al. (2012) maintain, the book by Isidore of Seville is not a reliable source of information about the wild goats living in Iberia at that time.

The first texts written in medieval Spanish that referred to the Iberian fauna did not call C. pyrenaica ibex; rather, they were referred to as cabra montés (wild goat) in general or for females, and cabrón (he– goat). Most of the authors were hunters and knew wild goat very well, having observed them. For instance,

in Libro de la Caza (1325), Don Juan Manuel noted that wild goats were present in the County of Villena in the Kingdom of Murcia (Gutiérrez de la Vega et al., 1879). In the famous Libro de la Montería by King Alfonso XI (Argote de Molina, 1582), the wild goat is not mentioned, specifically, but several toponyms associated with wild bock are mentioned (Valverde, 2010), confirming the predominance given to the male to name the species in Classical and Modern texts (Gessner, 1551; appendix 3). In all the old treaties subsequently published in Spanish or Portuguese, the reference is to cabras monteses for females or for the species, and cabrones or macho montés for the male (Barahona de Soto, 1575; Martínez de Espinar, 1644; Calvo Pinto, 1754; Barboza du Bocage, 1857).

Some texts reference cabras silvestres from the Canary Islands, which were used to supply vessels with fresh meat (Argote de Molina, 1582). Clearly, those were feral goats, Capra hircus, as there were no goats other than domestic ones in the Canary Islands. In summary, in the Iberian peninsula the term ibex was never used in hunting, wildlife, geographical dictionaries, or legal texts as a common name for Iberian wild goats (appendix 3).

In the section devoted to Capris silvestribus, Gessner (1551, 1602) did not mention Iberian wild goats, specifically. Rather, he indicated the names that were used in various languages. For the 'Hispanica'

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Fig. 3. Caper hispanicus from Historiae Naturalis by Jonston (1650), one of the first representations of Iberian wild goat after the drawings in Livre de la Chasse (Phoebus, 1387). The drawing illustrates the typical lyre– shaped horns of the Pyrenean morphotype. www.biodiversitylibrary.org/item/137912#page/135/mode/1up, public domain (holding institution: Smithsonian Libraries; sponsored by Biodiversity Heritage Library).

Fig. 3. Caper hispanicus de Historiae Naturalis de Jonston (1650), una de las primeras representaciones de la cabra montés posteriores a las ilustraciones de la publicación Livre de la Chasse (Phoebus, 1387).

En la ilustración se observan los típicos cuernos en forma de lira del morfotipo pirenaico. www.biodiversitylibrary.org/item/137912#page/135/mode/1up, dominio público (institución depositaria: Smithsonian Libraries; patrocinado por Biodiversity Heritage Library).

language, he gave cabra, cabrito, cabrón, cabronzillo montés, but did not mention ibex.

Among the pre–Linnaean Natural History texts from the early Modern period, the first to show the Iberian wild goat was Jonston (1650), who called it Caper hispanicus (fig. 3). Probably, it is the first or one of the first images of the species after the bouquetin drawings in Le livre de la Chasse (Phoebus, 1387).

Subsequently, the Latin name Caper Hispanicus was used by Charleton (1677) in his Historia Naturalis and he gave it the name 'Spanish wild goat'. The 'ibex', which was illustrated by a drawing copied from Gessner (1551), occurs in the Alps.

Post–Linnaean texts before the first scientific description of C. pyrenaica in 1838 Erxleben (1777) described five species in the genus Capra: hircus, ibex, mambrina, depressa, and reversa. In the hircus group he included αἶγας (aigas) and τράγος (tragos) from Aristotle, Capra from Pliny, several domestic goats described by various authors, and C. aegagrus, which was the first taxonomic description of the species recognized today. In that group, Erxleben included Caper Hispanicus based on Jonston (1650).

These taxa were differentiated from the ibex group (Alpine Ibex Capra ibex), for which he used the 1758 Linnaeus definition (Capra cornibus nodosis in dorsum recIinatis) and quoted Pliny, specifically.

Asso (1784) is one of the few in the 18th C. who remarked upon the fauna of the Aragon region in Spain. He differentiated three kinds of goats that occurred in the Pyrenees: Capra Hircus (domestic), Capra Rupicapra (chamois) and Capra Ibex, (living in Plan, Gistau Valley), and certainly was referring to the Pyrenean wild goat. He used that name because he followed Linnaeus faithfully and, at that time, C. pyrenaica had not been described scientifically. In the second half of the 18th C. and the early 19th C., various authors used the term C. ibex for wild goats in general (Klein, 1751; Pennant, 1793).

Cuvier et al. (1827–1835) used the common name ibex and the scientific name Capra Ibex for all the European wild goats. He presumed that they still existed in Candia (Crete), Greece, and the Carpathians. He stated that Iberian wild goats exist in the Asturias Mountains and in the Pyrenees 'where they are almost extinct'.

In summary, most of the pre– and post–Linnaean texts that describe the Iberian fauna did not refer to the Iberian wild goat as an ibex, but as 'cabra montés' (wild goat). A few authors who do refer to it as ibex (Isidore of Seville, Asso, Cuvier G.) follow the inertia of naming all European wild goats as ibex, misinterpreting Pliny the Elder who used this term only for the wild goats from the Alps. The scientific description of C. pyrenaica was not achieved by Schinz until 1838.

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Taxonomically, few have considered Capra pyrenaica an ibex Scientific descriptions of the species in the 19th C. In one of the first descriptions of C. pyrenaica, Saint– Hilaire and Cuvier (1824–1842) included extensively long passages from Gaston Phoebus's (1387) book.

In the text, they called it Bouquetin des Pyrenées, but in the index it is referred to as C. ibex. They also reproduced a drawing of a young male in captivity in La Ménagerie (a private zoo in Paris) that is unrepresentative of the species (Sánchez Hernández, 2010, p. 41). The drawing was reproduced by Schinz (1838) in the first taxonomic description of C. pyrenaica. In the title and through the text he used Pyrenäenbock and Steinbock der Pyrenäen as the common name to differentiate it from the Alpensteinbock. Schinz’s description of the new species was based on skins and drawings given to him by his colleague Carl F. Bruch (Sánchez Hernández, 2010). Ten years later, Schimper (1848) described a new species of Capra for Iberia, C. hispanica, based on specimens collected on an expedition to the Sierra Nevada (Spain). For the common names, he used the ones used locally, cabra montés (wild goat) or Montesa (wild she–goat).

The morphotype of C. pyrenaica differs from that of the other wild goats, at least from the Alpine ibex (fig. 4). Therefore, in one of the first catalogues of the British Museum, Gray (1850–1852) separated C. pyrenaica and the tur C. caucasica from the other Capra and assigned them the generic name Aegoceros.

To Ae. pyrenaica he assigned the common name Pyrenean tur.

In his interesting treatise of mammals from Galicia, López Seoane (1861) noted the presence of C. pyrenaica, which was present in the NW Spanish sierras at that time, where it was called craba brava or craba fera, a vernacular term for wild goat (appendix 3). Graells (1897), following Gervais (1854), assigned the Iberian goats to the genus Ibex (Ibex pyrenaicus).

He used the term Ibex as a synonym of Capra. For example, he called the Alpine ibex Ibex alpinus and the recently described (Schimper, 1848) wild goat of southern Iberia Ibex hispanicus. In some cases, the name Ibex had been used as a generic name instead of Capra; e.g., Frisch 1775 (cited in Parrini et al., 2009), Pallas (1776), Pennant (1793), Gervais (1854). For the common name, Graells (1897) used cabra montés.

Lydekker (1898) named C. pyrenaica the Spanish tur (probably following Gray) and assigned it an intermediate morphotype between the Caucasian tur and the 'true ibex' although more similar to the former. He also called it the Spanish wild goat (p. 255), but added "but it may best be called a tur rather than an ibex".

Classification and common names of C. pyrenaica in the 20th C. In an influential paper, Cabrera (1911) defined the currently accepted subspecies of C. pyrenaica (Shackleton, 1997; Herrero et al., 2020). He used the common name Spanish ibex to refer to the species.

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The work of Cabrera (1911) had a significant impact by substantially changing the taxonomy of the Iberian wild goats and contributed to the spreading of the inappropriate term Spanish ibex in the 20th C. Specifically, Cabrera (1911) combined into a single species (C. pyrenaica) the two species initially described by Schinz (1838), C. pyrenaica, and Schimper (1848), C. hispanica, designated each as a subspecies. He also described two new subspecies (lusitanica and victoriae). Camerano (1917) and others (Forsyth Major, 1879; Graells, 1897) advocated maintaining the two original species.

Probably, Cabrera's (1911) use of the term Spanish ibex was influenced by his relationship with English–speaking scientists (Casado, 2012) and by contemporary texts of English explorers (Buxton, 1892; Chapman and Buck, 1893, 1910) that he used in part to describe the species' distribution in Iberia. These English hunters who explored Iberia at the end of the 19th C. and earlier 20th C probably did not know the description of Iberian wild goats by Schinz and Schimper, whom they do not quote in their works, and adopted the generic term 'ibex' used for the European wild goats in general (see previous sections). In his monography on Iberian mammals, Cabrera (1914) provided a list of vernacular names used for the species in the Iberian peninsula. Almost all of them are variations of wild goat (cabra montés, cabra salvatge, craba brava, cabra montez, bucardo).

In addition, he noted that in Old Spanish, it was named ibis or íbice, probably because of the influence of Las Etimologías by Isidore of Seville, which does not parallel the hunting or popular texts of the Medieval Period (appendix 3).

More recently, Ellerman and Morrison–Scott (1951) differentiated C. pyrenaica and C. caucasica (which includes C. cylindricornis) from the ibexes, and recognized five species for Capra: C. hircus (domestic goats and bezoars), C. ibex (ibexes sensu lato, see below), C. caucasica (Caucasian tur), C. falconeri (markhor), and C. pyrenaica (called Spanish ibex but included in a different subgenus Turocapra). In the renowned text Mammals of the Soviet Union, Heptner et al. (1989) proposed a taxonomy for the genus Capra that included eight species, which is similar to the nine accepted currently (Shackleton and Lovari, 1997; Groves and Grubb, 2011). Heptner et al. (1989) grouped C. hircus with C. aegagrus in one species. In their review, they referred to C. pyrenaica as Pyrenean goat, not Spanish ibex (appendix 1).

The phylogeography and systematic classification of Iberian wild goats (Capra pyrenaica) is unclear (Acevedo and Cassinello, 2009) although there are several hypotheses for their origin. An overview of these is presented in appendix 5.

In summary, Capra pyrenaica has been given a variety of common names (Caper Hispanicus, Spanish tur, Spanish wild goat). By a fortuitous occurrence, the term Spanish ibex has become common in scientific texts, but this does not mean that it is the most accurate or appropriate. The use of the term Spanish ibex began to appear in some English–language texts written in the 19th C. (Cuvier et al., 1827–1835;

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A

C

B

D E

Fig. 4. Horn morphology of the five major Capra morphotypes: A, ibex–type (C. ibex, C. nubiana, C. sibirica, and C. caucasica); B, the Spanish goat type(C. pyrenaica); C, the Eastern tur (C. cylindricornis); D, the markhor (C. falconeri); and E, the bezoar–type (C. aegagrus). Artwork by Julie Dlugos (Pidencier et al., 2006, with permission from Elsevier).

Fig. 4. Morfología de los cuernos de los cinco morfotipos del género Capra principales: A, tipo íbice (C. ibex, C. nubiana, C. sibirica y C. caucasica); B, tipo cabra montés (C. pyrenaica); C, tur del Cáucaso oriental (C. cylindricornis); D, marjor (C. falconeri); E, tipo bezoar (C. aegagrus). Ilustración de Julie Dlugos (Pidencier et al., 2006, con permiso de Elsevier).

Busk, 1877) and it spread rapidly in the early 20th C. as English emerged as the predominant language of science. Several popular books about hunting stories

by English hunters and explorers in Spain, such as Buxton (1892) and Chapman and Buck (1893, 1910), perpetuated the term Spanish ibex. This was aided by the influential paper by Cabrera (1911). Nevertheless, there was still no reason to use the name ibex in English to describe European wild goats other than Alpine ibex.

Horn morphology and molecular genetics As seen in previous sections, the taxonomy of the Capra genus has been controversial and is not yet fully resolved today (Groves and Grubb, 2011; appendix 1).

Until the incorporation of molecular techniques, it was mainly based on morphological and biogeographical criteria (Lydekker, 1898; Heptner et al., 1989). One of the most widespread criteria used the shape of the horns of adult males. For example, Pidancier et al. (2006) established five morphotypes for Capra:

the Spanish goat type (C. pyrenaica), the eastern tur (C. cylindricornis), the markhor (C. falconeri), the bezoar–type (C. aegagrus), and the ibex type (fig. 4; see also appendix 1). The last applies to a particular horn morphotype, in which adult males bear scimitar–shaped horns that have prominent knobs or ridges on their anterior surfaces (Ellerman and Morrison–Scott, 1951; Schaller, 1977). This is typical for several Capra species (C. ibex, partially in C. caucasica, C. sibirica, C. nubiana, and C. walie) and some authors considered they might be subspecies of C. ibex (Ellerman and Morrison–Scott, 1951; Couturier, 1962; Shackleton and Lovari, 1997). Adult males of the C. pyrenaica morphotype (also called the lyre– shaped morphotype) present double–curved and, normally, smooth horns (Schinz, 1838; Lydekker, 1898; Pidancier et al., 2006). The ibex and C. pyrenaica morphotypes differ so much that De Beaux (1949) proposed a new subgenus, Turocapra, only for the Iberian wild goat, although this has not been accepted and used in scientific publications.

Molecular genetic results do not necessarily correspond with morphological characteristics. For example,

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Capra sibirica (of the ibex morphotype) is genetically quite distant from C. ibex (Alpine ibex) (Kazanskaya et al., 2007; Joshi et al., 2020). Several molecular analyses show C. nubiana (ibex morphotype) to be genetically more distant from C. ibex than from other Capra species of different morphotypes (Lalueza–Fox et al., 2005; Pérez et al., 2014). Conversely, markhor (C. falconeri) is relatively genetically close to C. aegagrus (Zvychaynaya, 2010; Bibi et al. 2012) despite having radically different horn morphotypes (fig. 4, appendix 1). C. caucasica and C. cylindricornis belong to two different horn morphotypes although some authors point out a close genetic relationship between the two (Manceau et al., 1999; Lalueza–Fox et al., 2005). Others (Kazanskaya et al., 2007) have also indicated this dissimilarity and consider that the ibex morphotype could be a plesiomorphic character for the Capra genus. These discrepancies are not particularly unusual since the genes that regulate the shape and size of the horns are evolutionarily easy to modify (Schaller, 1977), as livestock risers know.

However, neither external morphological features nor genetic distances based on particular molecular characters are suitable alone for a reliable diagnosis of taxonomic status. To be biologically meaningful, classifications must involve integration of genetic, morphological, physiological and behavioural data (Giacometti et al., 1997).

Most molecular studies have shown a close genetic relationship between C. pyrenaica and C. ibex (Manceaux et al., 1999; Ureña et al., 2018, even if horn morphotypes are completely different (fig. 4).

Genetic closeness does not justify the adoption of a common name (Spanish ibex) which additionally is based on a morphotype that does not match Capra pyrenaica. The scientific nomenclature follows a rigorous regulation guided by phylogenetic relationships, which is not the case of common names. Common names are usually recognizable, easy to pronounce and stable over time, and they are intended to link the people of the territory with its species (Bowen–Jones and Entwistle, 2002).

The conservation value of common names and the use of the name 'wild goat' Although scientists agreed to name the species of organisms based on the Linnaeus (1758) binomial system, the common names given to taxa are important to promote sound communication in fields such as science, conservation and legislation. Often, common names of species are linked to vernacular names that local people attribute to the plants and animals they know, and these become part of their cultural heritage. It is important to take this into account when using common names of species in monographs, catalogues, or legal documents, because the inhabitants of affected areas will be more committed to the conservation of these species (Duckworth and Pine, 2003; Stevens et al., 2014).

English common names are important in the public's perception of animals and are therefore essential for

flagship species (Bowen–Jones and Entwistle, 2002).

Capra pyrenaica is a outstanding endemic species of the Iberian peninsula, and emblematic for many nature enthusiasts, conservationists, and hunters.

Some taxonomists (Ellerman and Morrison–Scott, 1951; Corbet, 1980; Groves and Grubb, 2011) have used the term wild goat preferably or exclusively for the attributed ancestor of domestic goats (Capra aegagrus or bezoar). Although the term aegagrus originated from the Greek aiga agrios ('wild goat'), this term is not exclusive for C. aegagrus. As has been shown throughout the preceding text, the term 'wild goat' has been used (in different forms and languages) for the last 20 centuries for several Capra taxa including C. pyrenaica.

The term wild goat has arisen because of the need to differentiate the domestic and wild forms of the same species (C. aegagrus). Subsequently, the common name wild goat was reserved exclusively for Capra aegagrus. However, originally, for Pliny and his followers, wild goat included other wild goats; e.g., the caprea, rupicapra, and ibeces from Pliny the Elder (77 AD), and the Capra sylvestris of Gessner (1551).

To avoid mistakes, C. aegagrus is frequently called bezoar or pasang.

Some authors (Sarasa et al., 2012; Karaffa et al., 2012) assert that from the point of view of conservation, it is preferable not to use common names with pejorative connotations like wild or killer, avoiding the term wild goat. However, in our opinion, nowadays the term 'wild' can have positive connotations for a growing sector of the population that sympathizes with nature and wilderness. Consider for example, the now classic ideas of 'wildness' and 'wilderness' from Henry D. Thoreau and his followers ('In wildness is the preservation of the world'; Thoreau, 1854) or the more recent of 'rewilding' (the return of habitats to their natural state). A separate question is the term 'killer', improperly applied for example to Orcinus orca ('killer whale'), which is neither a whale and is certainly not a murderer. The argument of Sarasa et al. (2012) that the use of wild goat might reduce the conservation value of Capra pyrenaica because the general population might confuse them with 'stray or feral goats' is unrealistic. Since centuries ago in Iberia, people know perfectly well that cabra montés or cabra brava is a wild animal and not a domestic goat that has returned to a wild state. Regarding the latter, in Spanish, the term cabra asilvestrada or cimarrona (feral goat) is used.

Concluding remarks This review aimed to show that the names used most frequently to designate the wild members of the Capra genus (aegagrus, Steinbock) are related etymologically to the term wild goat, with different forms influenced by the sex of the animal or the language of origin. The use of one term or another by different authors over the last 2,000 years has depended largely on popular use and the original sources that the academics used as the basis for their work.

Animal Biodiversity and Conservation 44.1 (2021)

Probably, the term ibex is of Latin origin, and the etymology provided by Isidore of Seville (c. 556–636), which associates it with Ibis of the Nile, is unlikely.

In addition, he stated that ibices were exclusive of Iberia, which is incorrect. Pliny the Elder (77 AD), in his Historiae Naturalis, was the first to use the term ibex in Latin, which referred to the wild goats in the Alps. Other pre–Linnaean authors adopted the term. Gessner (1551), asserted the Alpine origin of ibices, and included in its description one of the main morphological features, viz., scimitar–shaped horns that have knots, and are curved backwards.

That diagnostic feature was adopted by Ray (1693) and by Linnaeus (1758) in what became the officially accepted definition for the species C. ibex ('capra cornibus nodosis in dorsum reclinatis').

The use of Latin as the erudite and scientific language in Europe until the 18th C. greatly influenced those who followed the early Roman authors, especially Pliny the Elder. For instance, the term ibex appeared in some ancient academic texts such as that of Isidore of Seville (Lindsay, 1911). Nevertheless, in medieval books about law, hunting, or Natural History, the common names of Capra in their respective languages or their derivatives began to be used. For example, cabra montes in Libro de la Caza by Juan Manuel (Gutiérrez de la Vega et al., 1879), bouquetin in Le Livre de la Chasse by Gaston Phoebus (1387), and Steinbock and Ibsch in the medieval Germanic treatises (Couturier, 1962).

The use of the term ibex continued in post–Linnaean English–language texts, and some included all the known wild goats (Pennant, 1793; Cuvier, 1798; Gervais, 1854; Schwarz, 1935). Even a seminal Spanish paper (Cabrera, 1911) followed that nomenclature for C. pyrenaica and called it Spanish ibex.

Subsequently, the term has been used extensively, although without a rational basis to do so, given that the first Natural History texts written in English used interchangeably ibex, Steinbock or bouc–etain as the common name for C. ibex.

In the 19th and 20th C. from the first description of the species in 1838 by Schinz (Pyrenäenbock) to the prestigious catalogs such as Lydekker (1898) and Heptner (1989), few considered C. pyrenaica as an ibex, taxonomically. Several experts have defended the morphological distinction between Iberian wild goat and the ibexes (Gray, 1850–1852; De Beaux, 1949; Ellerman and Morrison–Scott, 1951; Pidancier et al., 2006). However, various mtDNA studies have identified a close genetic relationship between C. pyrenaica and C. ibex (e.g., Manceaux et al., 1999; Ureña et al., 2018) and some assert the common name for C. pyrenaica should therefore be 'Iberian ibex'. Nevertheless, genetic proximity does not necessarily mirror morphological similarity (Schaller, 1977; Bar–Gal et al., 2002). In addition to morphology, common names can reflect any other useful feature for locals to easily recognize a particular species (Duckworth and Pine, 2003). Common names do not have to follow the rules of scientific nomenclature based on phylogeny.

If we accept that the common name of an animal is the popular name used by the general population,

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it should be noted no one in Portugal and Spain calls C. pyrenaica an ibex. There, they are referred to as cabra montés, cabra salvatge or cabra brava (among other similar vernacular names), which translate to wild goat. Experts and hunters use the same names, and when they speak about ibex they are referring to the Alpine ibex or to the ibex of other areas. We suggest that 'Iberian wild goat', a common name that has already been used in several languages for centuries and in scientific texts (see appendices 2 and 3), is the most appropriate common name for C. pyrenaica and that scientific, legal and popular media use this common name.

Acknowledgements We are very grateful to Juan Jiménez, Head of the Wildlife Service of the Valencia Government, for his comments on the history of Capra pyrenaica, and Rafael Vidaller (Aragonese Language Academia) and Luis Villar (IPE) for their advice regarding the etymological review. We also appreciate the comments of Spartaco Gippoliti, Sabine Hammer and an anonymous reviewer that contributed to improving an earlier version of this study. Bruce MacWhirter revised the English version of the manuscript. No specific financial support was provided for this work.

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Watkins, C., 1975. The American Heritage Dictionary.

Houghton Mifflin, Boston.

Zvychaynaya, E. Y., 2010. Genetic differentiation of wild goats (genus Capra) based on the analysis of mitochondrial gene cytochrome b and fragment of nuclear gene DRY. Galemys, 22 (special no): 255–276.

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Nestedness structure of bird assemblages in a fragmented forest in Central Argentina: the role of selective extinction and colonization processes S. Dardanelli, L. M. Bellis

Dardanelli, S., Bellis, L. M., 2021. Nestedness structure of bird assemblages in a fragmented forest in Central Argentina: the role of selective extinction and colonization processes. Animal Biodiversity and Conservation, 44.1: 17–29, Doi: https://doi.org/10.32800/abc.2021.44.0017 Abstract Nestedness structure of bird assemblages in a fragmented forest in Central Argentina: the role of selective extinction and colonization processes. Nestedness analysis constitutes an important tool to understand the processes that shape wildlife communities. It also allows a quick first evaluation of species extinction proneness in fragmented landscapes. Here, we tested whether avian assemblages in the fragmented Espinal forest exhibited nested subset patterns. Furthermore, we examined whether selective extinction or selective colonization are driving nested subset patterns. We studied avian assemblages in 13 forest fragments in central Argentina during breeding and non–breeding seasons. We completed partial Spearman rank correlations to explore the relationship between nestedness rank order and habitat patch variables and species life history traits related to species extinction proneness and colonization rate. Bird species showed strong nestedness patterns, both for the total incidence matrix and for forest fragments and species separately. Nestedness patterns were similar during the breeding and non–breeding seasons. The nested rank order of forest fragments correlated with area and distance to nearest fragment, both of which are patch characteristics known to increase the probabilities of species extinction. The nested rank order of species was correlated with the minimum area of species requirement, trophic guild, and range size, traits that are linked to extinction risk. Selective extinction processes rather than selective colonization appear to be driving nestedness patterns of bird assemblages in fragmented Espinal forest. The most effective way to preserve forest bird species in the Espinal forest seems to be by protecting the larger fragments of this relictual forest.

Key words: Forest fragments, Avifauna, Community assembly, Seasonality, Species traits, Espinal forest Resumen Estructura anidada de ensamblajes de aves en un bosque fragmentado del centro de Argentina: el papel de los procesos de extinción y colonización selectivos. El análisis de anidamiento constituye una herramienta importante para comprender los procesos que dan forma a las comunidades de vida silvestre. También permite hacer una primera evaluación rápida de la propensión a la extinción de las especies en paisajes fragmentados. En el presente estudio, analizamos si los ensambles de aves en el bosque fragmentado del Espinal siguen un patrón de subconjuntos anidados. Además, examinamos si la extinción selectiva o la colonización selectiva están impulsando patrones de subconjuntos anidados. Estudiamos los ensambles de aves en 13 fragmentos de bosque del centro de Argentina durante las estaciones reproductiva y no reproductiva.

Realizamos correlaciones parciales de rango de Spearman para analizar la relación entre el orden de rango de anidamiento y las variables de parche de hábitat y los rasgos de la historia de vida de las especies relacionados con la propensión a la extinción y la tasa de colonización de las especies. Las especies de aves mostraron marcados patrones de anidamiento, tanto en relación con toda la matriz de incidencias como con los fragmentos de bosque y las especies por separado. Los patrones de anidamiento fueron similares en la estación reproductiva y no reproductiva. El orden de rango de anidamiento de los fragmentos de bosque se correlacionó con la superficie y la distancia al fragmento más cercano, que son características del parche que aumentan la probabilidad de extinción de las especies. El orden de rango de anidamiento de las especies se correlacionó con el requerimiento mínimo de superficie de la especie, el gremio trófico y el tamaño del ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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rango, que son características vinculadas al riesgo de extinción. A diferencia de los procesos de colonización selectiva, los de extinción selectiva parecen estar impulsando los patrones de anidamiento de ensamblajes de aves en el bosque fragmentado del Espinal. La forma más eficaz de conservar las especies de aves del bosque del Espinal parece ser mediante la protección de los fragmentos más extensos de este bosque relictual del centro de Argentina.

Palabras clave: Fragmentos de bosque, Avifauna, Ensamblaje comunitario, Estacionalidad, Rasgos de especies, Bosque del Espinal Received: 19 III 20; Conditional acceptance: 21 IV 20; Final acceptance: 27 VII 20 Sebastián Dardanelli, Instituto Nacional de Tecnología Agropecuaria (INTA), Estación Experimental Agropecuaria Paraná, Ruta 11 km 12.5, 3101 Oro Verde, Entre Ríos, Argentina.– Laura M. Bellis, Instituto de Altos Estudios Espaciales "Mario Gulich" (CONAE–UNC), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), and Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina.

Corresponding author: S. Dardanelli. E–mail: sedardanelli@gmail.com ORCID ID: S. Dardanelli: 0000-0003-4341-3879; Laura Bellis: 0000-0002-0725-5079

Animal Biodiversity and Conservation 44.1 (2021)

Introduction Habitat loss and fragmentation are among the most important threats to biodiversity worldwide (Wilcove et al., 1998; Sala et al., 2000; Haddad et al., 2015). Broad– scale habitat fragmentation gives rise to archipelagos of natural habitat fragments or islands immersed in a matrix of anthropogenic open habitat (Matthews et al., 2015). Since species sensitivity to habitat fragmentation in a particular region is variable, species loss in those remaining habitat islands does not necessarily occur at random but may occur in a nested pattern (Patterson and Atmar, 1986; Atmar and Patterson, 1993, 1995).

In nested assemblages, poorer communities constitute proper subsets of increasingly richer communities (Patterson and Atmar, 1986). Therefore, less widespread species occur on sites with relatively large species assemblages while poorer assemblages are mostly composed of ubiquitous species (Cutler, 1991; Soga and Koike, 2012). Consequently, in archipelagos with 'perfect' nestedness structure, it is possible to predict the order of disappearance of the less ubiquitous species from the poorer sites in response to environmental gradients (Atmar and Patterson, 1993) as the species that are present only in the richer fragments are more likely to become extinct as environmental disturbances increase (Nupp and Swihart, 2000).

Nestedness analysis is an important tool to understand the processes that shape communities and to reveal the ecological and evolutionary limits of the species. Furthermore, it has valuable implications for conservation (Wright et al., 1998; Martinez–Morales, 2005). Nestedness analysis is attractive because it allows a quick first evaluation of species extinction proneness in species assemblages of fragmented landscapes (Ganzhorn and Eisenbei, 2001). Although this approach alone is insufficient to evaluate strategies to preserve biodiversity in fragmented biotas (Cutler, 1994) it could be highly useful as predicting species loss can be used to make informed land–use decisions and to effectively protect species that will disappear first in a determined fragmentation scenario (Fleishman et al., 2007).

Four main processes have been proposed to explain nestedness patterns: (1) selective extinction of species with large spatial requirements in relation to fragment area (Wang et al., 2012; Matthews et al., 2015); (2) selective colonization of species with low dispersal ability in relation to fragments isolation (Kadmon, 1995); (3) random, passive sampling from a common species pool, which can result in a nested pattern if sites are more likely to be occupied by species that are regionally more abundant (Cook and Quinn, 1995; Wright et al., 1998); and (4) selective occupation of hierarchically nested habitats (Honnay et al., 1999). However, studies of the mechanisms explaining nestedness structure on archipelagos resulting from habitat fragmentation have found that, in most cases, nestedness structure is driven by selective extinction and, to a lesser extent, to selective colonization process (Watling and Donnelly, 2006; Matthews et al., 2015).

The selective extinction hypothesis is related to the concept of faunal 'relaxation' (Brown, 1978;

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Wilcox et al., 1986). It states that fragment area is the main driver of communities' structure as species loss is predictable and follows gradients of species sensitivity to habitat size (Wright et al., 1998; Watling and Donnelly, 2006; Matthews et al., 2015). Under this mechanism animal species with large area requirements, high trophic guild (i.e. carnivorous and insectivorous), small range size and large body mass will be the first to become extinct when the area of the fragments is reduced (Matthews et al., 2015; Keinath et al., 2017; Li et al., 2019). On the other hand, the selective colonization hypothesis states that the habitat isolation would be the main mechanism behind nestedness structure of an assemblage (Watling and Donnelly, 2006; Meyer and Kalko, 2008). Under this mechanism, species with low dispersal ability –such as those with a low dispersal ratio or small body mass– will colonize only the less isolated fragments and will fail to colonize those that are more isolated (Loo et al., 2002; McAbendroth et al., 2005; Frick et al., 2009).

Although explanation of nestedness structure under selective extinction and selective colonization implies the combination of site variables with species traits (Ulrich et al., 2009), few studies have tried to analyze their roles in generating nestedness simultaneously (Wang et al., 2012; Li et al., 2019).

The Espinal xerophytic forest in central Argentina provides a suitable scenario to address the effects of habitat fragmentation in species assemblage structure.

Here, open forests historically used for cattle grazing have been converted to row crop production (Baldi and Paruelo, 2008). The expansion of cultivated land has been related to a combination of climate change (increasing precipitation), increasing global demand for agricultural products, national economic policies, and new technologies (genetically modified seeds, agrochemicals, machinery) (Grau and Aide, 2008; Zak et al., 2008).

At present, the Espinal xerophytic forest is an extremely degraded lowland forest with less than 5% of the original forest area (Dardanelli et al., 2006; Lewis et al., 2009; Morello et al., 2012; Noy–Meir et al., 2012). Because of this severe fragmentation and habitat loss, avian diversity has been negatively affected (Dardanelli and Nores, 2001; Dardanelli, 2006; Dardanelli et al., 2006). At least eight species appear to have become extinct in this forest in the province of Córdoba, Central Argentina, and another nine species are sensitive to fragmentation (Dardanelli et al., 2006). However, fragmentation effects on the species composition and nestedness structure of avian assemblages have not been assessed. Studying drivers behind nestedness structure of avian assemblages in fragmented Espinal forest would provide insights that could help avian conservation. The design of effective management plans in poorly studied and highly fragmented habitats, such as the Espinal forests of Córdoba, Argentina, could take advantage of nestedness analyses, especially in a place where there is no time or resources to undertake long–term studies and when decisions for conservation action are urgent (Ganzhorn and Eisenbei, 2001; Fleishman et

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al., 2007). Here, we tested whether avian assemblages in the fragmented Espinal forest exhibit nestedness patterns for winter and summer assemblages. Furthermore, we examined the mechanisms underlying the nestedness structure, particularly focusing on whether selective extinction, selective colonization, or passive sampling are driving nestedness patterns for winter and summer assemblages.

Material and methods Study area Our study was conducted in the Espinal forest fragments in the eastern lowlands of Córdoba Province, Argentina (fig. 1). Forest fragments are located in private lands since there are no protected areas in the region. The mean annual precipitation of about 700–800 mm falls mostly in late–spring and summer, from October to March; the rest of the year is the dry season. The mean annual temperature is 16 ºC, with a maximum peak of 44 ºC and minimum temperature of –9 ºC (Morello et al., 2012). This region is regarded a semiarid environment because of the high potential of evapotranspiration that generates a water deficit for 11 months of the year (Morello et al., 2012).

The vegetation of forest fragments has a tree stratum of 5–10 m in height composed mainly of Prosopis alba, Prosopis nigra, Celtis ehrenbergiana, Geoffroea decorticans, and Aspidosperma quebracho–blanco.

Common components of the understory (1 to 5 m height) are species in the genera Acacia and Schinus, also including Porliera microphylla and Jodina rhombifolia. The herbaceous stratum (0–1 m height) includes herbs and grasses; common components of the stratum are species of the genera Solanum spp., Eupatorium spp., Stipa spp., Setaria spp., Paspalum spp., etc. (Cabrera, 1994; Morello et al., 2012).

All fragments in our study had three well–developed vegetation strata (tree, shrub, and herbaceous), were completely isolated (no corridors or rivers connecting any fragment, fig 1), and were embedded in a matrix of croplands, mostly soybean during the austral summer and wheat or fallow fields during the winter.

Thus, we considered the contrast between forest fragments and the matrix to be high (Lindenmayer and Fischer, 2006) for forest birds.

Bird sampling We surveyed bird species in 13 forest fragments (ranged from 0.25 to 217.4 ha). Nocturnal species (Strigidae and Caprimulgidae) and species that only flew over the fragments were not considered. Surveys were conducted during the austral winter (June–August 2001) and austral summer (December2001–March 2002) seasons. One observer (SD) carried out all the surveys by intensive searches recording all bird species seen or heard while walking slowly through the whole fragment from pre–dawn to 11:00 and from 14:00 until sunset. We surveyed each fragment until no new species were added in 4–8 additional

sampling days (Dardanelli et al., 2006). To adjust for differences in species detectability we compared species richness among forest patches and between seasons using rarefaction curves. Rarefaction analysis calculates species richness after standardizing differences in abundance among samples by estimating the expected number of species of each sample if all samples are reduced to a standard size (Magurran, 2004). Rarefaction curves were performed using iNext (Chao et al., 2016).

We distinguished two types of birds occurring in the fragments: forest species (species that inhabit only xerophytic forests in the study area), and habitat generalists that use both forest and open areas (table 1s in supplementary material). Because the focus of this study is on patch level effects, we centred our investigation on species for which xerophytic forest is a primary habitat. Therefore, prior to analysis, we removed all species for which xerophytic forest is not considered primary habitat (Cook et al., 2002; Watson, 2003; table 1s in supplementary material). We also removed migratory species (Nores, 1996; Barnett and Pearman, 2001), considering only year–round residents as they necessarily colonize the fragments at the beginning of the breeding season and leave (disappear) at the end of the breeding season (Watson, 2003). However, we acknowledge the response of generalist and migratory bird species to fragmentation could have some relevance and would need to be considered when designing conservation measures at regional scales for the Espinal forests in Argentina.

It is important to mention that most fragments and all species analyzed in this study persist in the study area (Verga et al., 2019; eBird, 2020). Thus, we consider that the results of our study could be applied to the current scenario, as both the fragmented forest and the bird species have remained constant.

The order of the families and the generic and specific names of bird species follow the South American Classification Committee (Remsen et al., 2020).

Species traits To analyse the influence of extinction and the colonization process in structuring species occurrences, we selected species life history traits commonly associated with avian species extinction proneness or dispersal ability (table 2s in supplementary material). Geographic range size, trophic guild and natural abundance are life history traits related to extinction proneness (Davidar et al., 2002; Henle et al., 2004; Feeley et al., 2007; Wang et al., 2010). On the other hand, body mass and dispersal ratio area are life history traits that are usually linked to species ability to colonize new sites (Schoener and Schoener, 1984; Cook and Quinn, 1995; Henle et al., 2004; Jenkins et al., 2007).

We obtained distributional range size from Birdlife International species factsheets (BirdLife International, 2020). Trophic guild data were constructed by extracting data of local species diet (Zotta, 1940; Del Hoyo et al., 1992; Alessio et al., 2005; Salvador et al., 2017) and creating four categories: 1, herbivores; 2, omnivores; 3, insectivores, and 4, carnivores. Mini-

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A B

G K

A

E

C J

D H L F M I

Google Earth

N

Image Landsat / Copernicus

60 km B

B

L D

G

N

N

700 m

1 km

Fig. 1. A, study area showing the spatial distribution of the forest fragments of Espinal included in the study of nestedness of forest birds in central Argentina; B, examples of some of the studied forest fragments.

Fig. 1. A, área de estudio en la que se muestra la distribución espacial de los fragmentos de bosque del Espinal incluidos en el estudio del anidamiento de aves forestales en el centro de Argentina; B, ejemplos de algunos de los fragmentos de bosque estudiados.

mum area requirement was obtained from Dardanelli et al. (2006). Body mass data were obtained from Dunning (2008). The dispersal ratio was calculated by dividing each species mean wing length (mm) by the cube root of its mean mass in grams (Fischer and Lindenmayer, 2005; Li et al., 2019). The relationship of this ratio with dispersal ability is positive so that species with higher ratios will disperse longer distances and species with lower ratios will disperse shorter distances and will consequently be poor

dispersers (Fischer and Lindenmayer, 2005; Li et al., 2019). Species traits were not correlated among them (Pearson r < 0.4).

Site variables We selected different landscape variables to characterize spatial configuration of the forest fragments: area (Area; ha), perimeter (m), two isolation variables: distance to the nearest fragment (DNF; meters) and

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proximity index in a 2 km–buffer area (PI), and shape index (SI) (table 3s in supplementary material). Area, Perimeter and Isolation metrics were calculated using Quantum GIS (QGIS) software. We estimated shape index as SI = Pm/Pc, where Pm is the measured perimeter of the fragment and Pc is the perimeter of a circular fragment of the same area. This SI index was used in similar studies and has been found to be less correlated to the area than other shape indices (Hinsley et al., 1995; Santos et al., 2002; Watson et al., 2004).

We found that the Perimeter and Shape index were highly correlated with Area (Pearson r ≥ 0.7). For this reason, we excluded these variables, as they were dependent on area.

Data analysis Matrices of presence–absence were assembled for both seasons. We used the metric based on overlap and decreasing fill 'NODF' to evaluate nestedness (Almeida–Neto et al., 2008). Through the online interface NeD (http://ecosoft.alwaysdata.net/) developed by Strona et al. (2014), nestedness can be calculated for the whole incidence matrix and independently for species (NODF between rows) and sites (NODF between columns). We ran five null models to estimate the significance level of nestedness: equiprobable row and column totals (EE), equiprobable row totals– Fixed column totals (EF), fixed row totals–equiprobable column totals (FE), and fixed–column and fixed–row totals (FF) algorithms. FF algorithm has shown to be highly restrictive and EE poorly restrictive (Ulrich and Gotelli, 2012; Strona and Fattorini, 2014; Matthews et al., 2015; Si et al., 2015). All these null models have strengths and weaknesses (Ulrich and Gotelli, 2012; Strona and Fattorini, 2014; Matthews et al., 2015; Si et al., 2015). However, PP and FF null models were described as less biased than the others (Ulrich and Gotelli, 2012). Furthermore, PP has been found to be the preferred model when research systems contain relatively small islands, when the scale of analysis is small, and because it is considered more ecologically meaningful (Ulrich and Gotelli, 2012; Strona and Fattorini, 2014; Matthews et al., 2015; Si et al., 2015). This model provides an unbiased proportional resampling of matrix incidences proportional to row and column totals (Almeida–Neto and Ulrich, 2011).

Expected nestedness metrics and related parameters were generated for winter and summer assemblages by running 1,000 Monte Carlo simulations.

The passive sampling hypothesis can be tested using the Coleman's (Coleman, 1981; Coleman et al., 1982) random placement model (Calme and Desrochers, 1999; González–Oreja et al., 2012; Wang et al., 2012; Li et al., 2019). The random placement model was used to verify whether passive sampling from species abundance distributions was driving the nestedness structure of bird communities. Coleman et al. (1982) state that the number of species ŝ(α) to be found residing in a given site depends on this site relative area, α (which equals the ratio of the area of a particular fragment to the summed area of all frag-

ments), and the overall abundances n1, n2,…, ns of the S species represented in C, which is a collection of N individuals from S species (Coleman, 1981): S

ŝ(α)= S ‒

S

i=1

(1 ‒ α)

ni

The variance σ2ŝ(α) is determined as S

σ2(α)=

S

i=1

S

(1 ‒ α)

ni

‒

S(1 ‒ α)2

ni

i=1

If the hypothesis of random placement holds roughly two–thirds of the points should fall within the band bounded by ± one standard deviation of the expected curve, or if less than two–thirds of the points fall within the bands, it should be rejected (Coleman et al., 1982).

To check for spatial autocorrelation in the data (i.e. figures of variables sampled at nearby locations tend to have more similar values than would be expected by chance) we fitted a semivariogram randomisation analysis based on 99 Monte Carlo permutations (Isaaks and Srivastava, 1989). Spatial autocorrelation in the response variable (species richness) violates the assumption of independently and identically distributed errors and hence inflates type I errors (Dormann, 2007).

The order in which sites and species are organized

by NODF can be compared with several independent variables to evaluate their possible roles in producing nestedness (Patterson and Atmar 2000). To test the effects of forest fragment traits on nestedness, we performed Spearman rank correlations between the forest fragments rank orders in the maximally packed matrix and ranked traits of the forest fragments (table 3s in supplementary material). Similarly, to assess the role of species traits in driving nestedness patterns, we calculated Spearman rank correlations between the species rank orders in the maximally packed matrix and ranked species traits (table 2s in supplementary material). Statistical significance was established at P < 0.05.

Partial Spearman rank correlations and semivariograms were performed using R (R Development Core Team, 2016).

Results We recorded 43 forest resident species in the fragments (tables 2s, 4s, and 5s in supplementary material). Rarefaction analyses confirmed that all forest patches were adequately and comparatively sampled in both seasons (fig. 2). Four species were ubiquitous for both seasons, the stripe–crowned spinetail (Cranioleuca pyrrhophia), the pearly–vented tody–tyrant (Hemitriccus margaritaceiventer), the golden–billed saltator (Saltator aurantiirostris), and the black–and– chestnut warbling–finch (Poospiza whitii) (tables 4s, 5s in supplementary material). Three other species had only one absence in winter, the great antshrike (Taraba major), the white–tipped plantcutter (Phytotoma rutila),

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Species diversity

40 30 20

Summer Winter

10 0

Interpolated Extrapolated 0

1,000

2,000 Number of individuals

3,000

4,000

Fig. 2. Rarefaction curves for bird species richness for resident forest birds of forest fragments in the austral winter (blue) and austral summer (orange), in Córdoba, Argentina.

Fig. 2. Curvas de rarefacción de la riqueza de especies de aves forestales residentes en fragmentos de bosque en el invierno austral (azul) y el verano austral (naranja), en Córdoba (Argentina).

and the creamy–bellied thrush (Turdus amaurochalinus) (tables 4s and 5s in supplementary material); and one species had only one absence in summer, the brown cachalote (Pseudoseisura lophotes). All these species were common in the fragments. On the other hand, eight species: the sharp–shinned hawk (Accipiter striatus erythronemius), the spot–winged falconet (Spiziapteryx circumcinctus), white–barred piculet (Picumnus cirratus), the scimitar–billed woodcreeper (Drymornis bridgesii), the narrow–billed woodcreeper (Lepidocolaptes angustirostris), the crested hornero (Furnarius cristatus), the suiriri flycatcher (Suiriri suiriri) and the cinereous tyrant (Knipolegus striaticeps) occupied only the largest fragments (≥ 80 ha) and were all scarce. Some of these species occupied smaller fragments during winter (tables 4s and 5s in supplementary material).

The semivariogram did not show a significant association between the spatial distribution of the forest fragments and species richness in winter or summer (fig. 1s in supplementary material).

The bird assemblages were significantly nested in both seasons (table 1) for all null models except the very restrictive FF (fixed–fixed) model. Both NODF values and matrix structure were similar between seasons for resident birds (table 1). Our results show a high temporal constancy in the nested pattern for resident bird assemblages in Espinal forest fragments in Central Argentina.

Spearman's rank correlations showed that the remnant order that maximized nestedness in both winter and summer was correlated with remnants ordered according to the area and distance to the nearest fragment (table 2). The proximity index was not significantly correlated with remnant order.

Species order in matrices packed for maximum nestedness showed a significant relationship with minimum area requirement, trophic guild, and range size both in winter and summer, and with species distributional range size in summer (table 2). Species traits commonly related to colonization ability like body mass and dispersal ratio were not significantly correlated with the species order.

The nestedness of forest birds' assemblages was not caused by passive sampling in summer or winter assemblages. Only one data point in summer and four out of 13 in winter data points fell within ± 1 SD of the expected Coleman's species/relative area curves (fig. 3, 4), which means that it did not follow expectations from the random placement hypothesis.

Discussion Bird assemblages in fragmented Espinal forest in Central Argentina showed a non–random structure, with species aggregation consistent with the nested subset model across seasons, for the whole matrix, and for columns (forest fragments) and rows (bird species) separately. This nested structure did not follow the random placement hypothesis (Coleman, 1981; Coleman et al., 1982).

The nestedness structure in our studied system showed a structure consistent with the selective extinction hypothesis as nestedness was related to fragment area and species traits associated with extinction proneness such as trophic guild, minimum area requirement and distributional range size. The correlation of fragment area and species traits with nested rank indicated that bird assemblages on

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Table 1. Comparative analyses of nestedness for resident forest birds in forest fragments between seasons, in Córdoba, Argentina. Nestedness metrics and related parameters are provided for two seasons: winter and summer. P–values were generated by 1,000 Monte Carlo simulations: EE, equiprobable–eqiprobable null model; PP, proportional–proportional null model; FF, fixed–fixed null model; SD, standard deviation; * significant nestedness (P < 0.05); matrix, nestedness estimator for the whole presence–absence matrix; species, row nestedness estimator among species (based on species incidence); fragments, column nestedness estimator among fragments (based on species composition).

Tabla 1. Análisis comparativos del anidamiento de las aves residentes en fragmentos de bosque entre estaciones, en Córdoba (Argentina). Se proporcionan los valores de anidamiento y los parámetros relacionados para las dos estaciones: invierno y verano. Los valores P se generaron a partir de 1.000 simulaciones de Monte Carlo: EE, modelo nulo equiprobable–equiprobable; PP, modelo nulo proporcional–proporcional; FF, modelo nulo fijo–fijo; SD, desviación estándar; * anidamiento significativo (P < 0,05); matrix, estimador de anidamiento para toda la matriz de presencia–ausencia; species, estimador de anidamiento de fila entre especies (basado en la incidencia de especies); fragments, estimador de anidamiento de columna entre fragmentos (basado en la composición de especies).

Season Extent

NODFobs NODFEE NODFEF NODFFE NODFPP NODFFF

Winter Matrix

84.51 57.95* (2.06) 73.03* (0.81) 62.00* (2.18) 66.77* (2.20) 85.07 (0.46)

Species

84.19 57.87* (2.15) 73.23* (0.66) 61.43* (2.31) 66.70* (2.21) 84.83 (0.479)

Fragments

88.29 58.81* (2.94) 70.72* (3.19) 68.54* (0.84) 67.57* (2.97) 87.93 (0.25)

Summer Matrix

86.11 57.08* (2.12) 72.83* (0.87) 60.96* (2.16) 66.25* (2.24) 85.88 (0.49)

Species

85.93 57.02* (2.21) 72.99* (0.72) 60.42* (2.28) 66.19* (2.97) 85.49 (0.54)

Fragments

88.25 57.75* (2.91) 71.02* (3.94) 67.17* (0.84) 66.84* (3.05) 88.27 (0.25)

smaller fragments were predictable subsets of richer faunas occurring on larger fragments. It also indicated that species requiring large areas have a restricted

distribution range and high trophic guild, are predictable subsets of species that do not need large areas, are broadly distributed, and are at low trophic guild.

Table 2. Results of Spearman Rank correlations of forest fragments nestedness rank order with fragment traits; and bird species nestedness rank order with bird life history traits, for the maximally packed nested matrix: DNF, distance to nearest fragment; PI, proximity index in 2 km buffer; MAR, minimum area requirement; RS, distribution range size; TG, trophic guild; BM, body mass; DR, dispersal ratio. (Level of significance: ** P < 0.01, * P < 0.05) Tabla 2. Resultados de las correlaciones de rango de Spearman entre el orden de rango de anidamiento de los fragmentos de bosque con los rasgos de los fragmentos, por un lado, y entre el orden de rango de anidamiento de las especies de aves con los rasgos de la historia de la vida de las aves, por otro, para la matriz anidada empaquetada al máximo: DNF, distancia al fragmento más cercano; PI, índice de proximidad en la zona de amortiguación de 2 km; MAR, requerimiento mínimo de superficie; RS, tamaño del área de distribución; TG, gremio trófico; BM, masa corporal; DR, índice de dispersión. (Nivel de significancia: ** P < 0,01, * P < 0,05).

Fragment traits

Species life–history traits

Area DNF PI

MAR TG RS BM DR

Winter

0.60* 0.63* 0.42

0.75** 0.35* 0.20 0.10 0.11

Summer

0.78** 0.59* 0.53

0.78** 0.41** 0.33* 0.04 0.25

Animal Biodiversity and Conservation 44.1 (2021)

25

50 45

Species number

40 35 30 25 20 15 10 5 0 –3.5

–3

–2.5 –2 –1.5 Log (relative area)

–1

–0.5

0

Fig. 3. Comparison of observed data to expected values under the random placement model for resident forest birds in forest fragments in the austral summer, in Córdoba, Argentina. Expected values (solid line) and associated standard deviations (± 1 SD; dashed lines) are shown. Open circles represent observed species richness.

Fig. 3. Comparación de los datos observados y esperados según el modelo de ubicación aleatoria para aves forestales residentes en fragmentos de bosque en el verano austral, en Córdoba (Argentina). Las líneas continuas representan los valores esperados y las líneas discontinuas representan las desviaciones estándar asociadas (± 1 DE; líneas discontinuas). Los círculos representan la riqueza de especies observada.

These results are in agreement with similar studies in fragmented habitats where selective extinction arises as the most common driver of nestedness structure (Wright et al., 1998; Matthews et al., 2015; García–Quintas and Parada, 2017; De la Hera, 2019). The importance of extinction driven processes in shaping community assembly has been found in many fragmented landscapes (Martinez–Morales, 2005). It has been suggested that the trigger for this kind of patterns is a faunal relaxation process, which is characteristic of highly fragmented or relictual forest ecosystems (Brooks et al., 1999; Ferraz et al., 2007).

The prevalence of colonization driven patterns is less frequent in fragmented terrestrial habitats (Wright et al., 1998; Watling and Donnelly, 2006), and it appears to be an important driver for other isolated habitats such as mountaintops, land–bridge islands and oceanic islands (Cook and Quinn, 1995; Wright et al., 1998; Watling and Donnelly, 2006; Meyer and Kalko, 2008; García–Quintas and Parada, 2017). Our results showed that selective colonization seems to have some influence on community assembly as distance to nearest fragment was correlated with fragments nested order. However, species traits commonly associated with dispersal ability such as body mass and dispersal ratio were not related to species order. In this regard, it is possible that dispersal ratio and body mass were not good indicators

of dispersal ability for birds in this study. The other possibility is that because colonization has marginal importance in driving nestedness structure in our system, it does not express any significant relationship with our dispersal ability proxies. Consequently, we could venture to say that the selective colonization hypothesis only partially explains birds' nestedness structure in Espinal forest of Central Argentina. One possible explanation for the low influence of selective colonization is that species with low dispersal ability have already become extinct in the study area. We documented this in a previous study in the same area where, for example, most large birds have disappeared from fragmented forests (Dardanelli et al., 2006).

Moreover, as has been demonstrated in other studies (Watling and Donnelly, 2006; Matthews et al., 2015), it is very difficult to find biologically meaningful isolation effects on assemblage structure. In the case of bird communities in South America, it is even more challenging considering knowledge of colonization ability or dispersal rate of species is scarce (Faaborq et al., 2010; Jahn et al., 2017). It is therefore challenging to assess the role of selective colonization hypothesis in the assemblage structure of Espinal forest birds.

Nevethless, it seems to have secondary importance as a driver of nestedness aggregation. This highly fragmented forest has almost disappeared from this region and the few remaining fragments have undergone faunal relaxation for many years, giving

Dardanelli and Bellis

26

50 45

Species number

40 35 30 25 20 15 10 5 0 –3

–2.5

–2 –1.5 Log (relative area)

–1

–0.5

0

Fig. 4. Comparison of observed data to expected values under the random placement model for resident forest birds of forest fragments in the austral winter, in Córdoba, Argentina. Solid lines represent expected values and dashed lines represent associated standard deviations (± 1 SD; dashed lines). Open circles represent observed species richness.

Fig. 4. Comparación de los datos observados y esperados según el modelo de ubicación aleatoria para las aves forestales residentes en fragmentos de bosque en el invierno austral, en Córdoba (Argentina). Las líneas continuas representan los valores esperados y las líneas discontinuas representan las desviaciones estándar asociadas (± 1 DE; líneas discontinuas). Los círculos representan la riqueza de especies observada.

rise to extinction driven biotas. Consequently, we did not find any relationship between proximity indexes or any species trait related to dispersal ability with nestedness order.

Nestedness structure did not vary between seasons. Consequently, seasonality does not seem to influence nestedness in our system. These results are consistent with the results of Seoane et al.

(2013), García–Quintas and Parada (2014), Zhou et al. (2014) and De la Hera (2019) who found no seasonality effects on nestedness structure of birds in isolated woodlots in Spain and birds of urban parks in Hong Kong and Spain. Our results, however, contradict the results of Murgui (2010) who found small but significant differences in nestedness structure and species–area relationships between seasons in urban parks in Spain. This author ruled out an increase in mortality outside the breeding seasons as they have mild winters. He considered that the use of alternative habitats outside of parks during autumn and winter is the most likely explanation for the observed patterns. The winters in the Espinal forest fragments in Central Argentina are mild and bird species are probably less prone to use alternative habitats than birds in urban parks. Another difference is that specialist birds analyzed in our system are generally more sensitive to disturbances and less adaptable than generalist species in urban parks in Spain.

Protecting the larger and less isolated forest fragments would be the most effective way to preserve resident birds in this relictual Espinal forests. The preservation of large and less isolated fragments would help to protect resident birds with large area requirements, small distribution range size, and high trophic guilds (i.e. carnivorous and insectivorous species). For example, by protecting the two largest forest fragments it is possible to maintain most species (97.7 % in summer; 95.3 % in winter) of forest birds in the dataset. As mentioned by other authors, nestedness analysis can be used in combination with other approaches to provide valuable recommendations for decision–making when long–term data are not available. Based on the results of the present study, future landscape management of Espinal forest should ensure the protection of large fragments as they preserve the largest populations of resident forest species throughout the year.

Acknowledgements We thank G. and M. Esmóris, R. Parra, A. Varselotti and F. Mansilla for providing access to their properties. We also thank D. A. Serra and M. Nores for assistance with the bird surveys. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) provided partial funding.

Animal Biodiversity and Conservation 44.1 (2021)

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Evaluación de un protocolo automatizado para la obtención de medidas morfométricas de huevos de aves a partir de fotografías digitales V. M. Ramírez–Arrieta, D. Denis, Y. Ferrer–Sánchez

Ramírez–Arrieta, V. M., Denis, D., Ferrer–Sánchez, Y., 2021. Evaluación de un protocolo automatizado para la obtención de medidas morfométricas de huevos de aves a partir de fotografías digitales. Animal Biodiversity and Conservation, 44.1: 31–43, Doi: https://doi.org/10.32800/abc.2021.44.0031 Abstract Evaluation of a protocol for automated extraction of morphometric measurements from avian eggs using digital photography. As many ecomorphological studies are limited by the time required to gather manual measurement data, automatizing the process is an important focus of methodological innovations. We developed, implemented and validated a protocol for the semi–automated extraction of a set of morphometric variables of egg size and shape from digital pictures. The protocol was implemented in R language as a web app called OvometriK. After binarizing and calibrating images, this protocol uses geometric and trigonometric functions to calculate eleven egg variables. We tested calculations in several ways, assuming contour continuity or using voxel counts. Application was validated with geometric shapes and 30 manually–measured chicken eggs.

Mathematical validation with spheres showed that the algorithm provided high precision diameter measures, with a correlation of 99.9 %. Average estimation error was 1.4 %. The mathematical volume estimation was underestimated by 27 %, while voxels were underestimated by only 6 %. Differences between manual egg measurements of diameters and those obtained from images was less than 3 mm (4 %). Correlation between estimated volume and measured by silica gel filling was higher than 90 % using the voxel count method.

Neither inclination angle or picture resolution had significant effects on precision (3.2 % maximum difference).

Measures showed high repeatability and represent a significant saving in processing time. This new protocol represents an improvement on previous programs regarding limitations of platform, accessibility and number of variables. Furthermore, its flexibility and openness means it can be adapted to other specific applications.

Key words: Automatizing, Morphometric, Digital image processing, Oology, Egg dimensions Resumen Evaluación de un protocolo automatizado para la obtención de medidas morfométricas de huevos de aves a partir de fotografías digitales. Muchos estudios ecomorfológicos están limitados por el tiempo que demora la recopilación manual de mediciones. Por ello, las innovaciones metodológicas han dado tanta importancia a la automatización del proceso. En el presente trabajo se elabora, implementa y valida un protocolo para la obtención semiautomatizada de un conjunto de variables morfométricas de los huevos de las aves a partir de fotografías digitales. El protocolo se implementó en lenguaje R como una aplicación web llamada OvometriK que, luego de binarizar y calibrar las imágenes, permite calcular once variables utilizando funciones geométricas y trigonométricas. Se prueban varias vías de cálculo, suponiendo la continuidad del contorno o por conteo de vóxeles. La aplicación se valida con figuras geométricas y 30 huevos de gallina medidos manualmente. La validación matemática con círculos mostró que el algoritmo fue capaz de medir los diámetros con gran precisión, con una correlación del 99,9 %. El error de estimación fue del 1,4 % en promedio. La estimación del volumen por métodos matemáticos lo subestima en un 27 %, mientras que por conteo de vóxeles solo lo subestima en un 6 %. La diferencia entre las medidas manuales de los diámetros de los huevos y las obtenidas a partir de las imágenes fue inferior a 3 mm (4 %). La correlación entre el volumen estimado y medido por vaciado con gel de sílice fue superior al 90 % cuando se emplea el método de conteo de vóxeles. Ni el ángulo de inclinación de los huevos ni la resolución de las fotografías tuvieron efectos significativos (diferencia máxima del 3,2 %).

Las mediciones mostraron una replicabilidad alta y representaron un ahorro significativo de tiempo. El protocolo ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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representa una mejora respecto de las limitaciones de plataforma, la accesibilidad y el número de variables en comparación con programas anteriores, además de que su carácter abierto y flexible permite adaptarlo a otras aplicaciones específicas.

Palabras clave: Automatización, Morfometría, Procesamiento de imágenes digitales, Oología, Dimensiones de huevos Rebut: 13 V 20; Conditional acceptance: 27 VII 20; Final acceptance: 31 VII 20 Víctor M. Ramírez–Arrieta, Instituto de Investigaciones del Mar, Cuba.– Dennis Denis, Universidad de La Habana, Cuba.– Yarelys Ferrer–Sánchez, Universidad Técnica Estatal de Quevedo, Ecuador.

Corresponding author: D. Denis. E–mail: dda@fbio.uh.cu ORCID ID: V. M. Ramírez–Arrieta: 0000-0002-4642-3143; D. Denis: 0000-0003-4808-7195

Y. Ferrer–Sánchez: 0000-0003-0623-1240

Animal Biodiversity and Conservation 44.1 (2021)

Introducción Muchos estudios ecomorfológicos están limitados por la combinación del número de ejemplares que debe ser procesado y la gran cantidad de variables que se pueden tomar de cada uno, lo que supone una inversión considerable de tiempo y esfuerzo de los investigadores. Por ello, las innovaciones metodológicas han dado tanta importancia a la automatización del proceso (Corney et al., 2012a, 2012b, Easlon y Bloom, 2014, MacLeod y Steart, 2015). Los avances en las técnicas digitales y en el análisis de imágenes han facilitado el desarrollo de algoritmos de toma de datos a partir de fotografías de objetos biológicos mediante la obtención de sus contornos o de puntos clave (Ramírez–Arrieta y Denis, 2020).

Las dimensiones y forma de los huevos son una parte importante de las estrategias reproductivas de las aves y tienen un papel esencial en las historias de vida (Lack, 1968), ya que están relacionadas con aspectos como la conducta o la masa corporal de los progenitores, la fecha de puesta, la composición del huevo, el éxito de anidamiento, el tamaño de las crías y la supervivencia de los pichones (Nol et al., 1997; Grønstøl, 1997; Flint y Sedinger, 1992; Ricklefs, 1984; Arnold, 1989; Reed et al., 1999; Briskie y Sealy, 1990; Williams, 1994; Galbraith, 1988; Grant, 1991). Por ello, la medición de estas estructuras ha sido un aspecto fundamental del estudio de la biología de la reproducción, y muchos de sus patrones de variación todavía se desconocen y merecen mayor atención, a pesar de haber sido objeto de un amplio debate (Slagsvold et al., 1984; Arnold, 1999; Jover et al., 1993).

En algunos de estos estudios, se ha procesado un elevado número de muestras, por ejemplo, Denis (2015) describió los patrones de variación entre los huevos de nueve especies de garzas a partir de las dimensiones externas de 3.142 huevos y Stoddard et al. (2017) hicieron un amplio estudio de las variaciones en la forma de los huevos de 1.400 especies de aves. Algunas variables de importancia fisiológica o ecológica han sido estimadas a partir de las dimensiones lineales, como en el caso del volumen, la superficie o la masa (Preston, 1974; Hoyt, 1979).

Tradicionalmente, estas dimensiones se han determinado por mediciones directas, pero las medidas tomadas en el campo con instrumentos manuales son propensas a introducir errores de manipulación y del observador. La manipulación de los huevos puede afectar negativamente al éxito o la supervivencia de los nidos, particularmente en la medición del volumen mediante el cálculo del desplazamiento de agua (Hoyt, 1976; Tarassov, 1977; Loftin y Bowman, 1978; Thomas y Lumsden, 1981; Szekely et al., 1994; Kern y Cowie, 1996). Con frecuencia, el volumen o el peso se han estimado a partir de modelos matemáticos que emplean las dimensiones lineales y, en algunos casos, variables de forma específicas de cada especie (Westerkov, 1950; Coulson, 1963; Stonehouse, 1966), pero esto no recoge la variabilidad intraespecífica de la forma de los huevos. La forma también se ha estudiado frecuentemente mediante coeficientes entre medidas lineales (ver resumen

33

en Preston, 1969; Narushin, 2001; Havlíček et al., 2008; Troscianko, 2014), siendo las más usadas la elongación y la asimetría.

Varios autores han desarrollado métodos computarizados automáticos para obtener medidas precisas de los parámetros de la talla de los huevos a partir de fotografías digitales (Paganelli et al., 1974; Mand et al., 1986, Bridge et al., 2007). Dangphonthong y Pinate (2016) usan el procesamiento de imágenes digitales para estimar el peso de huevos de aves de granja. Las variaciones en la curvatura de la cáscara también son un componente importante de la forma y, por lo general, se describen con perfiles bidimensionales extraídos de fotografías, que en un primer momento se calculaban de forma aproximada mediante ecuaciones matemáticas (Hutt, 1938; Bonnet y Mongin, 1965; Besch et al., 1968; Carter, 1970, Nedomova et al. 2009; Troscianko, 2014) y que actualmente se estudian en mayor profundidad con descriptores derivados de funciones de Fourier y puntos clave (Johnson et al., 2001; Havlíček et al., 2008; Bravo y Marugan–Lobon, 2012; Murray et al., 2013; Deeming y Ruta, 2014; Deeming, 2017). Estas herramientas disminuyen el tiempo de manipulación del huevo y aumentan la precisión y repetibilidad de las mediciones. El empleo de fotografías digitales tiene como ventaja que su precisión no depende de la especie y la forma de sus huevos como sucede con los modelos alométricos. Las fotografías se toman con mayor rapidez, lo que minimiza el tiempo de manipulación de los huevos sin detrimento en la exactitud de la medida, lo cual minimiza los riesgos de rotura accidental o abandono de los nidos. Por último, las fotografías se pueden conservar, lo que permite la trazabilidad de errores y otros estudios futuros. Por estas razones, se prevé que los métodos que emplean proyecciones bidimensionales para obtener la forma de los huevos se seguirán utilizando por un buen tiempo dada su simplicidad y bajo coste (Attard et al., 2017).

Sin embargo, el empleo de fotografías también es una fuente de numerosas imprecisiones que hay que tener en cuenta. Entre ellas, se cuentan problemas asociados a la toma de fotografías, como la falta de coplanaridad entre el eje de los huevos y el plano de las imágenes, las sombras creadas por la iluminación direccional y las diferencias entre la resolución de las fotografías. Otros problemas tienen que ver con imprecisiones asociadas al procesamiento digital de las imágenes, como la binarización y los filtros de detección de bordes o de suavizados. Existen también problemas asociados a la variabilidad biológica de los propios huevos, que también afectan a la repetibilidad de las mediciones manuales tradicionales, sobre todo la relacionada con la ausencia de simetría radial. Estos efectos se han evaluado en contadas ocasiones y muchas veces se pasan por alto o se subestiman, para ahorrar tiempo de procesamiento de las muestras, pero pueden llegar a ser de una magnitud significativa.

Dados estos antecedentes, en el presente trabajo se elabora, implementa y valida un protocolo de análisis digital, programado en forma de aplicación web en lenguaje R (R Core Team, 2018), para la extrac-

34

ción semiautomatizada de un conjunto de variables relacionadas con las dimensiones y la forma de los huevos de las aves a partir de fotografías digitales.

La aplicación genera datos compatibles con el propio programa R y el MS Excel, por lo que se puede integrar a otros algoritmos de análisis estadísticos.

Por ser de código abierto es gratuita, modificable y puede adaptarse a otros objetos biológicos similares (frutas, semillas, estructuras).

Material y métodos El protocolo de medición a partir de fotografías se basa en la extracción de las coordenadas del contorno del huevo, a partir de la modificación del algoritmo propuesto por Claude (2008), luego de binarizar la imagen y transformar las unidades de píxeles a milímetros por medio de una escala de referencia que debe aparecer en las fotografías. A partir de estos contornos, se calculan automáticamente once variables morfométricas con funciones geométricas y trigonométricas básicas. Estas variables son el diámetro mayor (distancia máxima entre un par de puntos del contorno), el diámetro menor (distancia máxima entre dos puntos, perpendicular al eje del diámetro mayor), los diámetros en los tres cuartiles del diámetro mayor, el volumen del huevo, el área superficial y el nivel de asimetría (fig. 1). El volumen se estimó por tres vías, a partir de la suma de secciones transversales, que se suponen cilindros de 1 píxel de altura. La primera vía matemática simple consistió en estimar el volumen a partir del cálculo geométrico del volumen de un cilindro, haciendo una aproximación matemática en la que se supone que los bordes del huevo son superficies continuas. La segunda vía fue el simple conteo de vóxeles en cada sección. "Vóxel" es el término de origen inglés para referirse a un elemento de volumen (acrónimo de "volume element"), equivalente tridimensional del concepto de píxel ("picture element"). Para estimar el volumen por esta vía, se utilizaron valores discretos, con lo cual se elimina el sesgo de las aproximaciones de continuidad. En ambos métodos se supone la circularidad transversal en cada sección del huevo, es decir, que los cortes transversales son círculos perfectos (también se supone en Bridge et al., 2007).

La tercera vía fue la ecuación alométrica descrita por Hoyt (1979), que parte de las dimensiones lineales estimadas previamente (diámetro mayor y menor).

Esta ecuación, obtenida de forma empírica por su autor para 23 especies de aves, es una manera tradicional de estimar el volumen de los huevos que por defecto emplea el coeficiente volumétrico general de 0,509, pero que contempla la opción de utilizar un coeficiente específico de cada especie, como los que se han determinado posteriormente para otras especies (p. ej.: Kern y Cowie, 1996; Denis et al., 2008).

Para hacer una estimación más precisa de la superficie del huevo, se supuso que cada sección de 1 píxel de grosor era la proyección de un semicono cuyo diámetro mayor era igual al de la sección anterior (como sugieren Paganelli et al., 1974). El centro del huevo coincide con el punto medio del eje del diámetro

Ramírez–Arrieta et al.

mayor, y el centroide se calcula como la media de las coordenadas de todos los puntos que forman el contorno (que puede presentar irregularidades locales por defectos de la imagen).

La forma de los huevos se determina mediante los descriptores elípticos de Fourier, calculados a partir del contorno normalizado por el radio mayor. El número de armónicos se puede variar manualmente, pero por defecto se emplean cuatro, que según Denis (2014) son suficientes para describir las formas más frecuentes de los huevos de las aves. Estos se pueden reducir, opcionalmente, con un análisis de componentes principales, que permite calcular el puntaje de los componentes efectivos. Estos puntajes pueden ser usados como variables de forma en otros análisis.

Se calculan, además, tres indicadores para evaluar la asimetría: la proporción de área que representa la mitad vertical superior del huevo (extremo más fino) en relación con la mitad inferior (extremo más oblongo); la excentricidad del huevo, dada por la distancia entre el centroide y la mitad del diámetro mayor del huevo, y el porcentaje que representa el área de la sección longitudinal del huevo en relación con el rectángulo externo mínimo que contiene la figura. Estos índices suelen ser bajos en los huevos más redondeados y simétricos y relativamente más altos en los más alargados y asimétricos.

Todo este protocolo se implementó en una aplicación de R 3.5.1 (R Core Team, 2018) llamada Ovometrik, con una interfaz gráfica web confeccionada con el paquete shiny (Chang et al., 2018). Emplea además, los paquetes shinyalert, shinyWidgets, shinyBS, zip, imager, imagerExtra y Momocs. La aplicación puede ser utilizada en línea en el sitio https://victormramirez. shinyapps.io/ovometrik/ o descargada para su uso sin conexión desde el mismo sitio. Esta aplicación es capaz de manejar imágenes en formatos .png, .jpeg y .bmp, y el tiempo de carga está en relación directa con el tamaño de las imágenes, pero la versión en línea solo puede cargar un máximo de 4.000.000 de píxeles por imagen (2.000 x 2.000). Para imágenes de tamaño superior es necesario descargar la versión sin conexión, cuya capacidad de procesamiento dependerá de los recursos de la computadora en la que se ejecute.

Si las fotos de los huevos se toman de forma estandarizada (igual fondo homogéneo, cámara, resolución y distancia) se pueden procesar automáticamente todas las imágenes que se desee; de lo contrario, hay que supervisar manualmente cada imagen para fijar las escalas, fijar el umbral de binarización en el histograma de valores de grises y ubicar los huevos. La escala se establece a partir de un objeto de referencia, de longitud conocida, en la imagen. Los resultados (coordenadas del contorno, dimensiones lineales y descriptores de Fourier) se exportan en archivos en formato de texto (.csv) con el nombre de la imagen procesada como identificador de caso. Una descripción más detallada del procedimiento para trabajar en la aplicación puede ser consultada en su ayuda en línea.

Para la validación de OvometriK y del protocolo de medición se siguieron varios niveles. El primero, dirigido a comprobar la efectividad de los algoritmos matemáticos de extracción de las variables, se realizó

Animal Biodiversity and Conservation 44.1 (2021)

A

B

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Vóxel

Diámetro mayor

asimetría D.p1 excentricidad centro D.p2 centroide D.p3 tro me Diá enor m Rectángulo externo mínimo

Aproximación matemática al cálculo de volumen

Aproximación matemática al cálculo de superficie

Fig. 1. Representación de las dimensiones tomadas en los huevos a partir de las fotografías digitales calibradas (A) y de las aproximaciones que se realizan al hacer las estimaciones por medio de conteo de vóxeles o de ecuaciones matemáticas (B) (D.p1, D.p2, D.p3: diámetro transversal en los cuartiles del eje del diámetro mayor).

Fig. 1. Representation of egg measurements extracted from calibrated digital pictures (A) and numerical approximation when using estimates from voxels or mathematical equations (B) (D.p1, D.p2, D.p3: transversal diameter at each quartile of longitudinal axis).

con figuras geométricas (círculos) perfectas e imágenes binarias (n = 60). En estas imágenes, se eliminan los posibles errores debidos al procesamiento digital, el umbral de binarización y la variabilidad asociada a las asimetrías naturales de la forma de los huevos, así como los posibles errores de manipulación y toma de fotografías. Las dimensiones estimadas por OvometriK se compararon con las obtenidas por el programa ImageJ v3.6 (Schindelin et al., 2015). El segundo nivel de validación se llevó a cabo con 30 huevos de gallina doméstica (Gallus gallus), que se midieron manualmente con un pie de rey (0,01 mm de precisión) y cuyo volumen interno se midió por rellenado con gel de sílice, siguiendo el protocolo empleado por Denis et al.

(2008). La validación de los coeficientes de Fourier se hizo comparando los obtenidos por la aplicación con los obtenidos a partir de las mismas imágenes con el programa Shape v.1.3 (Iwata y Ukai, 2002).

La repetibilidad de las mediciones se evaluó tomando cinco veces todas las medidas manuales (por la misma persona) y procesando cinco fotografías digitales (de dimensiones 1.024 x 683 píxeles) perpendiculares hacia abajo, de cada huevo, en distintas rotaciones alrededor del eje mayor, permitiendo que adoptasen su inclinación natural. Como el ángulo de inclinación del huevo puede influir marcadamente en las medidas hechas a través de la proyección plana de la imagen, se midieron los ángulos de inclinación natural de cada huevo al descansar sobre una superficie plana a partir de fotografías laterales. Para evaluar el efecto de este ángulo, se tomaron también fotos superiores controlando manualmente la coplanaridad entre el eje central del huevo y el plano de la fotografía (fig. 2).

Como estos huevos son de color blanco, el fondo que

se utilizó fue negro. Para evaluar el efecto de la calidad de la imagen, se tomaron dos series adicionales de fotografías de menor calidad: una a menor resolución (824 x 550 píxeles) y otra con baja sensibilidad (bajo ISO) e iluminación insuficiente.

El nivel de efectividad de las fotografías digitales se evaluó mediante regresiones lineales entre las variables obtenidas por vía manual y las calculadas siguiendo el protocolo sobre las imágenes digitales, así como para evaluar los efectos relativos de la posición del huevo, el ángulo de inclinación y la calidad de la imagen. La replicabilidad se evaluó por medio de los coeficientes de variación entre las medidas repetidas sobre los mismos huevos. Para asegurar la reproducibilidad del trabajo, todos los datos y el código de la aplicación en R se encuentran disponibles de forma gratuita en el repositorio Figshare (https:// figshare.com/s/2cd84268ed4f69387f80).

Resultados La validación matemática con círculos perfectos mostró que el algoritmo fue capaz de medir el diámetro de los círculos con una alta precisión, ya que existe una correlación superior al 99,9 % entre las medidas de los diámetros obtenidas por el programa ImageJ y por la aplicación de R (fig. 3A). El error de estimación fue generalmente en el sentido de la subestimación de la medida por OvometriK entre 0,3 y 2,8 unidades, con un promedio general de –1,7 (1,4 %) y estuvo correlacionado de manera negativa con el tamaño del círculo (r = –0,28; p < 0,05), de manera que a medida que los objetos que se miden son mayores,

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B

C Fig. 2. Representación de las orientaciones de la cámara en la toma de fotografías de huevos para validar la aplicación OvometriK en lenguaje R: A, orientación coplanar; B, orientación acimutal natural; C, orientación lateral para medir ángulo de inclinación.

Fig. 2. Representation of camera orientations when taking pictures of eggs for validating OvometriK software in R language: A, coplanar orientation; B, natural azimuthal orientation; C, lateral orientation for inclination angle measurement.

220

R = 0,9993 2

190 160 130 100 70 70 100 130 160 190 220 Diámetro obtenido por ImageJ

8.000

Volumen estimado por OvometriK

Distancia obtenida por OvometriK

y = x

7.000

Volumen por estimación matemática R2 = 0,9986

y = x

R2 = 0,9971

1.500 1.300

5.000

3.000

y = x

1.900 1.700

6.000

4.000

Superficie estimada por OvometriK

A

la diferencia entre estimaciones disminuye. El cálculo del volumen estimado fue ligeramente más variable, pero aun así, la relación con el volumen calculado fue superior al 99 % (fig. 3B). Al hacerse la estimación con el método matemático continuo, se tendió a sobreestimar el volumen un 27 %, mientras que el conteo de vóxeles fue mucho más preciso, con una ligera subestimación (6 %). La estimación de la superficie de la esfera a partir de la imagen también estuvo altamente correlacionada con la calculada con métodos trigonométricos (r = 99,8) (fig. 3C) aunque la sobreestimó sistemáticamente un 9,1 %, de media.

En la segunda fase de validación, las mediciones lineales tomadas de las fotografías de los huevos mostraron una alta coherencia con las medidas tomadas físicamente (fig. 4). La estimación fotográfica sobreestimó ligeramente las dimensiones lineales, con una diferencia entre los diámetros medidos por ambos métodos inferior a 3 mm (4 % de error). El cálculo del volumen arrojó resultados más variables, pero la correlación entre las estimaciones y las medidas manuales fue superior al 90 % con el método de conteo de vóxeles (fig. 5). Las estimaciones del volumen a partir de las fotografías fueron superiores a las mediciones manuales por rellenado con gel de sílice; en este sentido, la diferencia máxima se encuentra cuando se hacen las estimaciones suponiendo la linealidad de la superficie (promedio 31,6 %). El volumen estimado por el algoritmo de conteo de vóxeles arrojó resultados muy semejantes al estimado por la ecuación de Hoyt con las medidas digitalmente extraídas, con sobrees-

Volumen por conteo de vóxeles R2 = 0,9992

2.000 1.000 0 0 2.000 4.000 6.000 8.000 Volumen obtenido por cálculo

1.100 900 700 500 300 100 100 500 900 1.300 1.700 Superficie obtenida por cálculo

Fig. 3. Validación matemática del algoritmo de OvometriK, implementado en R, a través de la medición del diámetro y el volumen de círculos y esferas geométricamente perfectos, respectivamente, con imágenes binarias.

Fig. 3. Mathematical validation of the OvometriK algorithm, implemented in R, by measuring diameter and volume of geometrically perfect circles and spheres with binary images.

Diferencia media 1,7 ± 0,2 mm

y = x

59 57 55 R2 = 0,9883

53 51 51 53 55 57 59 61 Diámetro mayor estimado por OvometriK (mm)

47

37

Diferencia media 1,4 ±0,1 mm

46 45 44 43 42

R2 = 0,9917

41 40 39 39

65

y = x

41 43 45 47 Diámetro menor estimado por OvometriK (mm)

Volumen (cm3) manual

61

Diámetro menor (mm) manual

Diámetro mayor (mm) manual

Animal Biodiversity and Conservation 44.1 (2021)

Diferencia media 3,2 ±1,3 cm3

y = x

60

55

50

R2 = 0,9126

45 45 50 55 60 65 Volumen estimado por OvometriK (cm3)

Fig. 4. Relación entre las medidas físicas de 30 huevos de gallina y las estimadas a partir de fotografías con la aplicación OvometriK en lenguaje R. Fig. 4. Relationship between physical measurements of 30 chicken eggs and estimated measurements from its photographs with OvometriK application in R language.

timaciones del 7,1 % y el 7,6 %, respectivamente, en relación con el calculado manualmente. Cabe señalar que el volumen calculado por la ecuación de Hoyt con las dimensiones medidas manualmente sobre el huevo, subestimó al volumen medido por vaciado del contenido interno en un 3,9 % de media.

Las dimensiones estimadas por la aplicación OvometriK sobre fotos con y sin la corrección del ángulo de inclinación de los huevos (que varió entre 3,7º y 12,3º) mostraron que el efecto de este factor en la estimación de las dimensiones lineales es mínimo (fig. 6).

Aunque, como promedio, la afectación del volumen fue muy pequeña, en algunos casos las diferencias llegan a ser de hasta casi 6 cm3 (10 %), igual que en el caso del área superficial (hasta 4 cm2). Sin embargo, el hecho de que estas diferencias no estuviesen asociadas a la magnitud del ángulo de inclinación sugiere que están expresando en mayor medida las diferencias de las distintas vistas del mismo huevo (asimetrías radiales) que el propio efecto del ángulo.

El tamaño de las fotografías también tuvo un pequeño efecto en los valores medios de las mediciones, superior en el caso de las estimaciones de volumen, que llegó a ser un 3,2 % superior en las fotografías de mayor resolución (fig. 7). Las dimensiones lineales difirieron en menos de un 1 %, lo cual indica que la resolución de la imagen no reviste mucha importancia en la exactitud de las estimaciones.

El resto de las dimensiones e índices extraídos de los huevos tampoco mostraron diferencias marcadas asociadas al tamaño de las imágenes o al ángulo de inclinación de los huevos (tabla 1). El índice de asimetría del huevo, expresado en porcentaje, mostró

la mayor variabilidad (33 %), seguido del volumen (14 %) y el área superficial estimada (9 %).

La repetibilidad de las mediciones manuales de los huevos, dada por el coeficiente de variación entre las medidas repetidas sobre los mismos ejemplares, fue del 0,19 % para el diámetro mayor (DE = 0,27 % y máximo = 1,8 %) y del 0,24 % para el diámetro menor (DE = 0,18 % y máximo = 0,93 %). En el caso de emplear fotografías, el coeficiente de variación entre las mediciones del diámetro mayor fue del 2,55 % ± 1, el 33 % (mínimo = 1,04 % y máximo = 5,3 %) y para el diámetro menor de 2,60 % ± 1,30 % (mínimo = 1,09 % y máximo = 5,44 %).

Las mediciones manuales del conjunto total de huevos, realizadas por una misma persona, se tomaron durante 15 minutos de media (sin contar el tiempo posterior para pasar los datos a formato digital) en el caso de las dimensiones lineales, más entre 4 y 5 minutos por cada huevo para la medición del volumen. El procesamiento de las imágenes en la aplicación desarrollada se tomaba entre 2 y 3 minutos y el resultado ya sale en formato digital.

Discusión La validación matemática con círculos perfectos mostró que el algoritmo fue capaz de medir el diámetro de los círculos con una alta precisión. El empleo de imágenes en blanco y negro permite controlar el efecto de la binarización de las imágenes en escala de grises, cuyo umbral de corte determina la clasificación de los píxeles del contorno, que suelen ser

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63

y = x

Volumen medido (cm3)

61 59 57 55 53 51 49 47 45 45

Conteo de vóxeles R2 = 0,9126 Fórmula de Hoyt R2 = 0,8852 Estimación matemática contínua R2 = 0,8889

55 65 75 Volumen estimado por OvometriK (cm3)

Fig. 5. Comparación entre los métodos implementados en el programa OvometriK para estimar el volumen de los huevos a partir de las fotografías (por estimación matemática suponiendo continuidad, por conteo de vóxeles y por la ecuación de Hoyt).

Fig. 5. Comparison between volume estimation methods of eggs from pictures, implemented in OvometriK software (using mathematical equations assuming continuity, voxel counts and Hoyt's equation).

de tonos más claros. Al establecerse manualmente este umbral, se pueden producir diferencias en el orden de varios píxeles, que en términos de áreas o volúmenes pueden llegar a representar porcentajes elevados de variación en objetos de pequeño tamaño y en imágenes de baja resolución. En las fotografías reales de huevos, la binarización produce contornos irregulares que influyen en la precisión de las medidas; la opción de suavizado, si bien reduce este efecto, también puede alterar de forma imperceptible las medidas tomadas, por lo que debe usarse con precaución y de manera similar entre las muestras que se vayan a analizar conjuntamente.

La validación del algoritmo con esferas es un paso imprescindible, ya que el funcionamiento de la aplicación se puede comparar con una medida geométricamente calculable, lo cual no es posible si se emplean huevos directamente por su forma irregular (Bridge et al., 2007). La diversidad de formas en los huevos de las aves es un fenómeno bien conocido que refleja la diversidad taxonómica (Olsen et al., 1994; Stoddard et al., 2017). Las formas varían desde los huevos casi esféricos de los búhos (Hoyt, 1976), pasando por los

ligeramente puntiagudos de las gallinas (Havlíček et al., 2008) hasta los extremadamente puntiagudos de ciertas vadeadoras, álcidos y pingüinos (Birkhead et al., 2017; Stoddard et al., 2017). Al aplicar el algoritmo programado en la aplicación sobre fotos de huevos, en escala de grises se suman tres fuentes importantes de variabilidad: la dada por la binarización de la imagen, la relacionada con la inclinación del eje del huevo con respecto al plano de la fotografía y la variabilidad dada por la ausencia de simetría radial en la forma de los huevos. Los dos últimos factores son los que explican las diferencias de variabilidad o precisión entre las mediciones de los diámetros mayor y menor.

Todos los análisis 2D se apoyan en la premisa de que el plano de simetría es constante con la rotación alrededor del eje longitudinal (Deeming y Ruta, 2014).

Esto puede estar incorrecto, ya que no se tienen en cuenta las pequeñas variaciones en las curvaturas alrededor de las cáscaras completas; existen ejemplos de variaciones extremas en la simetría radial que se han descrito en algunas especies (Birkhead, 2016). El diámetro mayor tiende a estar menos afectado por las asimetrías radiales, que afectan más a las medidas transversales al eje longitudinal del huevo. Sin embargo, ambos diámetros se ven igualmente afectados por la inclinación del huevo en el momento de tomar las fotografías. Los errores en ambas medidas lineales se reflejan en la estimación del volumen, por su naturaleza cúbica.

De los tres métodos utilizados para estimar el volumen, el más preciso fue el algoritmo que tenía en cuenta el carácter discreto de los píxeles de las imágenes y que contaba el número de vóxeles en todas las secciones transversales a lo largo del eje mayor. El volumen obtenido manualmente por rellenado del interior de las cáscaras vacías para la validación no es estrictamente análogo al calculado a partir de las fotografías, ya que en estas se emplea la superficie exterior del huevo, mientras que el vaciado excluye la cáscara y posibles restos de membranas internas, que aunque son delgadas en relación con las dimensiones externas de los huevos, no se deben pasar por alto totalmente. La estimación a partir de los diámetros es más semejante en términos teóricos, y Bridge et al. (2007) la emplean para validar un método automatizado similar al presentado en este trabajo en huevos de Turdus migratorius. Para ello, emplean un programa libre GraphicConverter en combinación con Applescript, un componente del sistema operativo Macintosh. Estos autores validan su procedimiento derivado de las imágenes con los volúmenes obtenidos con la ecuación de Hoyt (1979) con un coeficiente de forma específico para la especie analizada (0,504). No usan huevos reales para validar el sistema aduciendo que no tenían medios para estimar el volumen que fueran más precisos que el sistema fotográfico.

Las estimaciones de las dimensiones externas de los huevos mostraron que el algoritmo es capaz de hacer estimaciones con menos de un 5 % de error.

En cinco huevos, el 15 % de la muestra, el cálculo del volumen tuvo un error medio superior (7,1 %),

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y = x

59 57 55

R2 = 0,8623

53 51 51 53 55 57 59 61 Diámetro mayor (mm) (posición natural)

49 48

Diferencia media 0,2 ± 0,6 mm y = x (0,50 %)

47 46 45 44 R2 = 0,8916

43 42

8 Diferencia entre estimados de volumen (cm3)

Diferencia media 0,4 ± 0,8 mm (0,85 %)

Diámetro menor (mm) (foto coplanar)

Diámetro mayor (mm) (foto coplanar)

61

39

6 4 2

0 3 –2

5

7

9

Promedio 0,65 ± 2,6 (1,48 %)

11

–4

41

40 40 45 Diámetro menor (mm) (posición natural)

–6

Ángulo de inclinación natural del huevo (grados)

Fig. 6. Efecto del ángulo de inclinación del huevo en las medidas principales tomadas a partir de las fotografías por medio del programa OvometriK. Fig. 6. Effect of the inclination angle of the egg on main measurements estimated from pictures with OvometriK software.

con desviaciones máximas de entre 7 y 8 cm3. La repetibilidad de las mediciones de los huevos es relativamente alta, aunque en las medidas tomadas a partir de fotografías tiende a disminuir ligeramente al aumentar la variabilidad de las medidas repetidas (fotos diferentes de los mismos huevos), posiblemente por los componentes de varianza asociados a la toma

de fotos (iluminación, contraste, ángulo y distancia) y al proceso de binarización. En las mediciones manuales, el coeficiente de variación entre medidas tomadas de manera repetida sobre los mismos huevos es menor del 1 % y es ligeramente superior en el diámetro menor por efecto de las asimetrías radiales.

La variabilidad de las mediciones fue ligeramente

Variables estimadas

Volumen (vóxeles) Volumen (Hoyt) Volumen (Mat) Diámetro mayor Diámetro menor Área superficial 0,0

–0,5

–1,0 –1,5 –2,0 –2,5 Diferencia porcentual

–3,0

–3,5

Fig. 7. Diferencia porcentual entre las estimaciones de las principales medidas tomadas a partir de fotografías de baja y alta resolución, por medio del programa OvometriK (diferencia = estimación a partir de foto de mayor resolución – estimación a partir de foto de menor resolución).

Fig. 7. Percentage of difference between estimates of the main measures obtained from pictures of eggs at low and high resolution, with OvometriK software (difference = estimation in higher resolution pictures – estimation in lower resolution pictures).

Ramírez–Arrieta et al.

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Tabla 1. Comparación entre las estimaciones de las dimensiones y los índices de formas que OvometriK extrae a partir de fotografías digitales de alta resolución, de baja resolución y con corrección manual del ángulo de inclinación de los huevos para hacerlos coplanares con la imagen. Para cada variable se muestran la media con su desviación estándar y los límites de confianza al 95 %.

Table 1. Comparison between dimension estimates and shape indexes that OvometriK extracts from digital egg pictures at high resolution, low resolution, and using manual correction of egg inclination angle for coplanarity with image plane. For each variable, mean with standard deviation and 95 % confidence limits are presented.

Variables

Normales (n = 195)

Fotos

Baja resolución Con ángulos coplanares (n = 27) (n = 54)

Diámetro mayor (mm)

58,21 ± 2,87

(57,81–58,62) (56,14–57,76) (55,58–57,16)

Diámetro menor (mm)

44,08 ± 2,03

(43,79–44,36) (42,4–43,5) (42,15–43,21)

Asimetría áreas

0,94 ± 0,02

56,95 ± 2,04 42,95 ± 1,4 0,93 ± 0,02

56,37 ± 2 42,68 ± 1,33 0,94 ± 0,01

(mitad superior / mitad inferior)

(0,93–0,94)

(0,93–0,94)

(0,93–0,94)

Excentricidad

0,01 ± 0,005

0,008 ± 0,003

0,007 ± 0,002

(distancia centroide–centro)

(0,009–0,01)

(0,007–0,009)

(0,006–0,008)

Índice de forma

0,77 ± 0,01

0,78 ± 0

0,76 ± 0

(área / rectángulo externo mín.)

(0,77–0,77)

(0,77–0,78)

(0,76–0,76)

Ancho en percentil 1 (mm)

39,28 ± 1,74

38,41 ± 1,07

38,02 ± 1,03

(39,04–39,53) (37,98–38,83) (37,61–38,42)

Ancho en percentil 2 (mm)

43,78 ± 2,02

(43,5–44,07) (42,2–43,31) (41,75–42,84)

Ancho en percentil 3 (mm)

36,13 ± 3,1

42,76 ± 1,41 35,42 ± 1,24

42,3 ± 1,38 32,55 ± 9,33

(35,7–36,57) (34,93–35,91) (28,86–36,24)

Área superficial (cm2)

80,61 ± 7,76

75,89 ± 3,97

75,97 ± 3,95

(79,51–81,7) (74,32–77,46) (74,41–77,53)

Volumen (cm3)

57,82 ± 7,43

53,99 ± 4,24

52,24 ± 4,1

(conteo de vóxeles)

(56,77–58,87)

(52,32–55,67)

(50,62–53,86)

superior en las estimaciones fotográficas, pero la diferencia se puede explicar por la ausencia de simetría radial y las variaciones locales en la superficie del huevo. La ausencia de marcadas diferencias entre las estimaciones manuales y las obtenidas a partir de las fotografías, unido al notable ahorro de tiempo y esfuerzo, hacen que este método sea una variante atractiva cuando hay que procesar gran cantidad de muestras, aunque sea mucho más confiable para estimar las dimensiones lineales que para calcular el volumen o la superficie, que en sus algoritmos supone la existencia de simetría radial.

El empleo de las fotografías para obtener perfiles 2D suele dar un error asociado al alineamiento de las cámaras con el plano paralelo al eje del huevo (Troscianko, 2014), ya que el centro de gravedad de los huevos está desplazado hacia el extremo mayor, lo que produce que el huevo se incline sobre una superficie plana (Mao et al., 2007). Este error

potencial se incrementa con el grado de asimetría del huevo y en muchos casos ni siquiera se trata de corregirlo (Stoddard et al., 2017). En el caso de los huevos empleados como prueba, la inclinación no afectó de manera significativa a las estimaciones de las dimensiones, lo cual no implica que en huevos de formas más aguzadas y, por tanto, con mayores ángulos de inclinación, no pueda llegar a ser un sesgo significativo. Para que las siluetas sean una representación precisa de la forma del huevo, se recomienda asegurarse de que las fotografías estén bien alineadas (Attard et al., 2017) y sean coplanares al plano central del huevo, aunque siempre puede haber un error. Una solución práctica podría ser tomar las fotos sobre una superficie esponjosa o con una concavidad, que permita colocar el huevo de manera óptima en un plano perpendicular a la cámara sin que se mueva.

En el protocolo se incluyen varios índices relacionados con la forma de los huevos, ya que su estudio

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más allá de la simple descripción de las dimensiones, ha demostrado su valor en la comprensión de las estrategias reproductivas de las aves. La forma del huevo influye en su solidez estructural (Gosler et al.

2005), en el crecimiento del embrión (Deeming, 2017), en la eficiencia de incubación (Mao et al., 2007), en la inversión materna de calcio (Gosler et al., 2005), en el intercambio de gases y en muchos otros factores que se relacionan con el éxito del pichón (Briskie y Sealy, 1990).

Tradicionalmente, la forma de los huevos se ha estudiado a partir de índices derivados de distancias lineales (Preston, 1969; Narushin, 2001, 2005; Havlíček et al., 2008; Troscianko, 2014) que, a pesar de sus limitaciones, continúan siendo muy usados y es por ello que se incluyen en el algoritmo de OvometriK. Estos índices están generalmente correlacionados entre sí y con las dimensiones, lo que dificulta la evaluación precisa de las variaciones entre muestras y dificultan la selección de las mejores variables (Narushin, 2001).

En los estudios publicados en inglés sobre morfometría se diferencian los conceptos "form" y "shape" (que no existe en español). El primer término se define como la combinación de información sobre formas y tamaños, mientras que el segundo se refiere exclusivamente a la información espacial de un objeto, que es la que queda luego de eliminar los efectos de la ubicación, la escala o las dimensiones y la rotación (Adams et al., 2013). Los índices más empleados para describir los huevos son la elongación y la asimetría. La elongación se refiere al grado de diferencia de la elipse con el círculo (coeficiente entre diámetros mayor y menor) y la asimetría se refiere a las diferencias entre los dos extremos del huevo (Deeming y Ruta, 2014).

En la actualidad, se han comenzado a explorar otras vías para el estudio de la forma de los huevos, como los descriptores elípticos de Fourier (Denis, 2014), que también se incluyen en el programa OvometriK. Attard et al. (2018) proponen un nuevo método para cuantificar los patrones de variación entre los huevos utilizando puntos clave tridimensionales sobre modelos obtenidos por tomografía computarizada, lo cual elimina los errores inherentes a la proyección de un objeto tridimensional curvado sobre un espacio 2D y permite evitar las posibles correlaciones cuando se combinan varios descriptores de la forma. Sin embargo, el equipo necesario para hacer estas reconstrucciones digitales es todavía muy caro para la mayoría de los investigadores y los métodos fotogramétricos más asequibles no funcionan con precisión en estas formas tan suavizadas y sin puntos de referencia para alinear las fotografías.

La plataforma R es en la actualidad uno de los programas de preferencia en los estudios sobre ecología por ser libre, versátil y aplicable a diversas situaciones analíticas. El trabajo colaborativo de la comunidad de usuarios ha permitido mantener y enriquecer de forma constante los repositorios de paquetes y códigos para numerosos tipos de análisis. Esta aplicación supera algunas de las limitaciones de plataforma, accesibilidad y número de variables incluidas en los productos desarrollados previamente con este propósito, además de que su carácter abierto y flexible

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permite adaptarla a otras aplicaciones específicas.

Los próximos pasos deben estar relacionados con su validación sobre otros tipos de huevos, de formas más asimétricas y con distintos patrones de manchados que pudieran interferir en la calidad de la identificación del contorno.

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The impacts of domestic dogs (Canis familiaris) on wildlife in two Brazilian hotspots and implications for conservation J. J. M. Guedes, C. L. Assis, R. N. Feio, F. M. Quintela Guedes, J. J. M., Assis, C. L., Feio, R. N., Quintela, F. M., 2021. The impacts of domestic dogs (Canis familiaris) on wildlife in two Brazilian hotspots and implications for conservation. Animal Biodiversity and Conservation, 44.1: 45–58, Doi: https://doi.org/10.32800/abc.2021.44.0045 Abstract The impacts of domestic dogs (Canis familiaris) on wildlife in two Brazilian hotspots and implications for conservation.

Exotic species are major threats to biodiversity worldwide. Domestic dogs (Canis familiaris) are among the most common invasive predators in the world, interacting with wildlife in many ways. We present ecological data based on camera traps and occasional observations of free–roaming domestic dogs from localities within the Brazilian Atlantic forest and Cerrado hotspots. Canis familiaris was the second most abundant mammal species, and the most abundant carnivore. Dogs chased, killed, and/or competed with at least 26 native species. They consumed none of the killed animals, which together with the predominant records of solitary individuals acting during the daytime indicates they are mainly free–roaming dogs relying on humans for food and shelter. The high numbers of dogs and the wide range of prey suggest wildlife could be greatly impacted by domestic dogs, especially in areas that are highly threatened by anthropogenic activities, such as biodiversity hotspots. We highlight possible measures (such as the eradication or removal of dogs from natural areas) that could help to reduce the environmental damage caused by domestic dogs in the region.

Key words: Conservation biology, Biological invasion, Exotic species, Atlantic forest, Cerrado Resumen Efectos de los perros domésticos (Canis familiaris) en la vida silvestre en dos puntos críticos del Brasil e implicaciones para la conservación. Las especies exóticas son una de las principales amenazas para la biodiversidad en todo el mundo. Los perros domésticos (Canis familiaris) se encuentran entre los depredadores invasores más comunes del mundo, ya que interactúan con la vida silvestre de muchas maneras. Presentamos datos ecológicos obtenidos mediante cámaras de trampeo y observaciones ocasionales de perros domésticos criados en libertad de localidades situadas dentro de los puntos críticos del bosque atlántico y el Cerrado brasileños. Canis familiaris fue la segunda especie de mamífero más abundante y el carnívoro más abundante. Los perros interactuaron con al menos 26 especies nativas persiguiéndolas, matándolas o compitiendo con ellas. No consumieron ninguno de los animales muertos, lo que, junto con los registros predominantes de individuos solitarios en actividad diurna, indica que se trata principalmente de perros criados en libertad que dependen de los humanos para alimentarse y refugiarse. La elevada abundancia de perros y la gran variedad de presas sugieren que la vida silvestre podría verse muy afectada por los perros domésticos, especialmente en zonas muy amenazadas por actividades humanas, como los puntos críticos de biodiversidad. Destacamos algunas medidas (por ejemplo, la erradicación o eliminación de perros de áreas naturales) que representan una posibilidad de reducir los daños ambientales causados por perros domésticos en la región.

Palabras clave: Biología de la conservación, Invasión biológica, Especies exóticas, Bosque atlántico, Cerrado Received: 19 V 20; Conditional acceptance: 21 VII 20; Final acceptance: 22 IX 20 Jhonny José Magalhães Guedes, Programa de Pós–Graduação em Ecologia e Evolução, Departamento de Ecologia, Universidade Federal de Goiás, Campus Samambaia, 74690–900 Goiânia, GO, Brazil.– Jhonny José Magalhães Guedes, Clodoaldo Lopes de Assis, Renato Neves Feio, Departamento de Biologia Animal, Museu de Zoologia João Moojen, Universidade Federal de Viçosa, 36570–075 Viçosa, MG, Brazil.– Fernando Marques Quintela, Taxa Mundi Institute, Lagoa Santa, MG, Brazil.

Corresponding author: J. J. M. Guedes. E–mail: jhonnyguds@gmail.com ORCID ID: 0000-0003-0485-3994 ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

Guedes et al.

46

Introduction The Earth's biota has been severely impacted by anthropogenic activities, leading to population declines and species loss at a global scale (Barnosky et al., 2011; Dirzo et al., 2014). Among the many causes threatening wildlife, the introduction and dispersal of exotic species is a major threat, being of great concern to many conservationists (Gurevitch and Padilla, 2004; Macdonald et al., 2007). In general, the negative impact of exotic species does not only affect native species but can also affect whole communities and ecosystem structures (Sakai et al., 2001).

Although there are thousands of exotic species worldwide, invasive mammalian predators are likely those that cause most damage to biodiversity (Bellard et al., 2016; Doherty et al., 2016, 2017). For instance, invasive predators are directly related to the extinction of more than a hundred vertebrate taxa (Doherty et al., 2016). Among invasive predators, dogs (C. familiaris) and cats (Felis catus) are surely the most common, the most numerous and the most widespread (Butler et al., 2004; Ferreira et al., 2011). Currently, the global domestic dog population is about 700 million to 1 billion individuals (Hughes and Macdonald, 2013; Gompper, 2014). Dogs have been living in close proximity with humans since their domestication around 15,000–30,000 years ago (Savolainen et al., 2002; Gompper, 2014). When they escape, when they are abandoned, or when they are allowed by their owners to roam, they may become 'free–roaming' animals, relying on human communities for food and shelter, or become feral dogs, living in the wild without any contact with humans at all (Boitani and Ciucci, 1995; Young et al., 2011; Hughes and Macdonald, 2013).

Free–roaming and feral dogs can pose problems of many types. They can harm wildlife and natural environments, and endanger human welfare through the transmission of contagious diseases (Schloegel and Daszak, 2005). They may become predators and compete with other species for resources such as food and shelter (Young et al., 2011), and they may even hybridize with other canids (Vilà and Wayne, 1999). Furthermore, the costs involved in controlling free–roaming dog populations, in livestock kills, and in medical treatments for dog bites cannot be overlooked (Pimentel et al., 2000; Bergman et al., 2009). Domestic dogs have contributed to the global extinction of at least 11 vertebrate species, and free–ranging dogs have had some impact on a further 188 species worldwide (Doherty et al., 2017).

Species with limited defense capability, such as the Galapagos marine iguanas (Amblyrhynchus cristatus) or the New Zealand kiwi (genus Apteryx), have undergone population declines due to predation by a relatively small number of domestic dogs (Kruuk and Snell, 1981; Taborsky, 1988). In Tanzania, eastern Africa, an outbreak of rabies and canine distemper caused the death and apparent local extinction of African wild dogs (Lycaon pictus), and the mortality of 30 % of lions (Panthera leo) in Serengeti National Park (Cleaveland et al., 2007). In Brazil, domestic dogs might have contributed to the population decline of

the bush dog (Speothos venaticus) at Brasília National Park. In the same area, the maned wolf (Chrysocyon brachyurus) was recorded more frequently in sites without the presence of dogs (Lacerda et al., 2009; Lessa et al., 2016).

The total population of free–roaming domestic dogs in Brazil is about 25 million individuals (Campos et al., 2007). Free–roaming and feral dogs are commonly recorded in both protected and unprotected areas of high conservation relevance in the country (Galetti and Sazima, 2006; Lessa et al., 2016; Allemand et al., 2019). Their presence in natural areas can be particularly damaging if areas are embedded in hotspots for biodiversity conservation –areas with high species richness and endemism, but highly threatened by human activities (Myers et al., 2000)– such as the Atlantic forest and Cerrado ecoregions in Brazil. At least 35 species have already been reported as prey of domestic dogs in these ecoregions across seven Brazilian states (e.g., Galetti and Sazima, 2006; Campos et al., 2007; Lacerda et al., 2009; Lessa et al., 2016). Even highly fragmented and unprotected areas in these hotspots may harbor significant components of native fauna, possessing endemic, endangered, and even undescribed species (Lion et al., 2016; Barbosa et al., 2017; Avigliano et al., 2019). The damage caused by free–roaming dogs on wildlife are still little understood and even neglected, especially in South America countries (Lessa et al., 2016). Therefore, more studies are necessary to improve our current understanding of the real consequences of such interactions (Galetti and Sazima, 2006; Young et al., 2011; Hughes and Macdonald, 2013). Here we present novel records of the interaction between domestic dogs and wildlife together with data on the occurrence and abundance of both domestic dogs and native species in natural environments from the Atlantic forest and Cerrado hotspots in southeastern Brazil. We also discuss potential ecological consequences of such interactions on wildlife and associated ecosystems, and provide some guidelines for decision makers to mitigate those problems in the region.

Material and methods The study area was composed of 10 municipalities in the state of Minas Gerais, southeastern Brazil (fig. 1). These localities comprise unprotected forest fragments located in subtropical moist broadleaf forests and subtropical savanna ecoregions (Dinerstein et al., 2017) (hereafter Atlantic forest and Cerrado, respectively), and also an ecotone (transition) area between these two ecoregions (table 1). The Atlantic forest is currently reduced to about 12 % of its original cover. Most forest fragments are small (< 50 ha) and located near populated areas (Ribeiro et al., 2011). The Cerrado has also gone through a severe deforestation process over the last decades, with its original area now reduced to about 22 % (IBGE, 2019).

Overall, the matrices (surroundings) of the forest fragments in the study area are composed mainly of pasture and crop plantations. Although these forest

Animal Biodiversity and Conservation 44.1 (2021)

45º 46' 40" W

47

43º 40' 50" W

41º 35' 0" W

3

4

5

Espirito Santo

10

6 9 7 8

Rio de Janeiro

N

0

70 km

São Paulo

140

22º 53' 20" S

Minas Gerais

20º 47' 30" S

18º 41' 40" S

2

1

Biomes T / S–mb T / S–s Sampling methods Occasional encounters Occasional encounters and camera trap Camera trap

24º 59' 10" S

Brasil

Fig. 1. Municipalities where the study was conducted in the state of Minas Gerais: 1, Presidente Olegário; 2, São Gonçalo do Abaeté; 3, Olhos D'água; 4, Santa Bárbara do Leste; 5, Viçosa; 6, Ubá; 7, Astolfo Dutra; 8, Cataguases; 9, Miraí; 10, São Francisco do Glória. The inset map shows the Brazilian federative units, highlighting the state of Minas Gerais in grey. Biomes: T / S–mb, tropical and subtropical moist broadleaf forests; T / S–s, tropical and subtropical grasslands, savannas and shrublands.

Fig. 1. Municipios del estado de Minas Gerais donde se realizó el estudio: 1, Presidente Olegário; 2, São Gonçalo do Abaeté; 3, Olhos D'água; 4, Santa Bárbara do Leste; 5, Viçosa; 6, Ubá; 7, Astolfo Dutra; 8, Cataguases; 9, Miraí; 10, São Francisco do Glória. En el mapa ampliado se observan las unidades federativas brasileñas y se destaca el estado de Minas Gerais en gris. Biomas: T / S–mb, bosques húmedos tropicales y subtropicales; T / S–s, pastizales, sabanas y matorrales tropicales y subtropicales.

remnants are small and severely threatened by human activities, they are still relevant to the conservation of biodiversity because they harbor many endemic and endangered species (Faria et al., 2009; Moraes et al., 2015; Guedes et al., 2017; Laurindo et al., 2019).

To investigate the ecological interactions between dogs and wild animals, we first classified these

interactions into: (i) predation, (ii) chasing, and (iii) competition. We considered interactions as predation when dogs injured or killed other animals; chasing when other species were disturbed by dogs, but without physical engagement between them; and competition (i.e., for space and food) when dogs co–occurred (found in the same site) with native

Guedes et al.

48

carnivores (Hughes and Macdonald, 2013; Lessa et al., 2016). Interactions were recorded through opportunistic encounters (OE) and camera trap (CT) data.

Opportunistic encounters were obtained from seven municipalities during 2008 and 2020 (table 1) by two researchers during fieldwork to assess environmental impact, and represent sporadic, occasional, anecdotal records. When domestic dogs were observed interacting with wild animals, observers remained in place until the end of the interaction. Despite the long period involved in assessing the environmental impact in both ecoregions, we only obtained occasional records were obtained in areas of the Atlantic forest biome. Data of CTs obtained from 2014 to 2016 was also used to analyze ecological interactions between domestic dogs and native species and to estimate abundance for mammal species in the study area. These data were obtained from 23 sampling sites distributed across four municipalities (table 1). We used the number of records as a proxy for abundance, but it is worth mentioning that this does not correspond exactly to the number of individuals because sometimes one photograph can include more than one individual. Camera traps were installed on tree trunks at heights of 40–50 cm above the forest floor, all in areas of native vegetation; in other words, CTs were not installed in areas of eucalyptus (exotic) plantations. The distance between cameras (considering the closest one) at each site ranged from 0.7 to 14.8 km.

We used meat, fruits, and maize as bait, aiming to increase detection and to provide better estimates of abundance for the recorded species. We acknowledge that these baits may not cover the diet of all mammals occurring in the study area and could therefore bias our abundance estimates, but because most species are naturally rare (Preston, 1948), random detection would likely be too low without using baits. In all sampling sites, camera traps remained active for at least 67 days, had infrared sensors to detect movement and temperature variation, and were programmed to shoot at 10–second intervals between shots. The sampling effort in each study site was calculated as: 24h/trapping * nº of camera traps * nº of sampling period in days (see table 1).

Whenever possible, dogs were identified through aspects of pelage color, sex, size and any other characteristics that could be useful for individual distinction (fig. 2). For abundance estimates, individuals from the same species were counted only for a given sampling site when records were obtained over periods of more than 24 hours. We chose this conservative approach to avoid counting the same specimen of a given species more than once when it wanders around the same CT multiple times in the same day, which could inflate abundance estimates.

We used a non–parametric Kruskal–Wallis rank sum test to investigate whether there were differences in mean mammal abundance between ecoregions.

Using Pearson's x2–test we also tested if the number of records of domestic dogs, carnivores, and other mammals was dependent of the ecoregion. Analysis was performed using the statistical software R version 3.3.3 (R Core Team, 2017). The period of activity of

domestic dogs was obtained through time stamps of camera shots, and was classified into diurnal (active from 6 to 18 h) or nocturnal (active from 18 to 6 h), which roughly represent day/night time in southeastern Brazil during most of the year. Information on ecological aspects and geographic distribution of native mammal species follows Paglia et al. (2012).

The status of conservation of native mammal species at national and global levels follows ICMBio (2018) and IUCN (2020), respectively.

Results In seven municipalities we recorded a total of 79 individuals belonging to 25 native species that were killed or chased or were potentially competing for resources with domestic dogs in the study area (one bird, two lizards, and 22 mammals; table 2). Of 13 species killed by domestic dogs, three (Tropidurus torquatus, Cerdocyon thous and Nectomys squamipes) are recorded as being preyed upon by dogs for the first time. Species directly interacting with dogs varied greatly in body size, including small–sized animals such as the eastern collared spiny lizard Tropidurus torquatus (Teixeira and Giovanelli, 1999) and large mammals such as the capybara Hydrochoerus hydrochaeris (Paglia et al., 2012). The dogs consumed none of the animals they killed, and the attacks persisted until the prey stopped moving.

The total sampling effort of CTs was 65,520 hours (mean = 16,380 hours/city). Overall, we obtained 649 records of 31 mammal species (27 natives and four exotics) across four municipalities (fig. 3). More than half of these records were from the Atlantic forest (51.3 %), which also had higher average mammal abundance (mean = 19.6 ± 40, range: 1–162, n = 17). The Cerrado accounted for 40.2 % of the total abundance (mean = 10.9 ± 12.8, range: 1–45, n = 24), followed by the ecotone area with 8.4 % (mean = 5.5 ± 4.5, range: 5–13, n = 10). Although the differences in mean mammal abundance were not statistically significant among ecoregions (Kruskal–Wallis x2 = 0.501, df = 2, p = 0.778), the number of records of domestic dogs, carnivores, and other mammals was highly dependent on the biome in which they occurred (x2–test = 43.715, df = 4, p < 0.001). Considering all records, the black– eared opossum Didelphis aurita (24.96 %) was the most common species, followed by domestic dogs (14.18 %) and the tapeti Sylvilagus brasiliensis (7.7 %).

The number of records of domestic dogs varied among ecoregions, where most dogs were recorded in the Atlantic forest (n = 55; 59.7 %), followed by the Cerrado (n = 24; 26 %) and the transition area (n = 13; 14.3 %). Among species of the order Carnivora, Canis familiaris was the most common, followed by the South American coati Nasua nasua (3,24 %), the maned wolf Chrysocyon brachyurus (3.08%), the crab–eating fox Cerdocyon thous (2.62 %), the tayra Eira barbara (2 %), the striped hog–nosed skunk Conepatus amazonicus (0.92 %), the ocelot Leopardus pardalis (0.62 %), the cougar P. concolor (0.62 %), Felis catus (0.46 %), the crab–eating raccoon

Animal Biodiversity and Conservation 44.1 (2021)

49

Table 1. Detailed information about the methods used in each municipality in the state of Minas Gerais, southeastern Brazil: N, number of sites/city; T, total sampling effort. Biome: AF, Atlantic forest; Ce, Cerrado; Ec, ecotone. Sampling methods (SM): OE, occasional encounter; CT, camera–trap; * occasional encounters in Cataguases in 2010–2011, 2013–2015, and 2017–2018.

Tabla 1. Información detallada sobre la metodología utilizada en cada municipio del estado de Minas Gerais, en el sureste del Brasil: N, número de sitios/ciudad; T, esfuerzo de muestreo total. Bioma: AF, bosque Atlántico; Ce, Cerrado; Ec, ecotono. Métodos de muestreo (SM): OE, observación ocasional; CT, cámara de trampeo; * observaciones ocasionales en Cataguases ocurridos en los años de 2010–2011, 2013–2015 y 2017–2018.

Municipality

Coordinates

SM

Period

N

T

Biome

Astolfo Dutra

21º 18' 29'' S

OE

2009

–

–

AF

42º 51' 41'' W

Miraí

21º 09' 03'' S

OE

2008–2009

–

–

AF

42º 37' 06" W

Santa Bárbara do Leste

19º 58' 32'' S

OE

2015

–

–

AF

42º 08' 45'' W

São Francisco do Glória

20º 47' 31" S

OE

2020

–

–

AF

42º 16' 58" W

Ubá

21º 07' 15'' S

OE

2013

–

–

AF

42º 56' 11'' W

Viçosa

20º 45' 17'' S

OE

2015–2016

–

–

AF

42º 52' 42'' W

Cataguases *

21º 22' 31'' S

CT, OE

VI 2015

2

20,160 h

AF

42º 41' 08'' W

Olhos D'água

17º 23' 45'' S

5

10,800 h

Ec

43º 34' 11'' W

Presidente Olegário

18º 24' 56'' S

8

23,040 h

Ce

46º 25' 05'' W

São Gonçalo do Abaeté

18º 20' 29'' S

8

11,520 h

Ce

45º 49' 57'' W

CT CT CT

Procyon cancrivorus (0.46 %), the jaguarundi Puma yagouaroundi (0.15 %), and the southern tiger cat Leopardus guttulus (0.15 %).

Most domestic dogs were recorded in diurnal activity (n = 74; 80.4 %) but some individuals were also found at night (n = 18; 19.6%). On most occasions, domestic dogs were solitary (n = 66; 71.7 %), but we also recorded groups of two to four individuals (n = 26; 28.3 %). Although we did not measure any specimen, body sizes (estimated based on photographs) varied from small to large, but most individuals were medium–sized.

The great majority of native mammals occur both in the Atlantic forest and Cerrado biomes, except for Didelphis aurita and the black capuchin Sapajus nigritus, which are considered endemic to the Atlantic forest (Paglia et al., 2012). Although the black capuchin Sapajus nigritus is considered endemic to this ecoregion,

to VIII 2016 III 2014

to V 2014 VII 2016 to X 2016 IV 2016 to V 2016

we also observed this species in a Cerrado area. Half the species recorded have terrestrial habits, and only a few are scansorial ('climber') (16.6 %), semifossorial (can live above– and below–ground) (13.3 %), arboreal (13.3 %) or semiaquatic (can live partly on land and partly in water) (6.6 %). More than two thirds of mammals recorded in the study area are nocturnal, with only 20 % being diurnal, and 13.3 % being active both day and night. Regarding their conservation status, three species are considered vulnerable (the giant Anteater Myrmecophaga tridactyla, the giant armadillo Priodontes maximus and the oncilla Leopardus guttulus) and two are considered near threatened (Chrysocyon brachyurus and Sapajus nigritus) at a global level (IUCN, 2020). Nationally, six species are considered vulnerable (C. brachyurus, L. guttulus, Puma concolor, P. yagouaroundi, M. tridactyla, and P. maximus) (table 3).

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50

Table 2. Recorded species competing, chased, and/or killed by domestic dogs in seven municipalities in the state of Minas Gerais, Brazil: N, number of specimens. Impact type (IT): Ch, chasing; P, predation; C, competition. Municipality of record: AST, Astolfo Dutra; CAT, Cataguases; MIR, Miraí; ODA, Olhos D’água; SBL, Santa Bárbara do Leste; SFG, São Francisco do Glória; SGA, São Gonçalo do Abaeté; PRE, Presidente Olegário; UBA, Ubá; VIC, Viçosa.

Tabla 2. Especies registradas compitiendo, perseguidas o matadas por perros domésticos en siete municipios del estado de Minas Gerais, en Brasil: N, número de especímenes. Tipo de impacto (IT): Ch, persecución; P, depredación; C, competencia. Municipios de registro: AST, Astolfo Dutra; CAT, Cataguases; MIR, Miraí; ODA, Olhos D’água; SBL, Santa Bárbara do Leste; SFG, São Francisco do Glória; SGA, São Gonçalo do Abaeté; PRE, Presidente Olegário; UBA, Ubá; VIC, Viçosa.

Species

N

Common name

Callithrix penicillata

1

Black–pencilled marmoset

Cerdocyon thous

15

Crab–eating fox

Municipality of record

IT

CAT

Ch

UBA, PRE, ODA,

P, C

Mammalia

SGA, CAT

Chrysocyon brachyurus

9

Maned wolf

Conepatus amazonicus

2

Striped hog–nosed skunk

CAT, PRE, SGA, ODA

C

SGA

C

Cuniculus paca

1

Spotted paca

CAT, VIC

P

Dasypus novemcinctus

1

Nine–banded armadillo

CAT, MIR

Ch, P

Didelphis aurita

3

Brazilian common opossum

CAT

P

Eira barbara

1

Tayra

CAT, PRE

P

Hydrochoerus hydrochaeris 1 Capybara

VIC

Ch

Kannabateomys amblyonyx 1

Atlantic bamboo rat

CAT

Ch

Southern tiger cat

SGA

C

CAT

C

Leopardus guttulus

1

Leopardus pardalis

4 Ocelot

Mazama gouazoubira

1

Nasua nasua

20 South American coati

Red brocket

SBL

P

CAT, PRE, SGA

P, C

Nectomys squamipes

1

South American water rat

CAT

P

Philander frenatus

1

Southeastern four–eyed opossum

SFG

P

Procyon cancrivorus

3

Crab–eating raccoon

CAT, SFG

P, C

Puma concolor

4

Cougar

CAT, SGA

C

Puma yagouaroundi

2

Jaguarundi

MIR, CAT

Ch, C

Sphiggurus villosus

2

Orange–spined hairy dwarf porcupine CAT, VIC

Ch

Sylvilagus brasiliensis

1

Tepeti; forest rabbit

AST

P

Tamandua tetradactyla

1

Southern tamandua

CAT

Ch

1

Tataupa tinamou

CAT

Ch

Salvator merianae

1

Black–and–white tegu

CAT

P

Tropidurus torquatus

1

Eastern collared spiny lizard

CAT

P

Aves Crypturellus tataupa Squamata

Discussion In the present study, we found 13 species that were killed by domestic dogs, adding three novel

records (Tropidurus torquatus, Cerdocyon thous and Nectomys squamipes) to the growing list of native species killed by canines in the Atlantic forest and Cerrado ecoregions (Galetti and Sazima, 2006;

Animal Biodiversity and Conservation 44.1 (2021)

51

A B

C D

E F

Bushnell

27/07/2016

10:28:53

Bushnell

27/07/2016

11:09:04

Fig. 2. Records obtained from occasional encounters (A–D) and camera traps (E–F): A–D, Philander frenatus (A), Didelphis aurita (B), Cuniculus paca (C), and Mazama gouazoubira (D), all killed by domestic dogs in the municipalities of São Francisco do Glória, Cataguases, Viçosa, and Santa Bárbara do Leste, respectively; E–F, Dasyprocta azarae and a domestic dog recorded in the same locality, and near the same time, in the municipality of Presidente Olegário.

Fig. 2. Registros obtenidos de observaciones ocasionales (A–D) y con cámaras de trampeo (E–F): A–D, Philander frenatus (A), Didelphis aurita (B), Cuniculus paca (C) y Mazama gouazoubira (D), todos matados por perros domésticos en São Francisco do Glória, Cataguases, Viçosa y Santa Bárbara do Leste respectivamente; E–F, Dasyprocta azarae y un perro doméstico encontrados en la misma localidad y casi al mismo tiempo en Presidente Olegário.

52

Campos et al., 2007; Oliveira et al., 2008; Lacerda et al., 2009; Lessa et al., 2016; Pereira et al., 2019).

The diversity of animals killed, varying greatly in body size, indicates that free–roaming dogs are generalists regarding the prey they hunt and feed on (Galetti and Sazima, 2006; Campos et al., 2007; Pereira et al., 2019). Many other species, despite not being killed, were either chased or potentially competed with domestic dogs, which can also have negative effects on wildlife (Hughes and Macdonald, 2013; Doherty et al., 2017). Since the studied sites are embedded within two biodiversity hotspots (Myers et al., 2000), the native fauna in the state of Minas Gerais could be highly impacted by the additional pressure exerted by domestic dogs. It seems, too, that many species that are negatively affected by domestic dogs are also highly threatened by other impacts, such as habitat loss and illegal hunting (Lessa et al., 2016).

We highlight that terrestrial mammals (regardless of size) are more vulnerable to dog attacks than arboreal and aquatic mammal species, for example, as encounter rates are probably higher and chances of escape are lower. Similar results were found in other studies conducted in Brazil (Galetti and Sazima, 2006; Campos et al., 2007; Rangel et al., 2013; Pereira et al., 2019), and even in global assessments, terrestrial mammals are the group most impacted by interactions with domestic dogs (Hughes and Macdonald, 2013; Doherty et al., 2017). The fact that the dogs did not consume the animals they attacked suggests they are free–roaming –rather than feral dogs (Hughes and Macdonald, 2013)– in close relationship with human settlements where they may obtain food and shelter. This pattern of killing but not feeding upon their prey has been reported in other studies (Galetti and Sazima, 2006; Oliveira et al., 2008; Rangel et al., 2013; Pereira et al., 2019) where dogs may chase, capture, and eventually kill other species apparently for fun (Gompper, 2014). This could be explained by the close evolutionary relationship between dogs and wolves, and the 'predation instinct' preserved in dogs (Bradshaw, 2006). One aspect of concern related to this predatory behavior is that most remaining native vegetation in Brazil is currently highly fragmented, and small sized in the case of the Atlantic forest (Ribeiro et al., 2009). Combined with the proximity of these fragments to urban and rural areas, this environment creates a favorable scenario for invasion and dispersion of free–roaming dogs (Manor and Saltz, 2004; Torres and Prado, 2010; Paschoal et al., 2016; Allemand et al., 2019). We acknowledge, however, that human interference (presence during occasional encounters) could lead dogs to abandon their prey after killing it, thus biasing this result. Furthermore, dogs certainly feed upon many other specimens (especially small ones) that we could only know of through, for example, analysis of fecal samples (Campos et al., 2007; Nogales et al., 2013). Nonetheless, this only emphasizes that the predation events we observed might represent merely a small fraction of the real magnitude of the impact of dogs on wildlife, which in effect has been shown to be hugely underestimated (Doherty et al., 2017).

Guedes et al.

In our study, Canis familiaris was the second most abundant species out of 31 mammal taxa recorded by camera traps, and the most abundant carnivore.

Other studies have presented similar findings, where domestic dogs frequently stand out among the most abundant species in many natural areas in Brazil, affecting native species in several ways (Curi et al., 2006; Srbek–Araujo and Chiarello, 2008; Lacerda et al., 2009; Frigeri et al., 2014; Paschoal et al., 2016). In addition to the direct impact caused by injuries and death to other predators, such as the crab–eating fox (Cerdocyon thous) and the jaguarundi (Puma yagouaroundi), domestic dogs could also be indirectly affecting other carnivores through transmission of infectious diseases, for example (Young et al., 2011), or competition for space and food (Hughes and Macdonald, 2013; Lessa et al., 2016). The latter can be further aggravated when free–roaming dog abundances are high, since they can exert excessive predation pressure upon prey, considerably reducing their population size and their ability to recover, thus shrinking the availability of food for other predators (Young et al., 2011). Although it was not statically significant, the average and overall dog abundance in the Atlantic forest was high when compared to that in the ecotone and Cerrado areas. Variation in dog densities across regions are well known and depend mainly on human population densities (Gompper, 2014), which seems the main driver of the observed pattern since the Atlantic forest accounts for more than 40 % of the Brazilian population with more than 100 million people (da Fonseca, 1985; Morellato and Haddad, 2000).

Another interesting aspect is that most records showed dogs in diurnal activities mostly solitary. This is different from what is usually observed with feral dogs, which aggregate in groups of up to six individuals and are primarily active in nocturnal and crepuscular periods (Boitani and Ciucci, 1995). Coupled with other findings presented here (see above), this finding suggests that dogs observed in our sampled localities were likely free–roaming animals that retreat to nearby human habitations for shelter or food. The presence of free–roaming dogs rather than feral dogs is not surprising since more than 75 % of the world dog population are likely free–roaming individuals (Hughes and Macdonald, 2013). It is worth mentioning that most native mammals recorded in the study areas are nocturnal (see table 3), which could somewhat limit the negative impact of free–roaming dogs due to a mismatch of activity time. Moreover, as most dogs likely rely directly on humans to survive –at least partially– this consideration could provide an opportunity for the implementation of effective management actions to control the impact of dogs on wildlife.

The conservation status of most native mammals recorded herein in co–occurrence with domestic dogs is of least concern, and the majority of these species have wide geographic distribution (occurring in more than one biome; table 3). However, seven of these are included in threat categories at a national or global level. Considering that our study was conducted outside protected areas and the recorded native taxa also suffer from other impacts, such as habitat loss and

Animal Biodiversity and Conservation 44.1 (2021)

53

162

Abundance (# of records)

150

100

50

92

50

45 43 33 32

0

21 20

17

13 11

9

9

6

5

5

4

4

4

3

3

3

2

1

1

1

1

1

Didelphis aurita *Canis familiaris Sylvilagus brasiliensis Dasyporcta azarae Dasypus novemcinctus Didelphis albiventris Pecari tajacu Myrmecophaga tridactyla Mazama gouazoubira *Nasua nasua *Chrysocyon brachyurus *Cerdocyon thous *Eira barbara Tamandua tetradactyla Cabassous tatouay Euphractus Sexcinctus Conepatus amazonicus Cuniculus paca Philander frenatus Bos taurus *Leopardus pardalis *Puma concolor Equus caballus *Felis catus *Procyon cancrivorus Hydrochoerus hydrochaeris Didelphis albiventris *Leopardus guttulus Priodontes maximus *Puma yagouaroundi Sapajus nigritus

25 23

Fig. 3. Total number of records of mammals obtained from 2014 to 2016 by camera trapping in four municipalities of the state of Minas Gerais, southeastern Brazil (see table 1). Species are ordered in decreasing number of records; * species from the order Carnivora.

Fig. 3. Número total de registros de mamíferos obtenidos de 2014 a 2016 mediante cámaras de trampeo en cuatro municipios del estado de Minas Gerais, en el sureste del Brasil (véase la tabla 1). Las especies se ordenan por número decreciente de registros; * especies del orden Carnivora.

fragmentation (Chiarello, 1999), hunting (Cullen et al., 2001), and road kill (Cáceres et al., 2010), our results underline another concerning issue for the biological conservation in these areas. Although the magnitude of the impact of domestic dogs is still unclear (Doherty et al., 2017), it is evident that this invasive predator can add to the impact and risk of local extinctions of native species, particularly of other carnivores (Doherty et al., 2016, 2017; Lessa et al., 2016).

Even with the growing recognition and concern of the impact caused by domestic dogs on native species, management of the problem is a challenge for professionals working in wildlife conservation. The society, animal protection and welfare organizations,

and authorities or decision makers do not generally take the impact of this invasive predator on wildlife into account, and may be reluctant to take action to control dog populations, particularly due to their close association with humans (Dalla Villa et al., 2010; Hughes and Macdonald, 2013). For example, in the municipalities where predation events were recorded in this study, animal welfare organizations and the local people commonly organize campaigns to feed free–ranging dogs but are reluctant to manage dog populations such as their removal from streets, vaccinations, and long–term castration programs. These contrasting 'behaviors' could, eventually, have a negative effect on animal welfare. These organizations

Guedes et al.

54

Table 3. Distributional, ecological and conservation data of native mammals recorded through occasional encounters and camera trapping in the studied sites: Biomes: AF, Atlantic forest; AmF, Amazon forest; Ca, Caatinga; Ce, Cerrado; Pp, Pampa; Pt, Pantanal. Habitat: Ar, arboreal; Te, terrestrial; Sf, Semifossorial; Sc, Scansorial; Saq, Semiaquatic. Activity period: D, diurnal; N, nocturnal. Conservation status (CS): DD, data deficient; LC, least concern; NT, near threatened; VU, vulnerable.

Tabla 3. Datos ecológicos, de distribución y de conservación de mamíferos nativos registrados en observaciones ocasionales y con las cámaras de trampeo en los sitios estudiados. Biomas: AF, bosque atlántico; AmF, bosque amazónico; Ca, Caatinga; Ce, Cerrado; Pp, Pampa; Pt, pantanal. Hábitat: Ar, arbóreo; Te, terrestre; Sf, semifosorial; Sc, escansorial; Saq, semiacuático. Periodo de actividad: D, diurno; N, nocturno. Estado de conservación (CS): DD, datos insuficientes; LC, preocupación menor; NT, casi amenazado; VU, vulnerable.

Species

CS Biome

Habitat Activity IUCN Brazil

Cabassous tatouay

AF, Ce, Pp

Sf

N

LC

LC

Callithrix penicillata

AF, Ce, Ca

Ar

D

LC

LC

Cerdocyon thous Chrysocyon brachyurus

AF, Ce, Ca, Pt, Pp

Te

N

LC

LC

Ce, Pt, Pp

Te

N, D

NT

VU

Coendou spinosus

AF, Ce

Ar

N

LC

LC

Conepatus amazonicus

Ce, Ca

Te

N

LC

LC

Cuniculus paca Dasyprocta azarae Dasypus novemcinctus Didelphis albiventris Didelphis aurita Eira barbara

AmF, AF, Ce, Ca, Pt, Pp

Te

N

LC

LC

AF, Ce, Pt, Pp

Te

D

DD

LC

AmF, AF, Ce, Ca, Pt, Pp

Sf

N

LC

LC

Ce, Ca, Pt, Pp

Sc

N

LC

LC

AF AmF, AF, Ce, Ca, Pt

Sc N LC LC Te

D

LC

LC

Euphractus sexcinctus

AmF, AF, Ce, Ca, Pt, Pp

Sf

D

LC

LC

Hydrochoerus hydrochaeris

AmF, AF, Ce, Ca, Pt, Pp

Saq

N/D

LC

LC

AF, Ce

Ar

N

LC

LC

AmF, AF, Ce, Ca, Pt, Pp

Te

N

LC

LC

Kannabateomys amblyonyx Leopardus pardalis

AF, Ce

Te

N

VU

VU

AF, Ce, Pt, Pp

Te

N, D

DD

LC

Myrmecophaga tridactyla

AmF, AF, Ce, Ca, Pt, Pp

Te

N

VU

VU

Nasua nasua

AmF, AF, Ce, Ca, Pt, Pp

Te

D

LC

LC

Leopardus guttulus Mazama gouazoubira

Nectomys squamipes Pecari tajacu

AF, Ce

Saq

N

LC

LC

AmF, AF, Ce, Ca, Pt, Pp

Te

N, D

LC

LC

AF, Ce

Sc

N

LC

LC

AmF, AF, Ce, Pt

Sf

N

VU

VU

Procyon cancrivorus

AmF, AF, Ce, Ca, Pt, Pp

Sc

N

LC

LC

Puma concolor

AmF, AF, Ce, Ca, Pt, Pp

Te

N

LC

VU

Puma yagouaroundi

AmF, AF, Ce, Ca, Pt, Pp

Te

N

LC

VU

Ar

D NT NT

Philander frenatus Priodontes maximus

Sapajus nigritus

AF

Sylvilagus brasiliensis

AmF, AF, Ce, Ca, Pt, Pp

Te

N

LC

LC

Tamandua tetradactyla

AmF, AF, Ce, Ca, Pt, Pp

Sc

N

LC

LC

do not usually consider that by only providing food, and without any other control measures, they may be increasing dog abundance, potentiating negative impacts over wildlife (Newsome et al., 2015). Several

studies conducted in different countries have provided subsidies, management methods and/or guidelines to decision makers for the mitigation of problems caused by domestic dogs (Butler et al., 2004; Campos et al.,

Animal Biodiversity and Conservation 44.1 (2021)

2007; Hughes and Macdonald, 2013; Lessa et al., 2016; Doherty et al., 2017). Based on the Brazilian 'reality' (of a developing country and its limitations), we highlight some of the measures we believe would be most feasible to implement: (1) introduce regular removal of domestic dogs in natural areas, mainly from small forest fragments; (2) establish programs of environmental education informing local people –especially dog owners– about the direct and indirect impacts of free–ranging dogs on wildlife and ecosystems; (3) introduce the mandatory use of dog collars containing contact information with the owner (especially around priority areas for conservation), coupled with legal prohibition of abandonment; (4) carry out population control through euthanasia and/ or castration of abandoned individuals in urban and rural areas; and (5) create and maintain long–term vaccination programs of domestic dogs, and when necessary, of native species.

In conclusion, in this study we have shown some of the impacts domestic dogs have on wildlife in unprotected areas in two Brazilian biodiversity hotspots.

Due to a long history of human exploitation, these areas are currently small, highly fragmented, and mostly under no legal protection. Their native fauna are under constant threat from activities such as illegal logging, hunting –especially medium to large–sized mammals, and fires. The additional impact of domestic dogs can thus have severe consequences on wildlife, contributing, for example, to local extinctions. Although the growing literature has highlighted these negative impacts, management of this invasive predator can be complex, especially due to the dog's close historical relationship with humans –often referred to as "man's best friend". Interdisciplinary approaches combining both ecological and social views will be essential to overcome these problems, allowing us to safeguard wildlife from this particular threat.

Acknowledgements We thank Dendrus Projetos Ambientais e Florestais and VertAmbiental Consultoria, Projetos e Serviços for financial support; and José Lelis Pontes and Anderson de Almeida for providing information about dog predation. J. J. M. G. and C. L. A. thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for their scholarship. We are also grateful to Montserrat Ferrer and three anonymous reviewers for their valuable comments on previous version of this manuscript.

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Variation in winter thrush abundance during the hunting season in southern Europe: the importance of hunting–free reserves L. Goñi, S. González, E. Biescas, D. Villanúa, J. Arizaga

Goñi, L., González, S., Biescas, E., Villanúa, D., Arizaga, J., 2021. Variation in winter thrush abundance during the hunting season in southern Europe: the importance of hunting–free reserves. Animal Biodiversity and Conservation, 44.1: 59–66, Doi: https://doi.org/10.32800/abc.2021.44.0059 Abstract Variation in winter thrush abundance during the hunting season in southern Europe: the importance of hunting–free reserves. We analysed variations in the abundance of the song thrush (Turdus philomelos) and the blackbird (T. merula) in the hunting season in hunting areas and hunting–free reserves. After controlling for habitat, we found that the abundance of song thrushes (hunted species) was lower in hunting areas than in reserves during the hunting season. This effect was not found for the blackbird (non–hunted species). This finding indicates hunting–free reserves have a positive effect on song thrush conservation.

Further research is crucial to determine the traits that should be promoted in this type of reserve in order to improve their efficiency.

Key words: Avian conservation, Hunting, Game birds, Wildlife management Resumen Variación de la abundancia del zorzal en invierno durante la temporada de caza en el sur de Europa: la importancia de las reservas. Analizamos las variaciones de la abundancia del zorzal común (Turdus philomelos) y el mirlo (T. merula) durante la temporada de caza en reservas y en zonas de caza. Una vez controlado el efecto del hábitat, la abundancia del zorzal común (especie cinegética) fue inferior en las zonas de caza que en las reservas. Este efecto no se observó en el mirlo (especie no cinegética). Este resultado indica que las reservas de caza tienen un efecto positivo en la conservación del zorzal común.

Es fundamental seguir trabajando para determinar los factores que se deberían promover en este tipo de reservas para mejorar su eficiencia.

Palabras clave: Conservación de aves, Caza, Especies cinegéticas, Gestión de la fauna silvestre Received: 21 V 20; Conditional acceptance: 29 VI 20; Final acceptance: 30 IX 20 Lander Goñi, Sergio González, Diego Villanúa, Juan Arizaga, Departamento de Ornitología, Sociedad de Ciencias Aranzadi, Zorroagagaina 11, E–20014 Donostia–S. Sebastián, Spain.– Esther Biescas, IES Tierra Estella, Remontival 7, 31200 Estella, Spain.– Diego Villanúa, Gestión Ambiental de Navarra (GAN–NIK), Padre Adoain 219 bajo, 31015 Pamplona, Spain.

ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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Introduction Southern European states are the main wintering areas for large numbers of European breeding birds (Andreotti et al., 1999; Tellería et al., 1999), including species of thrush (Snow and Perrins, 1998; Rivalan et al., 2007). These southern states, therefore, have a high responsibility in the conservation of many European bird populations. Hunting activity and its associated management have obvious effects on the conservation of biodiversity, leading to controversy across several spatial scales and between different sectors of our society (McCulloch et al., 1992; Madsen, 1998a; Sokos et al., 2013; Caro et al., 2014; Hirschfeld and Attard, 2017; Prieto et al., 2019). To increase the protection and conservation of game species it is essential to understand the impact of hunting management tools in order to implement 'good practice' standards (Madsen, 1998a; Guillemain et al., 2002; Hirschfeld and Attard, 2017). Many tools are used to reduce the impact of hunting. Such approaches include bag restriction (Schroeder et al., 2014), shortening hunting periods (Brochet et al., 2009), and the creation of hunting– free reserves. This latter option is considered a chief tools for preservation of game bird populations. The response of wintering birds to these reserves has been investigated especially in waterbirds (e.g. Fox and Madsen, 1997; Madsen 1998b; Guillemain et al., 2002; Brochet et al., 2009; Casazza et al., 2012; Beatty et al., 2014). Most of these studies found a positive effect of reserves on the wintering birds that concentrated in these areas during hunting days (Fox and Madsen 1997; Madsen 1998b; Guillemain et al., 2002; Casazza et al., 2012; Beatty et al., 2014). However, as not all waterfowl species show the same response (Madsen 1998a, 1998b; Guillemain et al., 2002) the role of game reserves may differ even among similar bird species. In the case of land birds, fewer studies have dealt with this issue (Duriez et al., 2005a; Casas et al., 2009; Brøseth and Pedersen, 2010) and we are not aware of any studies in thrushes.

The hunting of migrant thrushes (Turdus spp.) remains a popular practice in Mediterranean countries where important stopover/wintering areas for these species are located (e.g., Santos and Tellería, 1985).

Overall, ca. 15 millions of thrushes are hunted yearly in Europe (Myrberget, 1990), mostly in France (around 2 million; Aubry et al., 2016), Italy (around 7 million; Andreotti et al., 2010) and Spain (more than 4 million; Hirschfeld and Attard, 2017). The effects of hunting on thrush population dynamics is poorly known (Sokos et al., 2013). Some studies have shown that the annual adult survival rates of song thrushes were correlated with hunting pressure (Aebischer et al., 1999), while others failed to demonstrate such an effect (Payevsky and Vysotsky, 2003).

In this context, it is unclear whether management tools such as the creation of hunting–free reserves within the winter quarters may benefit the conservation status of thrushes. To address this issue, we analysed abundance patterns in hunting areas and hunting–free reserves of two phylogenetically related thrush species, the song thrush (T. philomelos) and

the blackbird (T. merula) in a main wintering area of northern Spain. Both species share post–nuptial migratory phenology, that finishes in November (Aparicio, 2016; Purroy and Purroy, 2016), winter space use (Aparicio, 2016; Purroy and Purroy, 2016), and diet (Guitián, 1985; Soler et al., 1991; Paralikidis et al., 2009). However, the song thrush is a game bird within this region, while the blackbird is not. Therefore, we hypothesized that, after controlling for factors such as habitat type, if birds react to the existence of the reserve, abundance should contrast between areas, especially in the game species.

Methods The study was carried out in the Alhama River basin, Navarra, northern Spain (42º 3' 17.80'' N to 42º 10' 55.70'' N, 1º 53' 39.79'' W to 1º 43' 53.09'' W; fig. 1). The river bank consists of riparian forest comprising mainly ash trees Fraxinus spp., poplars Populus alba, tamarisks Tamarix spp., and shrubs such as brambles Rubus spp., rosebush Rosa spp. and hawthorns Crataegus monogyna. Contiguous to this forest and more distant from the river there is an agricultural matrix comprising olive trees, fruit orchard, vineyards, cereal crops and small farms. The zone is thus an attractive stopover and wintering site for many migratory passerines, further promoted by the zone's location near the Pyrenees and the southeastern edge of the Bay of Biscay (Galarza and Tellería, 2003; Carrascal and Díaz, 2006).

All thrush species except the blackbird and the ring ouzel (T. torquatus) can be hunted in Navarra from November to January, usually from fixed hunting sites. Overall, ca. 30,000 thrushes are shot every year in Navarra (source: Government of Navarra), which means relatively high hunting pressure in a region of ca. 10,400 km2. Navarra's hunting laws require the creation of hunting–free reserves. These areas must cover at least 12 % of the entire hunting surface within each regional county, and they must also comprise those habitats which have a higher importance for the conservation of game species. Reserves created for thrush species usually include olive groves and vineyards or riparian forests, which correspond to habitats selected by these species in winter (Soler et al., 1988).

In this study we carried out censuses immediately prior to the hunting season in 2018 (in October) and one month after the hunting season began (in December).

The point–count method (Blondel et al., 1970) was used. This method consists of counting all the birds seen or heard within a radius of 25 m from the observer’s position over a period of 10 min. We considered this radius in order to elude the possible negative effect of vegetation structure on bird detectability (Pacifici et al., 2008). To avoid observer–associated bias we performed all censuses were performed by the same observer (DV) (Diefenbach et al., 2003), from +1 h from dawn to –1 h before dusk. Twilight periods were then avoided to exclude the variations in birds' song activity throughout the day (Robbins, 1981) and the influence

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Hunting–free areas Alhama River Sampling points Hunting area Hunting–free area

N

0

1

2

3 km

Fig. 1. Map showing the location of the study area, the distribution of the reserves, and bird count points.

Fig. 1. Mapa de la localización de la zona de estudio en el que se muestra la distribución de las reservas y los puntos de conteo de las aves.

of typical movements from or to communal roosting places –rather common within the region– which would result in an over–estimation of bird counts. We considered a total of 44 sampling points, with 22 being situated in hunting–free reserves, and 22 in hunting areas (fig. 1). All sampling points were situated at a distance of > 500 m from each other in order to reduce double–counts (Sutherland et al., 2004).

Within each sampling point, the habitat was characterized within a radius of 25 m by calculating the proportion of nine habitats: riparian native forest, tamarisk, olive grove, fruit trees, orchard, vineyard, shrub, cereal crop, and farms (building) using GIS tools. The initial distribution of habitats was obtained from the Spanish map of crops and territory use, provided by the Ministry of Agriculture (source: www. mapa.gob.es) for 2000–2010. During the sampling work, the data provided by such maps were updated.

Statistical analyses Many habitat–related variables correlated with each other as they were calculated as a percentage over the area comprised within a buffer of 25 m–radius around each sampling unit (point–count) (for details see appendix 1). Thus, before starting to build a model we conducted a principal component analysis (PCA) on such variables in order to obtain a number of new variables that summarized habitat structure. The PCA provided five components (hereafter, PC1 to PC5) with an eigenvalue > 1, which, overall, accounted for

77.6 % of the variance (table 1): the PC1 correlated positively with natural habitat (riparian forest, shrubs) and negatively with croplands (groves, vineyards, and similar); PC2 correlated negatively with shrubs, cereals and olive groves; PC3 correlated positively with the presence of tamarisk and negatively with orchards and farms; PC4 correlated positively with vineyards and, to a lesser extent, with cereals; and PC5 correlated negatively with farms.

To test for the effect of hunting on bird counts we used generalized linear mixed models with bird counts as an object (dependent) variable, and the following explanatory variables: hunting regimen (hunting vs. reserve), period (October vs. December), a hunting regimen–period interaction, PC1 to PC5, and the sampling site, as random factor. Our target thrushes here were the song thrush and the blackbird. In this GLMM we considered a distribution of Poisson errors, with a log–linear link function. Using the 'lmer' package in R (Kuznetsova et al., 2017), we conducted a global starting model which included all the explanatory terms listed above (R notation): counts~hunting regimen × period + PC1 + PC2 + PC3 + PC4 + PC5 + (1|sampling site).

Between alternative models, those with lower Akaike (AIC) values were considered to have a better fit with the data (Akaike, 2011). A model would have a better fit with the data if it had an Akaike value lower than 2 as compared to a second model (Burnham and Anderson, 1998). We used the 'dredge' function for the model selection procedure (Barton, 2014). This

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Table 1. Factor loadings obtained from a principal component analysis on nine habitat–related variables.

We show here only those components that had eigenvalues > 1 (PC1 to PC5).

Tabla 1. Cargas factoriales obtenidas a partir de un análisis de componentes principales en nueve variables relacionadas con el hábitat. Solo se muestran los componentes con valores propios > 1 (de PC1 a PC5).

Factor Riparian forest Tamarisk Olive grove Fruit trees Vineyard Orchards Farms Shrubs Cereal crop Eigenvalue Variance (%)

PC1 +0.58 –0.01 –0.45 –0.52 –0.24 –0.16 +0.13 +0.32 –0.01 1.91 21.2

PC2 PC3 +0.28 +0.20 +0.17 +0.59 –0.35 +0.13 +0.25 +0.06 +0.11 +0.11 +0.21 –0.62 +0.13 –0.42 –0.50 –0.12 –0.62 +0.01 1.56 1.36 17.3 15.0

function runs all the possible combinations starting from the global model described above, and then list all of them according to their AIC value. Model averaging was carried out when more than a single model fitted the data equally well; for this the function we used 'model.avg' on the 'dredge' object.

PC4 PC5 –0.06 +0.13 –0.17 –0.06 –0.26 –0.23 –0.35 +0.21 +0.84 –0.05 –0.01 +0.42 –0.13 –0.79 –0.16 +0.28 +0.18 –0.01 1.15 1.01 12.8 11.3

We tested for the potential existence of spatial autocorrelation between bird counts and the location of our sampling points. With this goal we used the function 'correlogram' in R, built using a distance matrix for the sampling points and the residual values of the model which best fitted the data. Overall,

Table 2. List of the top–ranked models (those differing in less than 2 AICc units as compared to the first one) used to test for the effect of hunting–free reserves on song thrush and blackbird abundance.

For comparison, we also included null models.

Tabla 2. Lista de los modelos mejor clasificados (los que difieren en menos de 2 unidades de AICc respecto del primero) utilizados para determinar el efecto de las reservas en la abundancia del zorzal y el mirlo. A efectos de comparación, también se han incluido modelos nulos.

AICc

ΔAICc

AICc weight

Song thrush Model 1: PC3 + PC5 + hunt × peri 572.8 0.0 Model 2: PC3 + PC4 + PC5 + hunt × peri 574.1 1.3 Model 3: PC5 + hunt × peri 574.8 2.0 Null 722.6 149.8 Blackbird Model 1: PC1 + PC3 259.0 0.0 Model 2: PC3 259.1 0.1 Model 3: PC1 + PC3 + peri 260.6 1.6 Model 4: PC1 + PC3 + PC4 260.7 1.7 Model 5: PC3 + peri 260.7 1.7 Model 6: PC3 + PC4 260.9 1.9 Model 7: PC3 + hunt 261.0 2.0 Null 266.2 7.2

0.230 0.117 0.085 0.000 0.094 0.089 0.042 0.040 0.040 0.036 0.034 0.000

Animal Biodiversity and Conservation 44.1 (2021)

Autocorrelation

1.0

63

Correlogram

0.5 0.0 –0.5 –1.0 0

5,000

10,000 Distance

15,000

20,000

Fig. 2. Graphic representation of the spatial autocorrelation between bird count points.

Fig. 2. Representación gráfica de la autocorrelación espacial entre los puntos de conteo de las aves.

autocorrelation values for all distances were low, indicating a lack of spatial autocorrelation (fig. 2).

All statistical analyses were done in R (R Core Team, 2014).

A 80

We counted a total of 718 song thrushes in hunting– free areas (refuges) and the hunting area (495 and

B 5

Hunting Reserve

40

20

Hunting Reserve

4

Counts

60 Counts

Results

3 2 1

0 Oct

Period

Dec

0

Oct

Period

Dec

Fig. 3. Number of song thrushes (A) and blackbirds (B) detected in hunting and hunting–free reserve sampling sites before (Oct) or during (Dec) the hunting season. Horizontal lines denote median values; boxes extend from 25th to 75th percentile and the whiskers extend up to 1.5 times the interquartile range.

Any data beyond that distance are represented individually as points ('outliers').

Fig. 3. Número de zorzales (A) y mirlos (B) detectados en sitios de muestreo ubicados en zonas de caza y en reservas antes (Oct, octubre) del inicio de la temporada de caza o durante (Dec, diciembre) la misma. Las líneas horizontales denotan los valores medianos, las cajas se extienden desde el percentil 25 hasta el 75 y los bigotes, hasta 1,5 veces el intervalo intercuartílico. Los datos situados más allá de esa distancia se representan individualmente como puntos (valores atípicos).

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Table 3. Beta–parameter estimates of the averaged best–ranked models used to test for the effect of several factors on counts of song thrushes or blackbirds: 1 reference values (Beta = 0): hunt, hunting regimen; period, December.

Tabla 3. Estimaciones del parámetro beta de los modelos mejor clasificados de media y que se emplearon para determinar el efecto de varios factores en los conteos de zorzales y mirlos: 1 valores de referencia (Beta = 0); hunt, régimen de caza; período, diciembre.

Factor

Beta

SE (Beta)

P

Song thrush Hunt1:reserve

+0.95

0.25 < 0.001

Period :Oct.

+1.24

0.16 < 0.001

1

Hunt–Period –0.45 0.19 0.018 PC3

+0.20 0.09 0.035

PC4

–0.03 0.07 0.651

PC5

+0.34 0.11 0.002

Blackbird Period1:Oct. –0.04 0.12 0.755 PC1

–0.07 0.09 0.454

PC3

+0.34 0.11 0.004

PC4

+0.02 0.06 0.781

223 individuals, respectively), and 106 blackbirds (47 and 59 individuals, respectively).

After our selection procedure, we obtained two models that fitted the song thrush data equally well (table 2).

Both models included an effect of the hunting regime, period, the interaction between these two factors, and the PC3 and PC5. The second model also included an effect of PC4, although the parameter estimates of the averaged model showed that this effect was non– significant (table 3). Overall, song thrushes were more abundant in reserves in October than in December, in places richer in riparian habitats (riparian forest, tamarisk; PC3), and in orchards, shrubs and fruit crops and with a low proportion of farms (PC5). However, the hunting regime–period interaction showed that the number of song thrushes remained almost constant between periods in hunting–free reserve areas, and that abundance in both types of areas was similar in October (that is before the hunting season), whereas abundance was found to decrease notably in December in hunting areas (fig. 3).

For blackbirds, we obtained six models that fitted the data equally well. All of these models included an effect of PC3 on bird counts, with some models also including an effect of PC1 (3 models), PC4 (2 models), and period (2 models) (table 2). Interestingly, none of

these models showed an effect of hunting regime on bird counts. The averaged model included a significant, positive effect of PC3 on bird counts (table 3), showing that blackbirds tended to be more abundant at survey points richer in riparian forest or tamarisk.

Discussion Our results show that hunting activity in Navarra had an important effect on the abundance of song thrushes that over–wintered in an area comprising a mosaic of riparian forest and agricultural landscapes. Once the hunting season had started, song thrush abundance decreased in hunting areas but not in hunting–free reserves. Such effects were not found for the non–hunted thrush, the blackbird. The decrease in song thrushes in hunting sites could respond to several causes, either complementary or alternative: first, mortality by hunting in hunting areas could result in lower bird numbers across the season (e.g., Duriez et al., 2005a; Prieto et al., 2019); second, hunting disturbance to song thrushes may promote the abandonment of places where they were hunted in favor of those where hunting was not allowed (hunting–free reserve places) (e.g., Evans and Day, 2002; Bechet et al., 2004; Brochet et al., 2009; Casas et al., 2009; Casazza et al., 2012; Garaita and Arizaga, 2015). However, data in figure 2 show that the number of song thrushes did not increase in the hunting–free reserve sites in December, thus not supporting the idea that song thrushes displaced from hunting to hunting–free areas across the season.

Rather, our results may be more compatible with the idea that higher mortality causes a population decline in hunting places, but our data are insufficient to demonstrate this.Disturbed song thrushes may also leave the region and move to other areas outside the geographical range considered in this work. To confirm the exact mechanism driving abundance changes, it would be necessary to conduct studies based on individual marking (Salewski et al., 2007) or tracking e.g. using radio–telemetry (Bechet et al., 2004; Duriez et al., 2005b; Brøseth and Pedersen, 2010; Beatty et al., 2014).

Despite these shortcomings, the use of a hunting– free reserve is a critical management tool to contribute to the conservation of song thrush populations within the region, since song–thrushes did not decrease in numbers in hunting–free reserves in December, when the hunting season was about to end. A second question for future research will be to determine whether the current surface area of hunting–free reserves is sufficient to compensate for the apparently lower survival rates in hunting estates (an additional aspect to be investigated). Among other factors, the design of hunting–free reserves should consider all the ecological requirements of target species, and primary foraging and roosting places (e.g., Guillemain et al., 2002; Beatty et al., 2014).

In conclusion, we found hunting–free reserves had a positive impact on song thrush abundance at a local scale. The detected decline in abundance in hunting

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areas, however, could be due to various causes needing further research to discriminate between the factors potentially shaping this decline (mortality or emigration). Further studies will also help to determine which traits (e.g. size, habitat, connectivity with protected areas) should be promoted in this type of reserve (Fox and Madsen, 1997; Madsen, 1998a; Brochet et al., 2009) in order to improve their role as a refuge for thrushes and other game species.

Acknowledgements We thank Daniel Gould for his helpful advice and English revision, Adrián López for his help with the map, and Pelayo Acevedo for his help with the statistical analyses.

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Effects of elevation gradient and aspect on butterfly diversity on Galičica Mountain in the Republic of Macedonia (south–eastern Europe) M. Popović, B. Micevski, R. Verovnik

Popović, M., Micevski, B., Verovnik, R., 2021. Effects of elevation gradient and aspect on butterfly diversity on Galičica Mountain in the Republic of Macedonia (south–eastern Europe). Animal Bodiversity and Conservation, 44.1: 67–78, Doi: https://doi.org/10.32800/abc.2021.44.0067 Abstract Effects of elevation gradient and aspect on butterfly diversity on Galičica Mountain in the Republic of Macedonia (south–eastern Europe). The patterns of butterfly diversity and community changes in relation to elevation are an interesting and well–covered topic in ecology, but the effects of aspect have rarely been evaluated.

Here we studied the changes in butterfly species richness and communities along the elevation gradient and aspect of Galičica Mountain. As expected, species richness changed with altitude, showing a bimodal pattern with two peaks and a declining trend towards higher altitude. Changes were well–correlated with the area in each altitudinal zone, while the effects of productivity were less clear. Butterfly communities at higher altitudes were the most distinct when grouped according to β diversity estimates, followed by mid– and low–altitude communities. Indicator species were found in mid–altitudes and for the combination of low–mid and mid–high altitudes, but not among aspects. Overall, aspect produced a less conclusive effect on species richness and community composition. South and north accounted for most of these differences despite dominant western and eastern and exposition of the mountain slopes. The community temperature index declined with altitude and on the northern aspect, showing these areas hosted more cold–adapted species. Notes on butterfly conservation are provided as 23 species known from historical surveys have not been recorded recently.

Data published through GBIF (Doi: 10.15470/jacl7y) Key words: Species richness, Altitude, Exposition, Lepidoptera, iNEXT Resumen Efectos del gradiente de altitud y la orientación en la diversidad de mariposas de la montaña Galičica, en la República de Macedonia (Europa sudoriental). Los patrones de diversidad de mariposas y los cambios en las comunidades en relación con la altitud son un tema interesante y bien estudiado en ecología, pero los efectos de la orientación se han evaluado muy poco. En el presente estudio analizamos los cambios en la riqueza de especies de mariposas y sus comunidades a lo largo del gradiente de altitud y según la orientación de la montaña Galičica. De acuerdo con lo esperado, la riqueza de especies cambió con la altitud siguiendo un patrón bimodal con los máximos y una tendencia decreciente hacia mayores altitudes. Los cambios estuvieron bien correlacionados con la superficie de cada zona de altitud, mientras que los efectos de la productividad fueron menos evidentes. Las comunidades de mariposas a mayor altitud fueron las más peculiares cuando se agruparon según las estimaciones de la diversidad beta, seguidas de las comunidades a media altitud y a baja altitud. Se observaron especies indicadoras en altitudes medias y en la combinación de altitudes medias bajas y medias altas, pero no entre las orientaciones. En general, la orientación produjo un efecto menos concluyente en la riqueza de especies y la composición de las comunidades. La mayor parte de estas diferencias se produjeron en el norte y en el sur, a pesar de que las laderas de la montaña están predominantemente orientadas al oeste y el este. El índice de temperatura comunitaria disminuyó con la altitud y en la orientación norte, lo que pone de manifiesto que estas zonas albergaban más especies adaptadas al frío.

Se proporcionan notas sobre la conservación de las mariposas, ya que recientemente no se han registrado 23 de las especies observadas en estudios históricos.

Datos publicados en GBIF (Doi: 10.15470/jacl7y) ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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Palabras clave: Riqueza de especies, Altitud, Exposición, Lepidoptera, iNEXT Received: 10 VI 20; Conditional acceptance: 18 VIII 20; Final acceptance: 05 X 20 Miloš Popović, University of Niš, Faculty of Natural Sciences and Mathematics, Department for Biology and Ecology, Višegradska 33, 18000 Niš, Serbia.– Branko Micevski, University of Skopje, Faculty of Natural Sciences, Department for Animal Taxonomy and Ecology, Arhimedova 3 1000 Skopje, Republic of Macedonia.– Rudi Verovnik, University of Ljubljana, Biotechnical Faculty, Department of Biology, Jamnikarjeva 101, 1000 Ljubljana, Slovenia.

Corresponding author: M. Popović. E–mail: mpopovic@pmf.ni.ac.rs ORCID ID: Miloš Popović: 0000-0003-0887-6683; Rudi Verovnik: 0000-0002-5841-5925

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Introduction It is generally agreed that species diversity declines with altitude, somewhat repeating the more stable latitudinal pattern (Rahbek, 1995). However, changes with elevation are more complex and species diversity tends to follow four main patterns with rising altitude: decreasing, low plateau, low plateau with mid–elevation peak, and mid–elevation peak (McCain et al., 2010).

These patterns could be explained by several ecological factors, including climate and productivity, species–area relationship, mid–domain effect, effects of ecotone, biotic factors, evolution, and historical circumstances (Colwell and Lees, 2000; Lomolino, 2001; McCain, 2007; McCain et al., 2010). While studying the effects of biotic and evolutionary factors requires detailed planning and study design, other factors can often be tested more easily. Relatively large mountain ranges with diverse geological structure and climate (from Continental to Mediterranean) make south–eastern Europe an interesting region for studies of elevation gradients in species diversity. At the same time, data on butterfly diversity in this region is scattered in a multitude of faunistic papers, while few studies address the butterfly diversity pattern (Mihoci et al., 2011; Zografou et al., 2014, 2017; Kaltsas et al., 2018). Similarly, the effect of aspect is only rarely taken into consideration when addressing the distribution patterns of butterflies in mountains (Gutiérrez, 1997; Mihoci et al., 2011). However, the aspect of the mountain slope is considered an important topographic factor (i.e. Bennie et al., 2008) and it could play a role in shaping butterfly communities.

The climate along the elevation gradient is known to affect insect biology (Hodkinson, 2005) and is predicted to produce the diversity pattern with mid– altitude peaks in temperate regions (Despland et al., 2012; McCain, 2007). Butterflies have shown the same patterns of diversity changes in the mountains as other animal groups, and these changes are commonly guided by variation in climate (MacNally et al., 2003; Gallou et al., 2017). Harsh conditions at a higher elevation have prompted numerous ecological adaptations in butterflies (Junker et al., 2010; Kevan and Shorthouse, 1970; Leingärtner et al., 2014) and it has been suggested that species communities at high elevations tend to show some evolutionary constraints (Pellissier et al., 2013). As the current global climate change induces rapid shifts in butterfly communities across continents (Devictor et al., 2012, Zografou et al., 2014), mountain systems have become increasingly important as refugia for species retracting pole–wards (Fleishman et al., 2000; Hampe and Petit, 2005; Wilson et al., 2007). These rapid changes can be traced by climate change indicators such as the community temperature index (CTI) (Schweiger et al., 2014; Zografou et al., 2014). This index also allows the comparison of extant communities within altitudinal gradient or aspects, where CTI values are expected to decline with altitude and on northern slopes.

We compiled a check–list of butterfly species (Papilionoidea) and a large dataset of all records for the Galičica mountain range in the south–western part of the Republic of Macedonia, combining data from

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the literature and the authors’ field observations. The main goal of the study was to examine how butterfly species richness changes according to altitude and aspect of the mountain, which, in contrast to the nearby ranges, stretches in a north–south direction. We tested the effect of the area, ecosystem productivity and mid–domain effect on elevational patterns of species richness. In addition, we studied the similarities between butterfly communities and determined whether communities along the elevation gradient and aspect differed in community temperature indexes.

We also provide notes on the potential extinction of several butterfly species in the area and discuss the conservation value of this mountain range.

Material and methods Study area Galičica is a calcareous mountain range at the junction of Macedonia, Albania and Greece and is shared between the two first mentioned states (fig. 1). It rises between the lakes of Prespa in the east and Ohrid in the west. The climate is mild–continental and Mediterranean, with climatic conditions stabilized by the presence of large water bodies. The mountain is situated on an elevated plain, with the base at 695 m and reaching the altitude of 2,265 m (Avramoski et al., 2010; Ćušterevska, 2016). It stretches in a south–north direction; the east and west are therefore dominant aspects. In 1958 the Macedonian part of Galičica was proclaimed a National Park, with a total area of 24,151 ha, and protected by the state (Matevski et al., 2011).

Data collation and preparation A historical overview of butterfly fauna of Mt. Galičica was summarized by Krpač et al. (2011). This publication was geo–referenced within Biologer.org biodiversity database (Popović et al., 2020) and used as a baseline for our study. Besides records from the literature, we used an original dataset from Verovnik et al. (2010), unpublished data by I. Jugovic, A. Keymeulen, N. Micevski and the authors' personal records. Species observations of MP, RV and geo–referenced records from the literature can be downloaded after registration on Biologer.org or accessed through GBIF (Doi: 10.15470/jacl7y). Four major periods in butterfly studies can be recognized: i) an initial study in 1918; ii) short field surveys in the mid–19th century; iii) detailed inventory work in the seventies and eighties; and iv) intensive field studies by several experts from 1995 onwards. A detailed checklist of recorded species is given in supplementary material, differentiating historical (before 1995) and recent data.

Compiling species observations from different datasets could produce bias in the data and should be taken with caution. Thus, before proceeding to the statistical analysis, species occurrence records were subset to those with coordinate precision no less than 2 km.

The unique combination of the species name, locality name and year was used to create samples –lists of

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observed species– and was assumed to be equal to the list of species recorded at a single sampling event. The incidence of frequency of species was determined by combining the samples from a certain elevation zone, or aspect. To remove accidental individual observations, data were further subset to include only samples with more than five observed species.

Altitudes and aspects were extracted from a digital elevation model (European Environment Agency, 2016), while all GIS calculations were made using raster package in R (R Core Team, 2019). Altitude at each point of observation was extracted and used to divide samples in n classes of equal length between maximal and minimal altitude. Calculations were made starting from n = 20 and decreasing the value until good estimates were obtained (i.e. low standard errors, high sample coverage, and good representation of all classes).

This resulted in 10 altitudinal classes from 689 m to 2,234 m. Aspect values were calculated in degrees and transformed to four major aspects (cardinal directions): north (0º–45º) and 315º–360º), east (45º–135º), south (135º–225º) and west (225º–315º). To determine dominant mountain aspects for each sample, we included the area in a radius of 1 km around the observation point (i.e. not only the aspect at the exact sampling location).

The joint influence of several aspects was minimized by selecting samples with single aspects contributing more than 50 %, and discarding data for samples with more uniform aspect contributions.

Species richness To compare differences in species diversity between altitudinal classes and aspects, we used species richness measure as a representation of α diversity.

Calculations were made using the iNEXT package in R, allowing construction of both rarefaction and extrapolation curves; this provided a robust estimate of the true species diversity even in cases with low and unequal sampling effort (Chao et al., 2014; Hsieh et al., 2016). Incidence frequencies prepared in the previous step were used as input data and are available in supplementary material.

The effect of an area on species richness was assessed by plotting the available area in each altitudinal class or aspect versus estimated species richness. The relationship between productivity and species richness was examined by plotting values of normalized difference vegetation index (NDVI) versus estimated species richness. NDVI was obtained from MODIS (Didan, 2015) between April and September 2017–2019 (representing the vegetation period for the last three years). Average NDVI values were then calculated for each altitudinal class and aspect. Since productivity is directly related to climate, productivity–richness relationship could reflect the influence of climate on butterflies along the altitudinal gradient (Levanoni et al., 2011; Pettorelli et al., 2005).

The presence of mid–domain effect was checked by plotting 95 % CI of the null model (1,000 replicates) against observed species richness, using rangemodel R package in R (McCain, 2003; Colwell, 2008). Where applicable, statistical significance was checked using Spearman correlation test in R.

Changes in butterfly communities To estimate the similarity between butterfly communities (β diversity) at different altitudes and aspects of Mt. Galičica, we used the probability version of the Chao–Jaccard index, provided by CommEcol package in R. This index is less biased than classic similarity indices and it is not sensitive to the omission of some species from the samples (Chao et al., 2005). The results are shown as unrooted dendrograms produced in ape package in R. In addition to providing the Chao–Jaccard estimate, we used the indicator value index to search for indicator species of a certain elevation zone and aspect (Cáceres and Legendre, 2009). Elevation zones were grouped according to the estimates suggested by Chao–Jaccard index in three elevation classes (low, mid and high altitudes). Estimates were obtained using package indicspecies in R using IndVal.g estimator with 1,000 permutations.

To test whether climate had any effects on shaping the butterfly communities we calculated the community temperature index (CTI) for each delineated altitudinal class and aspect of Mt. Galičica. CTI values were calculated as an average of the species temperature index (STI), accounting also for butterfly abundance (Schweiger et al., 2014). If the climate affected the distribution of butterflies in communities, it could be expected that CTI would decline from the southern to the northern aspect and from lower altitudes towards the top of the mountain. Differences were statistically tested using ANOVA and pairwise t–test in R. Since the test could be affected by unequal sampling, different season, or year of observation, we used only our recent field observations that were collated with an even sampling effort and over the same period.

Results A total of 4,137 occurrence records from Mt.Galičica were collated, most of these (2,376) being new field observations (see also the dataset published through GBIF (Doi: 10.15470/jacl7y). After removing duplicates and imprecise records, we retained 2,883 observations for the analysis. A total of 168 species were recorded for Mt. Galičica, 159 of which were known before 1995, while 145 were confirmed in recent studies (supplementary material). The decline in species was also evident from an estimated 152 ± 15 species before 1995 to an estimated 143 ± 3 species in the recent period (sample coverage 0.90 and 0.99 respectively). Compared to the overview by Krpač et al. (2011), three species were recorded for the first time: Colias caucasica Staudinger, 1871 (already noted by Verovnik et al., 2010), Satyrium pruni (Linnaeus, 1758) and Melitaea ornata Christoph, 1893.

Species richness indices Estimated sample coverage for the iNEXT analysis ranged from 0.69 to 0.97 for altitudinal classes and from 0.61 to 0.98 for aspects, with the lowest estimate

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Country borders National Park Sampling locations Lakes Rivers Altitudinal zones 689 844 998 1,152 1,307 1,462 1,616 N 1,770 1,925 2,080 2,234

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Fig. 1. Galičica mountain range in the Republic of Macedonia shown on a relief map, with altitudes corresponding to the altitudinal classes given in the manuscript. Blue indicates the lakes of Ohrid (to the west) and Prespa (to the east). All butterfly sampling locations are shown as white circles.

Fig. 1. Mapa de relieve en el que se muestra la cadena montañosa Galičica en la República de Macedonia, con altitudes que se corresponden con las clases de altitud que figuran en el manuscrito. El color azul indica los lagos de Ohrid (al oeste) y Prespa (al este). Todos los sitios de muestreo de mariposas se indican con círculos blancos.

being for the southern aspect (supplementary material).

Butterfly species richness on Mt. Galičica showed a bimodal distribution along the altitudinal span, with peaks at about 1,100 m and 1,500 m, and a declining trend towards the higher elevations (fig. 2A). We observed a strong correlation between the size of the area available in each altitudinal zone and estimated species richness (fig. 2A); this relation was statistically significant (rho = 0.81, S = 32, P = 0.008). A comparison of species diversity among different aspects of the mountain showed a more uniform pattern, with somewhat lower estimates for species richness on the northern and eastern slopes and higher richness estimates for the southern and the western slopes (fig. 2B). The correlation between estimated species richness and the area available in different aspects of the mountain was not significant (rho = –0.20, S = 12, P = 0.917).

Most of the area of the mountain comprises western and eastern slopes due to the mountain predominant south–north direction (fig. 1, 2B). However, it should be

noted that observed and estimated species richness showed a large discrepancy for the southern aspect, while large standard errors and small sample coverage indicate imprecise calculations.

We were unable to determine a clear correlation between ecosystem productivity and butterfly species richness along the altitude, although estimates were close to significant (rho = 0.60, S = 66, P = 0.073) and some positive relation is clearly visible in the graph (fig.

2C). The highest discrepancies were near the second peak in species richness (fig. 2C). NDVI tended to increase to about 1,000 meters, then slowly decline towards the highest altitudes. In contrast, the NDVI index showed a similar distribution along the mountain aspects, with somewhat lower values on the warmer mountain slopes (fig. 2D); this could not be correlated with estimated species richness (rho = –0.80, S = 18, P = 0.333). We found no strong evidence for mid–domain effect on species richness as most points fell outside the confidence interval predicted by the null model (fig. 2E).

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Fig. 2. La relación entre la riqueza de especies en diferentes altitudes y orientaciones de la montaña Galičica y varias variables predictivas. En los gráficos superiores se muestra la comparación de la superficie disponible (histograma) y la riqueza de especies (líneas) de cada clase de altitud (A) y orientación (B). En los gráficos centrales se muestra una comparación parecida entre la productividad (histograma de los valores medios del índice normalizado diferencial de la vegetación) y la riqueza de especies (líneas) entre clases de altitud C) y orientación (D). En el gráfico inferior (E) se muestra el intervalo de confianza del 95 % para la predicción del modelo nulo (superficie azul) elaborada para comprobar el efecto del dominio medio. Los valores estimados de la riqueza de especies se señalan con rombos con los límites inferior y superior del intervalo de confianza. Los valores de la riqueza de especies observada se indican con círculos. Altitudinal classes: a, 689–844; b, 844–998; c, 998–1,152; d, 1,152–1,307; e, 1,307–1,462; f, 1,462–1,616; g, 1,616–1,770; h, 1,770–1,925; i, 1,925–2,080; j, 2,080–2,234.

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Fig. 3. A, cluster dendrogram constructed from Chao–Jaccard dissimilarity index of β diversity among butterfly communities at different altitudinal zones; B, mountain aspects; C, box–plots showing mean values for the community temperature index (CTI) of butterfly assemblages along elevation gradient; and D, box–plots showing butterfly assemblages at different aspects of Mt. Galičica. Detailed statistics with results of pairwise comparison in CTI values are given in supplementary material. For abbreviations of altitudinal classes see fig. 2.

Fig. 3. A, dendrograma de grupos elaborado a partir del índice de similitud de Chao–Jaccard de la diversidad β entre las comunidades de mariposas de diferentes zonas de altitud; B, orientaciones de la montaña; C, diagramas de caja en los que se muestran los valores medios del índice de temperatura comunitaria de los ensamblajes de mariposas a lo largo del gradiente de altitud, D, diagramas de caja en los que se muestran los ensamblajes de mariposas en las distintas orientaciones de la montaña Galičica. En material suplementatario se proporcionan estadísticas detalladas con resultados de la comparación por pares de valores del índice de temperatura comunitaria. Para las abreviaturas de las clases de altitud, véase la fig. 2.

Changes in species communities The Chao–Jaccard dissimilarity index was generally higher for communities at more distant altitudinal levels, with values ranging from 0.15 to 0.7 (more details available in supplementary material). Communities at the highest altitudes were clearly the most distinctive, but those at mid–elevations also tended to form a separate group in the dendrogram (fig. 3A). Communities on different aspects showed lower differentiation with a dissimilarity index ranging from 0.1 to 0.36 (supplementary material).

Eastern and western aspects hosted practically the same communities, while some differences were evident for northern and especially southern aspects (fig. 3B).

The indicator value index was computed for 127 and 75 species along the altitude and aspect, respectively. Indicator species were found in the mid–altitude zone and for the combination of low–mid and mid–high zones (table 1), while no indicator species were found for the mountain aspects.

The community temperature index (CTI) values differed significantly between altitudinal zones (F = 4.904, df = 9, P << 0.001) and also between different aspects (F = 3.558, df = 3, P = 0.014). A declining trend was visible in average CTI values towards the higher altitudes, although the zone around the mid–elevations deviated from the linear decline pattern (fig. 3C). Statistical significance in pairwise comparisons between altitudinal zones was

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Table 1. Indicator species for three altitudinal zones of Mt. Galičica. Altitudinal zones were delineated using the values of the Chao–Jaccard estimate (fig. 3) to three zones: low elevation (689–1,462 m), mid elevation (1,462–1,770 m) and high elevation (1,770–2,234 m). Only statistically significant indicator species are listed.

Tabla 1. Especies indicadoras de tres zonas de altitud de la montaña Galičica. Utilizando los valores de la estimación de Chao–Jaccard (fig. 3) se definieron tres zonas según la altitud: altitud baja (689–1.462 m), altitud media (1.462–1.770 m) y altitud alta (1.770–2.234 m). Solo se muestran las especies indicadoras estadísticamente significativas.

Mid elevation zone (15 species) Parnassius apollo Pyrgus alveus Carcharodus floccifera Hesperia comma Hamearis lucina Favonius quercus Lycaena thersamon Plebejus argyrognomon Brenthis hecate Kirinia climene Lasiommata petropolitana Hyponephele lycaon Hyponephele lupina Satyrus ferula Pseudochazara geyeri Mid and high elevation (5 species) Parnassius mnemosyne Lycaena candens Polyommatus eros Boloria graeca Melanargia russiae

observed only for more distant altitudinal classes, with and the first two altitudinal zones accounting for most of this significance (details in supplementary material).

However, the comparison of communities at different mountain aspects showed more uniform distribution of CTI (fig. 3D), and only the values on the northern aspect were significantly lower (supplementary material).

Discussion Butterfly diversity and its potential decline Despite the relatively small area studied, butterfly fauna of Mt. Galičica in the Republic of Macedonia is extremely rich, with 168 species recorded. This is comparable to other high biodiversity mountain regions in the Balkan Peninsula, such as Stara Planina in Serbia with 167 species (Langourov, 2019; Popović and Đurić, 2014), Stara Planina in Bulgaria with184 species (Kolev, pers.

Mid and low elevation (18 species) Iphiclides podalirius Pyrgus cinarae Thymelicus lineola Pieris balcana Pieris ergane Leptidea sinapis Lycaena phlaeas Plebejus argus Aricia agestis Polyommatus admetus Lysandra bellargus Argynnis paphia Issoria lathonia Polygonia c–album Coenonympha pamphilus Maniola jurtina Melanargia galathea Brintesia circe

comm.), Shar Planina with 169 species (Jakšić, 1998; Melovski, 2003), Mt. Olympus with 155 species (Pamperis, 2009), Vitosha with 155 (Beshkov, 2014), Rila with 174, and Pirin with 195 (Kolev, pers. comm.). In addition to high butterfly diversity, Galičica is an important area for butterfly conservation due to the presence of one threatened (Phengaris arion) and 17 near–threatened species at the continental level (van Swaay et al., 2010), and 21 threatened species at a national level (Krpač and Dacremont, 2012). This mountain has also been recognized as a prime butterfly area in Europe (Jakšić, 2003).

The absence of new records for as many as 23 species together with a lower estimated number of species in the recent period is noteworthy, however, and might indicate true extinctions of several taxa. The majority of potentially extinct species include habitat specialists, such as Anthocharis damone, Euchloe penia, Tarucus balkanicus, Pseudochazara amalthea and Spialia phlomidis that were known only from the open rocky

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habitats, once abundant above Ohrid town. This area in particular (authors pers. observ.) and the entire mountain is becoming overgrown due to abandonment of pasturing, with forest cover increasing on Mt. Galičica from 40 % to 58 %, and pastures declining from 50 % to 24 % in the last decades (Despodovska et al., 2012). Similar patterns have been found throughout Mediterranean Europe, with open grassland butterflies declining due to increased forest cover (Slancarova et al., 2016; Ubach et al., 2020).

The lack of new records for woodland species such as Limenitis camilla, Neptis rivularis and Erebia ligea is difficult to explain given the increased forest cover. However, these butterflies are linked to more humid habitats, and recent changes in climate –with prolonged droughts and higher aridity– could cause their decline. The same could be true for the extinction of Erebia oeme, one of seven high alpine species (Varga and Varga–Sipos, 2001) recorded for Mt. Galičica.

Species richness pattern The estimated richness of butterfly species on the elevation gradient of Galičica Mt. shows a bimodal distribution pattern, with two peaks and a declining trend towards the higher elevations. The decline in species richness between the two peaks was evident even when zones between 1,152 and 1,462 m were grouped together for the analyses (results not shown here), showing that the estimates were not caused by unequal or small sample sizes. Altitudinal patterns for butterfly species richness usually show similar, declining trend towards high elevations with peaks in mid–altitudes (Gutierrez and Menendez, 1995; Gutiérrez, 1997; Wilson et al., 2007; Levanoni et al., 2011; Stefanescu et al., 2011; Despland et al., 2012; Gallou et al., 2017; and the overview in Kaltsas et al., 2018).

However, a bimodal pattern is not a rare phenomenon for butterflies peaking at midaltitudes and it has often been recorded in other studies (Gutierrez and Menendez, 1995; Levanoni et al., 2011; Stefanescu et al., 2011, Gallou et al., 2017). There is also considerable evidence for the monotonic decline in butterfly diversity along the elevation gradient (Mihoci et al., 2011; Leingärtner et al., 2014; Kaltsas et al., 2018), but an insignificant trend (Kaltsas et al., 2018) and increase in species richness (Wettstein and Schmid, 1999; Pyrcz et al., 2009) has also been reported. Note that the increase in species richness with altitude is more likely to be caused by specific habitat composition (Wettstein and Schmid, 1999) or by the study of an exclusively montane taxonomic group (Pyrcz et al., 2009).

Species richness was significantly correlated with the area available in each altitudinal class on Galičica Mt., providing strong evidence for species–area relationship. In a similar manner, richness seemed to follow the ecosystem productivity (NDVI) until the prominent peak at about 1,500 m, which is probably caused by the vast area available in this altitudinal zone (coinciding with a large mountain plateau). Numerous studies have shown that butterfly diversity is correlated with precipitation and temperature (Mac Nally et al., 2003; Acharya and Vijayan, 2015). Productivity is derivative of these variables and is predicted to peak at mid altitudes

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along with species richness of butterflies, but heterogeneity in productivity was also an important predictor (Levanoni et al., 2011). The mid–domain hypothesis suggests that communities developing at high and low altitudes overlap in the mid–range, creating a peak in species richness, as predicted by theoretical models (Colwell and Lees, 2000; McCain et al., 2010). Although we found weak evidence that species richness follows pure predictions of the mid–domain model (fig. 2E), it is not impossible that some patterns in species diversity could be caused by overlapping of the communities from higher and lower elevation zones (see the discussion below). Diversity of butterflies along the elevation gradient could also be affected by heterogeneity of habitats, human disturbance (Lien, 2013; Gallou et al., 2017), biotic interactions, and evolutionary history (Pellissier et al., 2013). With so many factors involved, it is more likely that the actual species richness pattern is a product of these factors (Lomolino, 2001).

The effects of aspect on species communities are better studied in plants (i.e. Gallardo–Cruz et al., 2009; Holland and Steyn, 1975) and little is known about its effect on butterfly diversity. On the similarly oriented Toiyabe range in Nevada, eastern slopes are shown to host more butterfly species (Fleishman et al., 1997). This was explained by more diverse habitats on the eastern slopes and better connectivity, allowing intrusion of southern faunal elements. On Mt. Biokovo in Croatia, butterfly richness was higher on northern slopes than on the very steep and vegetation–poor southern aspects, which are also more exposed to strong bora winds (Mihoci et al., 2011).

Our results did not provide any conclusive evidence on the effects of aspect on butterfly richness, despite the unequal distribution of the aspects in Mt Galičica.

Somewhat lower estimates of species richness were observed in the northern and eastern exposures, but the estimates for the southern aspect were unreliable and discrepancy between observed and estimated species richness was strong (fig. 2B, 2D).

Community changes Changes in butterfly communities along the altitude (fig. 3A) coincided well with the transition zones of major forest communities on Galičica Mt., with oak forest up to 1,200/1,400 m and beech forests up to 1,900 m (Matevski et al., 2011). Interestingly, only the mid–elevation zone (1,462–1,770 m) had unique indicator species (15), and it shared some indicator species with lower (18) and higher elevation zones (5).

This mid–elevation zone also had the highest species richness, and at least partially, this richness could be attributed to the overlapping species from higher and lower elevation zones, providing some evidence for mid–domain or ecotone effects. The changes observed in the community temperature index over the altitudes (fig. 3C) matched our theoretical assumptions. As altitude increased, the communities were composed of more cold adapted species, resulting in lower values of CTI, but these changes were subtle.

In contrast to clear separation of high altitude species by the Chao–Jaccard index, no indicator species

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were found for butterfly communities in the highest elevation zone as high altitude species were shared with mid–elevations (table 1). Butterfly species at higher elevations are known to have distinctive ecological adaptations that restrict their distribution (Kevan and Shorthouse, 1970; Leingärtner et al., 2014) and some of them are known to have evolved as separate lineages in the Balkan refugia during the last glaciations (Varga and Varga–Sipos, 2001; Schmitt and Varga, 2012).

Admittedly, the number of high alpine species is low for Mt. Galičica, but such a pattern is also observed on other calcareous mountains in the Mediterranean region of south–east Europe (i.e. Sijarić, 1983; Mihoci et al., 2011; Kaltsas et al., 2018) and could probably be explained by predominant xeric conditions and limited alpine areas above 2,000 m. Finally, a small sample size at the highest altitudes in our study and the low number of high altitude species could limit the number of estimable indicator species.

The most striking result regarding aspect of Galičica Mt. is the lack of differentiation in species assemblages between western and eastern slopes even though they are the dominant aspects on the mountain and clearly separated by a central mountain plateau. A similar result was obtained in a study comparing tree cover on Mt. Galičica; it showed that only southern and northern slopes hosted distinctive communities, while western and eastern aspects were similar in species composition (Matevski et al., 2011). This is in line with lower estimates of CTI for butterflies on the northern aspect.

Northern slopes receive less insolation (Geiger et al., 1995) and thus host more cold–adapted species. The butterfly assemblage on the northern aspect are therefore likely affected by local ecological factors such as woodland cover, which is more extensive at colder and more humid parts of this calcareous massif.

Conclusion Altitude was found to be a strong driver in shaping butterfly species diversity, with species richness peaking twice at mid–altitudes and declining towards the top of the mountain. The explanation for this pattern is likely linked to a highly significant species–area relationship, with possible effects of ecosystem productivity (surrogate for climate) and community overlap. According to the β diversity estimates, most distinctive butterfly fauna was found close to the top of the mountain. However, indicator species were confined to the mid–elevation zone or shared between mid–low and mid–high elevations.

The effect of aspect was not as strong and easy to interpret as the effect of altitude. Comparing all the evidence, it can be concluded that eastern and western aspect have similar richness and species composition and some subtle differences were found when contrasting southern and northern slopes, the latter with marginally lower butterfly richness.

Habitat changes on Mt. Galičica in recent decades, especially the decline of pasturing, have already played a strong role in shaping butterfly communities and have probably caused extinction of several habitat specialist butterfly species. Habitats could easily be restored and

sustained with traditional grazing, creating a system that would benefit the local communities, maintain the diverse calcareous grasslands, and enable long–term survival of the unique butterfly communities of Mt. Galičica.

Acknowledgements The authors thank Ivan Jugovic, Angel Keymeulen and Nikola Micevski for their field observations of butterflies of Galičica Mt. We also thank Andrej Peternel, Kaja Vukotić and Đorđe Radevski for accompanying us during parts of our field surveys, and the anonymous reviewers and journal editors for useful and inspiring comments which substantially improved the manuscript. The work of MP was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia, contract No. 451–03–68/2020–14/200124.

RV was partially funded by the Slovenian Research agency (program P1–0184).

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Wilson, R. J., Gutiérrez, D., Gutiérrez, J., Monserrat, V. J., 2007. An elevational shift in butterfly species richness and composition accompanying recent climate change. Global Change Biology, 13: 1873– 1887, Doi: 10.1111/j.1365-2486.2007.01418.x Zografou, K., Kati, V., Grill, A., Wilson, R. J., Tzirkalli, E., Pamperis, L. N., Halley, J. M., 2014. Signals of climate change in butterfly communities in a Mediterranean protected area. Plos One, 9(1): e87245, Doi: 10.1371/journal.pone.0087245 Zografou, K., Wilson, R. J., Halley, J. M., Tzirkalli, E., Kati, V., 2017. How are arthopod communities structured and why are they so diverse? Answers from Mediterranean mountains using hierarchical additive partitioning. Biodiversity and Conservation, 26(6): 1333–1351, Doi: 10.1007/s10531-0171303-2

Animal Biodiversity and Conservation 44.1 (2021)

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The importance of addressing different Red Lists in conservation studies: an analysis comparing the conservation status of Brazilian mammals M. C. Drago, D. Vrcibradic

Drago, M. C., Vrcibradic, D., 2021. The importance of addressing different Red Lists in conservation studies: an analysis comparing the conservation status of Brazilian mammals. Animal Biodiversity and Conservation, 44.1: 79–88, Doi: https://doi.org/10.32800/abc.2021.44.0079 Abstract The importance of addressing different Red Lists in conservation studies: an analysis comparing the conservation status of Brazilian mammals. Red Lists are important conservation tools because they attempt to estimate the extinction risks of species. We compared the conservation status of Brazilian mammals presented in the Brazilian Red Book with those presented in the IUCN Red List, highlighting the importance of each list and why they should be used jointly. Out of 636 species, 181 were considered endemic to Brazil and 121 were considered threatened by at least one of the lists. Considering the complete database, 86 % of the species had the same status on both lists, whereas only 48 % of the threatened species had the same status. Some possible factors responsible for variations are the period in which the evaluations were carried out, the evaluation process and the fact that a species threatened nationally may not be threatened globally. We recommend that communication should be improved, that lists should be kept updated, and that both the type of information and the data itself to be used in the assessments should be standardized.

Key words: Brazilian Red Book of Threatened Fauna, IUCN Red List, Mammalia, Biodiversity, Endemic species, Threatened species Resumen La importancia de abordar diferentes Listas Rojas en los estudios de conservación: un análisis que compara el estado de conservación de los mamíferos brasileños. Las Listas Rojas son importantes herramientas de conservación porque intentan estimar el riesgo de extinción de las especies. Comparamos los estados de conservación de los mamíferos brasileños presentados en el Libro Rojo de Brasil con los presentados en la Lista Roja de la Unión Internacional para la Conservación de la Naturaleza (UICN) y destacamos la importancia de cada lista y el motivo por el que se deberían usar conjuntamente. De 636 especies, 181 se consideraron endémicas del Brasil y 121 se consideraron ameanazadas en al menos una de las listas. Considerando la base de datos completa, el 86 % de las especies tenía el mismo estado en ambas listas; no obstante, esto solo ocurría en el 48 % de las especies amenazadas. Las variaciones se explican, entre otros factores, por el período en el que se realizaron las evaluaciones, el proceso de evaluación y el hecho de que una especie amenazada a nivel nacional puede no estarlo a nivel mundial. Recomendamos que se mejore la comunicación, que las listas se mantengan actualizadas y que se estandaricen tanto el tipo de información como los propios datos que se utilizarán en las evaluaciones.

Palabras clave: Libro Rojo de Fauna Amenazada de Brasil, Lista Roja de la UICN, Mammalia, Biodiversidad, Especies endémicas, Especies ameanazadas Received: 23 VII 20; Conditional acceptance: 28 X 20; Final acceptance: 25 XI 20 Matheus C. Drago, Programa de Pós–Graduação em Ciências Biológicas (Biodiversidade Neotropical), Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, Brasil.– Davor Vrcibradic, Departamento de Zoologia, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, Brasil.

Corresponding author: Matheus C. Drago. E–mail: matheusdrago96@gmail.com ORCID ID: M. C. Drago: 0000-0003-3737-8552; D. Vrcibradic: 0000-0002-6355-3441 ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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Introduction Biodiversity conservation is one of the biggest challenges facing the current generation (Vale et al., 2009).

Megadiverse countries, such as Brazil, therefore have an enormous responsibility when it comes to protecting endangered species (Brandon et al., 2005). The richness of Brazil's mammal species, for example, is considered by some authors to be the highest in the world, with over 700 species and a high degree of endemism at the national level (Mittermeier et al., 1997; Costa et al., 2005; Lewinsohn and Prado, 2005; Quintela et al., 2020).

When species are assigned to categories (known as conservation status) that represent their degree of threat, their risk of extinction can be estimated, making it easier to infer which species need urgent conservation actions (Peres et al., 2011), evaluate the state of biodiversity, identify sites for conservation action, and inform policy and management (Rodrigues et al., 2006). Red Lists of threatened fauna are, from this point of view, important conservation tools. Having already assessed the global risk of extinction of more than 116,000 species (including more than 5,000 mammals), the International Union for Conservation of Nature (IUCN) has played a major role in making these lists known worldwide.

Some of the criteria used in those assessments are restricted geographic distribution, small and declining population size, and, based on quantitative analysis, a high probability of extinction in nature. Its scheme of species classification according to threat status uses the following categories: Not Evaluated (NE), Data Deficient (DD) (when there is no adequate information to assess the risk), Least Concern (LC) (when the species is evaluated but does not fall into the other categories; usually encompassing abundant and widely distributed taxa), Near Threatened (NT) (when the species is close to qualifying as threatened or when it is expected to be classified as such soon), Vulnerable (VU) (when the species faces a high risk of extinction in the wild), Endangered (EN) (when the species faces a very high risk of extinction in the wild), Critically Endangered (CR) (when the species face an even higher risk of extinction in the wild), Extinct in the Wild (EW) and Extinct (EX).

In Brazil, the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), a Brazilian government institution from the Ministry of Environment, periodically publishes the so–called Red Books of Threatened Fauna. These Red Books have a similar role to the IUCN Red Lists, listing the species considered to be threatened nationally, classifying them according to their conservation status, and providing ecological information about them. The most recent Red Book was published in 2018, representing a huge effort to evaluate all described vertebrate taxa occurring in the country and listing 680 mammal species officially known to occur in Brazil. Of these, 108 (15.9 %) were considered nationally threatened (ICMBio/MMA, 2018).

In the present study, we compared the conservation status of Brazilian mammal species listed in

the Brazilian Red Book of Threatened Fauna with those presented in the IUCN Red List, highlighting the importance of each list and why they should be used jointly in order to generate even more accurate assessments. We expected to find some differences in the status of species whose geographic distribution was broad and exceeded the country's territorial limits (i.e. non–endemic species). However, as the national distribution of species that occur exclusively in Brazil (i.e. endemic species) corresponds to their global distribution, we postulated that the status of those species would not vary between lists. In case some endemic species (especially those considered to be threatened) had a different conservation status in each list, we would emphasize the need for special attention the next time their conservation status is assessed.

Material and methods We compiled a database (see table 1s in supplementary material) containing all Brazilian mammal species (regardless of subspecies) according to the Brazilian Red Book of Threatened Fauna (ICMBio/MMA, 2018), their national (obtained from the Brazilian Red Book itself) and global conservation status (obtained from the IUCN Red List of Threatened Species platform, 2019–3 version), and the year in which the species’ status was assessed in each of the lists. In the Brazilian Red Book, however, the pampas deer (Ozotoceros bezoarticus) and some primates were evaluated only at the subspecific level. In these cases, to standardize our analysis, we chose to consider the status of the least threatened subspecies as the status of the species. Using the data found in the 'Geographic Range' section of the IUCN Red List and the Brazilian Red Book, we also added the information of whether a species was endemic to Brazil or not. The lists were then compared according to the conservation status of each species to observe which species differed in status between lists.

We also observed whether each species had the same status on both lists or if it had a lower conservation status (i.e. less threatened) on one of the lists.

For example, if a species was assessed as not threatened (i.e. Least Concern or Near Threatened) by the Brazilian Red Book but as threatened (i.e. Vulnerable, Endangered or Critically Endangered) by the IUCN Red List, we considered it had a lower status in the national list. Similarly, if a species was classified as Critically Endangered in the Brazilian Red Book and as Vulnerable in the IUCN Red List, we considered that it had a lower status in the global list, despite being considered threatened by both lists. We made those comparisons considering four different scenarios: a) all species present in our database; b) only the endemic species; c) only the species considered to be threatened (i.e. species classified as either Vulnerable, Endangered or Critically Endangered) by at least one of the lists; d) species considered, simultaneously, as endemic and threatened. These analyses did not include species that were categorized as Data Deficient in either of the lists.

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Ungulates (1/11)

Xenarthra (2/18)

Carnivora (1/28)

Aquatic Mammals (0/34)

Didelphimorphia (9/50)

Primates (61/108)

Chiroptera (13/175)

All mammals Endemic mammals

350 300 250 200 150 100 50 0

Glires (94/212)

Number of species

Animal Biodiversity and Conservation 44.1 (2021)

Fig. 1. Number of species of Brazilian mammals in each group, with the number of endemic species/ total number of species in parentheses.

Fig. 1. Número de especies de mamíferos brasileños en cada grupo, con el número de especies endémicas respecto al número total de especies entre paréntesis.

In order to better analyze the differences between the lists, we divided the analyzed species into eight groups based on taxonomy (Order rank) and/or ecological characteristics: Aquatic Mammals (comprising cetaceans and sirenians), Carnivora, Chiroptera, Didelphimorphia, Glires (comprising Rodentia and Lagomorpha), Primates, Ungulates (comprising Artiodactyla and Perissodactyla) and Xenarthra (comprising Pilosa and Cingulata). For each group, we compared the proportions of species classified in each conservation status with lists using Fisher's exact test (only the species classified as Near Threatened, Vulnerable, Endangered and Critically Endangered were considered). The analyses were performed in R version 4.0.2.

Results According to the Brazilian Red Book of Threatened Fauna, 680 mammal species were known to occur in Brazil. Since we chose not to include taxa that were not evaluated by the IUCN Red List, as well as those that IUCN considers as subspecies (as opposed to full species), and the candango mouse (Juscelinomys candango), classified as extinct by IUCN, our database comprised 636 species. Additionally, 181 species present in our database (28.5 % of the total) were considered endemic to Brazil. Primates, Chiroptera and Glires made up most of the species, both when considering the complete list and when considering only endemic species (fig. 1). As the tapeti (Sylvilagus brasiliensis) was the only member of the Order Lagomorpha in our database, the high representativeness of Glires in our analyses was due to the richness of rodent species. The Aquatic Mammals group, on the other hand, was the only group in which no species

were considered endemic to Brazil, and three other groups presented a low number of endemic species: Carnivora (the hoary fox, Lycalopex vetulus, was the only endemic species), Ungulates (the small red brocket deer, Mazama bororo, was the only endemic species), and Xenarthra (the three–banded armadillo, Tolypeutes tricinctus, and the maned three–toed sloth, Bradypus torquatus, were the only endemic species).

One hundred and twenty–one species (19.0 % of the total) were considered threatened by at least one of the lists (table 1). Of these, 104 were considered threatened according to the Brazilian Red Book, with 54 (51.9 %) being classified as Vulnerable, 40 (38.5 %) as Endangered and 10 (9.6 %) as Critically Endangered. In the IUCN Red List, 40 species (47.1 %) were classified as Vulnerable, 32 (37.6 %) as Endangered and 13 (15.3 %) as Critically Endangered, totaling 85 threatened species. Considering only the endemic species, 70 (38.7 %) are threatened to some level.

According to the Brazilian Red Book, 23 (39.0 %) of these endemics are classified as Vulnerable, 29 (49.1 %) as Endangered and seven (11.9 %) as Critically Endangered, totaling 59 species. According to the IUCN Red List, 19 species (35.2 %) are classified as Vulnerable, 23 (42.6 %) as Endangered and 12 (22.2 %) as Critically Endangered, totaling 54 species.

Primates and Glires made up most of the threatened species (table 1). Only one species classified as Critically Endangered according to the IUCN Red List did not belong to one of these two groups: the single–striped opossum (Monodelphis unistriata) (Didelphimorphia). The Brazilian Red Book, however, classified one didelphimorph (the black–shouldered opossum, Caluromysiops irrupta) and two cetaceans (the blue whale, Balaenoptera musculus, and the Franciscana dolphin, Pontoporia blainvillei) as Criti-

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Tabla 1. Number of species per group classified under each conservation status according to the Brazilian Red Book (national scale) and the IUCN Red List (global scale).

Tabla 1. Número de especies por grupo clasificadas en cada estado de conservación según el Libro Rojo de Brasil (escala nacional) y la Lista Roja de la UICN (escala global).

All species (Brazilian Red Book)

DD

LC

NT

VU

EN

CR

Aquatic Mammals

8

14

2

3

5

2

Carnivora

1 13 1 12 1 0

Chiroptera

41 126 1 6 1 0

Didelphimorphia

6 38 2 2 1 1

Glires

23 158 5 8 16 2

Primates

9 55 10 14 15 5

Ungulates

3 2 0 6 0 0

Xenarthra

4 10 0 3 1 0

Total (%)

95 (14.9)

416 (65.4)

21 (3.3)

54 (8.5)

40 (6.3)

10 (1.6)

All species (IUCN Red List)

DD LC

NT VU EN CR

Aquatic Mammals

4

19

3

5

3

0

Carnivora

0 18 7 2 1 0

Chiroptera

29 140 4 0 2 0

Didelphimorphia

4 42 2 1 0 1

Glires

38 150 4 5 12 3

Primates

4 56

Ungulates

1 4 1 5 0 0

Xenarthra Total (%)

7 18 14 9

0 12 2 4 0 0 80 (12.6)

441 (69.3)

30 (4.7)

40 (6.3)

32 (5.0)

13 (2.1)

Endemic species (Brazilian Red Book)

DD LC

NT VU EN CR

Aquatic Mammals 0 0 0 0 0 0 Carnivora

0 0 0 1 0 0

Chiroptera

5 5 1 2 0 0

Didelphimorphia

1 5 1 2 0 0

Glires

16 50

Primates

5 25 5 8 13 5

Ungulates

0 0 0 1 0 0

Xenarthra Total (%)

3 8 15 2

0 0 0 1 1 0 27 (14.9)

85 (47.0)

10 (5.5)

23 (12.7)

29 (16.0)

7 (3.9)

Animal Biodiversity and Conservation 44.1 (2021)

83

Tabla 1. (Cont.)

Endemic species (IUCN Red List)

DD LC

NT VU EN CR

Aquatic Mammals 0 0 0 0 0 0 Carnivora

0 1 0 0 0 0

Chiroptera

7 4 1 0 1 0

Didelphimorphia

3 4 1 1 0 0

Glires

32 39

4 5 11 3

Primates

4 22

5 10 11 9

Ungulates

0 0 0 1 0 0

Xenarthra

0 0 0 2 0 0

Total (%)

46 (25.4)

70 (38.7)

cally Endangered nationally. Proportionally, however, the most threatened groups (i.e. the groups in which the proportion of species classified as Vulnerable, Endangered or Critically Endangered was greater) were Ungulates, Carnivora and Primates (with, respectively, 54.5 %, 46.4 %, and 39.8 % of the species considered threatened in at least one of the lists).

Regarding the conservation status of species by group, the Least Concern status was the one in which most of the species of any group were classified. The group Carnivora, however, presented the most significant difference between the lists, with 13 species considered threatened according to the national list but only three according to the global one (table 1). Statistically significant differences between the proportions of species classified in each conservation status (excluding Least Concern) between the two lists were only observed for the groups Carnivora (p–value = 0.001) and Chiroptera (p–value = 0.01). While the Brazilian list has more species classified as Vulnerable, IUCN classifies more species as Near Threatened. Considering only the endemic species (and also excluding species classified as Least Concern), on the other hand, no statistically significant difference was observed between lists for any group. Although the two lists are similar when considering the total number of species classified in each conservation status, further analysis shows that this equivalence may be apparent, since the status of many species varies between the two lists.

Considering the complete lists and excluding the species that are classified as Data Deficient in either assessment, 420 species (85.7 % of the total) had the same conservation status on both lists, whereas 27 (5.5 %) had a lower status according to the national assessment, and 43 (8.8 %) had a lower status on the global list (table 2). However, when only the endemic species were considered, we observed that 100 species (79.4 %) were classified with the same status on both lists, while 16 (12.7 %) had a lower status on the national list and 10 (7.9 %) had a lower status on the global list (table 2). Nevertheless, divergence

11 (6.1)

19 (10.5)

23 (12.7)

12 (6.6)

between lists was even more pronounced when we restricted our analysis to threatened species. In this case, 51 species (47.7 %) had the same conservation status on both lists, 21 (19.6 %) had a lower status according to the national assessment, and 35 (32.7 %) had a lower status on the global list (table 2). Finally, considering the endemic species that are also threatened, 35 species (60.4 %) had the same status on both lists, whereas 13 (22.4 %) had a lower status on the national list and 10 (17.2 %) on the global list (table 2).

Considering the species analyzed by group, the Carnivora, once again, stands out: of the 13 analyzed species considered to be threatened, 11 (84.6 %) had a lower status on the global list and only one (7.7 %) had equal status on both lists (table 2). This pattern was also observed in the Aquatic Mammals group, where six of the 10 analyzed species (60.0 %) had a lower status according to the global assessment. Endemic didelphimorphs also presented a tendency of divergence between lists: only half of the six species considered had the same conservation status on both lists.

The average difference between the years in which species evaluations took place in each list was 2.73 years, with 21 species evaluated in the same year on both lists, six evaluated one year apart, 341 two years apart, 153 three years apart, 17 four years apart, 67 five years apart, 30 six years apart and one that was evaluated seven years apart.

Discussion Although the two lists pursue the same goal (i.e. to evaluate extinction risks of species and classify them accordingly) and use the same categories of threat and the same criteria on their assessments, the conservation status of more than half of the threatened taxa differed between lists, and this variation was more marked in some mammal groups than in others. Since a species threatened nationally may not be threatened globally (Gädendorfs, 2001), one

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84

Table 2. Number of species (out of a total of 490) that have either the same or lower conservation status according to the analyzed lists.

Tabla 2. Número de especies (de un total de 490) que tienen el mismo o diferente estado de conservación de acuerdo con las listas analizadas.

All species Same status

Lower status

Lower status

in both lists

in Brazilian Red Book

in IUCN Red List

Aquatic Mammals

14

1

7

Carnivora

15 1 11

Chiroptera 114 4 3 Didelphimorphia 35

1

5

Glires

148 3 8

Primates

74 17 7

Ungulates

7 0 1

Xenarthra

13 0 1

Total (%)

420 (85.7)

27 (5.5)

43 (8.8)

Endemic species

Same status

Lower status

Lower status

in both lists

in Brazilian Red Book

in IUCN Red List

Aquatic Mammals

0

0

0

Carnivora

0 0 1

Chiroptera

4 2 0

Didelphimorphia 3

1

2

Glires

46 3 6

Primates

45 10 0

Ungulates

1 0 0

Xenarthra

1 0 1

Total (%)

100 (79.4)

16 (12.7)

10 (7.9)

Threatened species Same status

Lower status

Lower status

in both lists

in Brazilian Red Book

in IUCN Red List

Aquatic Mammals

4

0

6

Carnivora

1

1 11

Chiroptera

1 1 3

Didelphimorphia 0

1

4

Glires

13 3 6

Primates

24 15 3

Ungulates

5 0 1

Xenarthra

3 0 1

Total (%)

51 (47.7)

21 (19.6)

35 (32.7)

Animal Biodiversity and Conservation 44.1 (2021)

85

Table 2. (Cont.)

Threatened endemic species

Same status

Lower status

Lower status

in both lists

in Brazilian Red Book

in IUCN Red List

Aquatic Mammals

0

0

0

Carnivora

0 0 1

Chiroptera

0 1 0

Didelphimorphia 0

1

2

Glires

12 3 6

Primates

21 8 0

Ungulates

1 0 0

Xenarthra

1 0 1

Total (%)

35 (60.4)

of the main reasons why the conservation status of many non–endemic species differ between the two lists becomes clear. If we look at mammal groups composed mostly of species with wide geographic distributions, in which rates of endemism are low (such as the orders Carnivora and Cetacea), this becomes even more evident. Indeed, the groups Carnivora and Aquatic Mammals were those with the greatest proportion of threatened species having a lower status in the global list than on the national list. The puma (Puma concolor), for example, can be found across much of the American continent, from Canada to southern Argentina (Nielsen et al., 2015) and it is classified as Least Concern globally, even though it is considered Vulnerable in Brazil. Similarly, the southern right whale (Eubalaena australis) has a circumpolar distribution across the entire Southern Hemisphere (Cooke and Zerbini, 2018) and is also classified as Least Concern globally, but as Endangered in Brazil.

In such cases, the IUCN recommends that national assessments evaluate species as if they were endemic or completely isolated from other populations to obtain a preliminary status. After taking this first step, the status of the species can either be changed or subsequently maintained, considering the possibility of migration of individuals into and out of the region under analysis (IUCN, 2012).

Endemic species, on the other hand, present a more delicate situation. As an endemic species only occurs within a restricted area, its regional population also corresponds to the global one. Therefore, it was expected that the conservation status of endemic species would not differ between national and global lists. However, our analysis has shown that this was not always the case, as the conservation status of 20.6 % of the endemic species and of 39.6 % of the species that were both threatened and endemic varied between lists.

One possible factor responsible for variation in status between lists is the period in which the evaluation of

13 (22.4)

10 (17.2)

the status of taxa was carried out. However, if we consider the time interval between the national and global evaluations of a given species, it is noteworthy that this never exceeded seven years. Furthermore, the Brazilian three–banded armadillo (Tolypeutes tricinctus) was classified as Endangered according to the Brazilian Red Book and as Vulnerable according to the IUCN Red List, despite being endemic to Brazil and both assessments taking place in 2013. This could indicate that the period in which the evaluation was carried out may not be the only reason for the divergences observed, nor the main reason for all of them. Nonetheless, we recognize that changes in the conservation status of a given species can occur within short periods of time, following new publications concerning reassessments of its geographic distribution and of major changes undergone by its habitat (e.g.

Fernandes et al., 2007; Attias et al., 2009; Hirsch and Chiarello, 2012), and taxonomic revisions (especially in cases where a single species is divided into two or more, e.g. Agapow et al., 2004; Nascimento and Feijó, 2017; Ang et al., 2020). The Brazilian Red Book (ICMBio/MMA, 2018) also mentions that more recent and accurate information (especially regarding declines or recoveries of populations) and adjustments in the method itself may be responsible for changes in the conservation status of species, sometimes even resulting in their removal from the list of threatened taxa (i.e. when a species classified as Vulnerable, Endangered or Critically Endangered is re–classified as Least Concern or Near Threatened). This was the case of the humpback whale (Megaptera novaeangliae): previously classified as nationally threatened, the prohibition of whaling activities by the Brazilian government in 1987 resulted in an increase in the number of individuals in national waters (Andriolo et al., 2010; Bortolotto et al., 2016) and led to the re–classification of the species under the Near Threatened status (ICMBio/MMA, 2018).

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Table 3. Endemic species considered to be threatened by at least one of the lists and whose conservation status varied between the assessments: * species with higher conservation risk according to the Brazilian Red Book (national assessment) than with the IUCN Red List (global assessment).

Tabla 3. Especies endémicas consideradas ameanazadas por al menos una de las listas cuyo estado de conservación varió entre las evaluaciones: * especies que tienen mayor riesgo de extinción según el Libro Rojo de Brasil (evaluación nacional) que según la Lista Roja de UICN (evaluación global).

Species

Order

BR status

IUCN status

Marmosops paulensis* Didelphimorphia VU LC Thylamys karimii

Didelphimorphia LC VU

Thylamys velutinus*

Didelphimorphia VU NT

Tolypeutes tricinctus*

Cingulata EN VU

Brachyteles arachnoides

Primates

EN CR

Callithrix kuhlii

Primates

NT VU

Leontopithecus caissara

Primates

EN CR

Mico leucippe

Primates

LC VU

Sapajus flavius

Primates

EN CR

Sapajus xanthosternos

Primates

EN CR

Chiropotes albinasus

Primates

NT EN

Chiropotes utahickae

Primates

VU EN

Lycalopex vetulus*

Carnivora VU LC

Lonchophylla bokermanni Chiroptera NT EN Kerodon rupestris*

Rodentia VU LC

Euryoryzomys lamia

Rodentia

EN VU

Hylaeamys laticeps

Rodentia

LC VU

Rhagomys rufescens

Rodentia

LC VU

Thalpomys cerradensis*

Rodentia VU LC

Thalpomys lasiotis*

Rodentia EN LC

Ctenomys lami*

Rodentia

Trinomys eliasi*

Rodentia VU NT

Sylvilagus brasiliensis

EN VU

Lagomorpha LC EN

A possible additional cause of divergences may be the evaluation process itself. Although both lists are based on expert opinion and follow a strict process to have assessments performed as accurately as possible, it should be considered that there may be a subjective component in assessing the risk of losing species (especially if the methods are not strictly followed). Costa et al. (2005) stated that national lists could also benefit from scientific knowledge generated by unpublished data, including theses, dissertations, local journals, and personal field experience. However, we observed that global lists can also use this type of data to assess species extinction risks. Therefore, some divergences between lists may not be related to the type of publication used, but as we have mentioned, to the data and to the process itself.

Some previous works have attempted to evaluate and compare Red Lists in a similar way to ours.

However, contrary to what we expected, publications focusing on Brazilian mammals are not that common.

Costa et al. (2005) briefly compared the conservation status of threatened Brazilian mammals using the 2003 national list. Nonetheless, in addition to the current list being much more comprehensive than the previous ones, those authors did not carry out as many analyzes as we did. The Brazilian national species list was also compared with the IUCN Red List by Brito et al.

(2010) in a work that addressed various taxa from three other countries besides Brazil: Colombia, China, and the Philippines. Other relevant works dealing with vertebrate groups other than mammals are those of Garcia and Marini (2006), who focused on threatened

Animal Biodiversity and Conservation 44.1 (2021)

Brazilian birds, Morais et al. (2012), who addressed threatened Brazilian amphibians, and Bender et al.

(2012), who focused on Brazilian reef fishes. As in our study, these studies found divergences between lists that needed to be resolved because they could raise doubts on the credibility and usefulness of these important conservation tools.

Nonetheless, there is little point in debating whether one list is better than the other. The main goal of our study was to draw attention to the fact that differences in the conservation status of species may exist between global and national lists and that such differences do not necessarily represent errors or outdated information.

The two lists are based on different spatial scales and, consequently, have distinct potential uses. The national list (i.e. the Brazilian Red Book), at least in Brazil, is the one used to define which species of Brazilian fauna are considered threatened, so that those species can be fully protected under the Brazilian laws, and actions such as their capture, transportation and commercialization be prohibited. The IUCN, on the other hand, aims to show what actions are needed to save species from extinction and where they should be directed (Rodrigues et al., 2006). The IUCN Red List therefore plays a fundamental role in guiding scientific research, influencing allocation of resources for conservation, and informing policies and conventions (especially international ones) (Rodrigues et al., 2006). Both lists also provide useful information about the assessed species, including their geographic range, ecology, natural history, and the main threats to their survival.

It seems reasonable to assume that while regional lists are critical to decision makers within a given country, serving as a basis for the elaboration of national public policies and during the creation of conservation units and other legally protected areas, global lists, which can also guide such actions within a bigger scenario, may function as a 'barometer of life' (an expression the IUCN often uses to describe its own potential) at a global scale. The global list gains a greater visibility than national lists, since it is internationally recognized, and is fundamental for the conservation of species with wide geographic distribution.

Assessing the extinction risk of a species is not an easy task since there are uncertainties and predictions throughout the process. We thus recognize the quality of the work that is done by the authorities responsible for evaluations and recommend that communication and information exchange between authorities and researchers be improved. Perhaps the best way to avoid future divergences between lists (especially for endemic species) would be to undertake a joint assessment between the authorities responsible for the national and global assessments.

It is also extremely important to keep the lists updated so that they always reflect the current status of each species. Standardizing both the type of information and the data itself to be used in those assessments would, if possible, also be of great value, as would be the presentation, by the Brazilian Red Book, of the conservation status of all species at the specific level (as we have mentioned, some species were evaluated only at the subspecific level).

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We also recommend special attention when making future conservation status assessments of species that, although endemic, were classified with different status in each of the lists (see table 3). Additionally, it is important to focus on species classified as Data Deficient since the main reason that leads a species to be classified as such is the lack of adequate information about its distribution and/or its population (ICMBio/MMA, 2018). Thus, the possibility that a given species classified as Data Deficient is threatened should not be overlooked.

Finally, we would like to mention that, while we focused on two main lists in this article, several other lists could be similarly analyzed. The larger the scale, the harder it is to detect and identify eventual regional discrepancies. Thus, state and biome lists, for example, can also be important, especially in a country of continental dimensions like Brazil. Indeed, while a few Brazilian states have their own lists of threatened fauna, most states still lack these (see Brito, 2008).

Analyses at smaller scales may allow more accurate conclusions and, when interpreted together, tend to promote a better understanding of how threatened a species really is. In this regard, some recent studies deserve to be highlighted because they have proposed novel approaches related to conservation status assessments using, for example, data on habitat preference and population abundance (e.g. Santini et al., 2019), or on ecological traits (e.g. Davidson et al., 2009). It is also important to highlight that endemism is a relative measure related to the idea of habitat restriction. Since all species end up being endemic to a certain area (although this area may be large enough to correspond to several countries, for example), care must be taken when using this concept.

Still, we believe that national lists may be easier to incorporate into effective conservation strategies than international lists. Conflicts in conservation policy can be avoided if the evaluation process is not confounded by processes that do not operate within the study area.

Nonetheless, we believe that the use of both global and national lists in a complementary way (or at least the mention, in the publications, of how threatened the studied species is, both at the global level and where the corresponding study took place) tends to make conservation studies and publications more comprehensible, providing readers with a better understanding of how threatened the studied species is.

Acknowledgements We would like to thank H. G. Bergallo, M. L. Lorini, J. C. Ferreira, L. N. dos Santos, V. A. Menezes, M. Almeida–Santos, J. L. do Nascimento and L. Jerusalinsky for the enlightening conversations and suggestions that contributed to the development of this work, L. M. Raposo for helping with the statistical tests, the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the Master's scholarship granted to MCD and all reviewers who participated in the process leading to the publication of this article.

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Seasonal variation in the diet of two predators in an agroecosystem in southern–central Chile A. H. Zúñiga, V. Fuenzalida, R. Sandoval, F. Encina

Zúñiga, A. H., Fuenzalida, V., Sandoval, R., Encina, F., 2021. Seasonal variation in the diet of two predators in an agroecosystem in southern–central Chile. Animal Biodiversity and Conservation, 44.1: 89–102, Doi: https:// doi.org/10.32800/abc.2021.44.0089 Abstract Seasonal variation in the diet of two predators in an agroecosystem in southern–central Chile. In ecosystems, seasonal fluctuations in the availability of resources can promote effects on species with similar trophic requirements, increasing the probability of interspecific competition. This scenario becomes more evident in human–dominated landscapes where homogenization of space can contribute to the shortage of resources, modifying species feeding behavior to an uncertain degree. Understanding how these species modify their feeding habits within the context of habitat transformation is of special interest. We evaluated the diversity of prey and overlap for two predators, the chilla fox Lycalopex griseus and the barn owl Tyto alba, during three seasons in 2018 (winter, spring and summer). The study was based on the analysis of feces and pellets in a landscape with agricultural predominance in Southern–central Chile. We found the chilla fox had a generalist dietary profile, feeding on a broad spectrum of prey, with predominance of lagomorphs and, to a lesser extent, rodents.In contrast, the diet of the barn owl mainly consisted of small rodents, with little variation across seasons. Analyses of dietary overlap showed fluctuations during the periods surveyed, with a maximum value in winter and a minimum value in spring. Variations in the consumption of prey based on their size could facilitate their coexistence in the study area.

Key words: Barn owl, Chilla fox, Diet overlap, Feeding behavior, Non–invasive methods, Trophic isoclines Resumen Variación estacional en la dieta de dos depredadores en un agroecosistema en el centro y sur de Chile. En los ecosistemas, las fluctuaciones estacionales en la disponibilidad de recursos pueden tener efectos en especies con requerimientos tróficos similares, lo cual aumenta la probabilidad de que surja la competencia interespecífica. Esta situación se hace más evidente en ambientes antropizados, donde la homogeneización del espacio puede agudizar la escasez de recursos y modificar el comportamiento alimentario en un grado incierto. De esta manera, resulta de especial interés entender cómo estas especies modifican sus hábitos alimentarios en un contexto de transformación del hábitat. Evaluamos la diversidad de presas y el solapamiento de dos depredadores, el zorro chilla, Lycalopex griseus, y la lechuza blanca o lechuza común, Tyto alba, durante tres estaciones en 2018 (invierno, primavera y verano). Se utilizaron heces y egagrópilas recolectadas en un paisaje con predominancia agrícola en el centro y sur de Chile. En el caso del zorro chilla, se observó un perfil trófico generalista, ya que consumió una amplia variedad de presas, en la que predominaron los lagomorfos y en menor medida, los roedores. En cambio, la lechuza concentró una gran proporción de su perfil alimentario a los pequeños roedores, con pequeñas variaciones entre estaciones. El análisis del solapamiento de las dietas mostró variaciones durante los periodos estudiados, con un valor máximo en invierno y uno mínimo en primavera. La variación en el consumo de presas en función de su tamaño facilitaría la coexistencia de ambas especies en la zona de estudio.

Palabras clave: Lechuza común o lechuza blanca, Zorro chilla, Solapamiento de la dieta, Comportamiento alimentario, Métodos no invasivos, Isoclinas tróficas

ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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Zúñiga et al.

Received: 14 IV 20; Conditional acceptance: 22 VI 20; Final acceptance: 21 XII 20 Alfredo H. Zúñiga, Laboratorio de Ecología, Universidad de Los Lagos, Osorno, Chile.– Víctor Fuenzalida, Consultora Ambientes del Sur, Temuco, Chile.– Rodolfo Sandoval, Red de la Conservación de la Biodiversidad de Nahuelbuta, Contulmo, Chile.– Francisco Encina, Núcleo de Ciencias Ambientales, Universidad Católica de Temuco, Temuco, Chile.

Corresponding author: A. H. Zúñiga. E–mail: zundusicyon@gmail.com ORCID ID: A. H. Zúñiga: 0000–0002–0504–7540; V. Fuenzalida: 0000–0003–3044–9610; R. Sandoval: 0000–0002–1338–7123; F. Encina: 0000–0002–8756–8736

Animal Biodiversity and Conservation 44.1 (2021)

Introduction Ecological communities are sets of species that coexist in a specific time and place (Morin, 2011). Within this organizational level, predators form a group of relevance whose main function is to control prey populations (Hairston et al., 1960). In general, intraguild species and, in particular, predators (Root, 1967), must minimize the co–use of resources between members to avoid effects derived from competition (Schoener, 1974; Fedriani, 1997). For this purpose, species can use several behavioral mechanisms. Food resources are relevant because they promote differentiation of diet between species through types of prey consumed (Zapata et al., 2007). The size of the predator can directly also influence prey size (Gittleman, 1985), deepening segregation. Seasonality, however, could also play a determining role in species interactions, mainly due to variations in the availability of resources. This possibility is evidenced through changes in growth and development in plant species (Rathcke and Placey, 1985) and demographic fluctuations between vertebrate prey (Meserve et al., 1999). Such variations of resources could affect the trophic response of predators, forcing them to modify their trophic spectra (Jaksic, 1989) and consequently to change the relationship of partition of resources between species, affecting their fitness (Wiens, 1977).

Transformation of original habitat has strong effects on biodiversity due to loss of resources for species and limitations on the movement of individuals through patches (Olff and Ritchie, 2002). This issue is important from the view of conservationbecause the increasing human impact on natural habitats affects their persistence (Crooks, 2002; Olifiers et al., 2005).

One of the main ways that habitats are transformed are agroecosystems, where habitat homogenization limits the availability of resources for many species (Benton et al,. 2003). Although predators modify their trophic spectrum in farmlands (Drouilly et al., 2018), the extent to which change occurs may be associated with the local composition of species and their ecological particularities, as these factors will enable their occupancy in this type of environments (Ferreira et al., 2018). Knowledge about how species respond to a changing habitat scenario and their interaction with other species in the community is therefore of special relevant to the implementation of conservation plans.

Chilean native forest is characterized by its unique representation of species in a wide latitudinal distribution, with a high degree of endemism (Armesto et al., 1995). Among the predators that occur in this habitat, chilla fox (Lycalopex griseus) is one of the three extant canids with a wide distribution, ranging from Arica to Tierra del Fuego, at altitudes that vary from sea level to 3,000 m a.s.l. (Iriarte and Jaksic, 2012). This canid has a generalist trophic behavior that includes small vertebrates and arthropods (Simonetti et al., 1984; Martínez et al., 1993; Zúñiga et al., 2008; Muñoz–Pedreros et al., 2018). On the other hand, the barn owl (Tyto alba) is a nocturnal raptor of the family Tytonidae (Pavez, 2004) and its subspecies tuidara is widely represented in Chile.This raptor’s diet is

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mainly carnivorous, with rodents making up the bulk of its food source (Carmona and Rivadeneira, 2006; Muñoz–Pedreros et al., 2016). Although these two species coexist across a broad geographic continuum, little is known about their trophic interaction, their seasonal dynamics and flexibility, and the potential co–use of resources (Jaksic et al., 1996; Correa and Roa, 2005).The purpose of this study was to compare the diet of these two predators in central–southern Chile in a seasonal context. We tested the hypothesis that the trophic spectrum would change for both species at both seasonal and interspecific levels as a way of differentiating the use of resources.

Material and methods The agroecosystem where the study was peformed is located 20 km. east of Mulchén (37º 49' 42'' S – 721º 4' 51'' W), an urban center in central–southern Chile, with an altitude ranging from 120 to 150 m a.s.l.

The climate is humid (Di Castri and Hajek, 1976), with a maximum mean temperature of 25 ºC in summer and a minimum temperature of 4 ºC in winter (Weather Spark, 2020). Rainfall fluctuates between a minimum mean of 21 mm in summer and a maximum mean of 151 mm in winter (Weather Spark, 2020). The vegetation consists of temperate deciduous forest (Gajardo, 1994). The dominant trees species are of the genus Nothofagus, mainly roble (Nothofagus obliqua) and coigüe (Nothofagus dombeyi). Crops in the area are mainly Avena barbata, Lupinus sp. Triticum sp. and Zea mays, with 62 % of the total area surveyed (fig. 1). Mosaics of exotic plantations of Eucalyptus globulus and Pinus radiata make up 28 % of the total area; prairies and shrublands account for a further 6 %, and native forest for 4 %.

Feces and pellets were collected along 1 km line segments during winter and spring 2018 and summer 2019. Feces from chilla foxes were identified using morphometric criteria (Chame, 2003; Muñoz–Pedreros, 2010) and confirmed through the use of camera traps (Kays and Slauson, 2008). Six cameras were placed in the study area, at a distance of 500 m from each other (Zúñiga et al., 2017). In the case of owl pellets, although their recognition was also made by morphological patterns (Muñoz–Pedreros and Rau, 2004), their identification was reinforced through direct observation in a group of trees used by the individuals as a roost.

In the transect where these trees are present, the presence of the fox has also been recorded. Feces and pellets were measured, weighed and stored in paper bags for later analyses in the laboratory.

In the laboratory, the samples (feces and pellet were dried at 60 ºC and examined manually to determine prey. The criteria to recognize rodents was the morphological pattern of skulls and shape of cuticle of hairs (Day, 1966; Reise, 1973; Pearson, 1995), and for birds it was was feathers (Day, 1966).

Reference collections (property of 'Ambientes del Sur consultores') were used for the remaining. The trophic analysis for both species was based on frequencies of relative occurrence of each prey in relation to

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the total observed (Rau, 2000), providing an index of trophic diversity (Levins, 1968). This index (B) is based on the formula B = 1/(∑pi2), where pi is the relative frequency of the prey in the diet. This number fluctuates between 0 and n (n, the number of categories of prey), reflecting the degree of uniformity of prey consumption in relation to the total number of categories observed. Standard deviation of this index was obtained using the Jackknife method (Jaksic and Medel, 1987). Additionally, we calculated a standardized index (Colwell and Futuyma, 1971), which fluctuated between 0 and 1, according to the degree of homogeneity in resources used (0, no homogeneity; 1, total homogeneity). This index allows a better comparison between seasons, assuming the variation of resources during these periods. We assessed the variation in the proportion of each category of prey according to season through the goodness–of–fit test (Sokal and Rohlf 1995), where the average consumption of each category was considered as the expected proportion for the comparisons, due to uneven sample size between seasons.

To quantify the co–use of resources by both species, we used the dietary overlap index (Pianka, 1973).

This index fluctuates between 0 and 1, according to the degree of similarity of consumption of prey (0, no overlap; 1, total overlap). Seasonal variations in the diet of the two predators and the effect of the interaction of one species on the other on their respective diets were analyzed by a hierarchical agglomerative clustering, using Bray–Curtis as an index of similarity.

SIMPROF tests were performed to identify groups in these sources of variation. (Clarke et al., 2014). Additionally, multivariate analysis of variant (Permanova) was carried out to test differences between groups (Quinn and Keough, 2002).

To evaluate the effect of the biomass of prey on the trophic spectrum of the two predators, we calculated the geometric mean of the prey (Jaksic and Baker, 1983).

Likewise, trophic isoclines were applied (Kruuk and De Kock, 1980), allowing us to determine the importance of each prey based on its location in a graphic layout.

This analysis was performed taking all seasons into account. In both cases (geometric mean and isoclines), weights of prey were obtained from Muñoz–Pedreros and Gil (2009) for the case of mammals, and from Norambuena and Riquelme (2014) for birds.

Results A total of 53 feces and 101 pellets were collected over the study period (table 1). Diet for chilla fox consisted of eight categories: small mammals (cricetid and murid rodents), lagomorphs (Lepus europaeus), echimyds (Myocastor coypus), reptiles (lizards), birds (Passeriformes), insects, and vegetable matter.

Categories varied according to season (fig. 2). When diversity of prey was compared between seasons, the proportions of items varied for seven groups (fig. 3).

Differences were non–significant when winter was compared with spring (Pair–wise tests, T = 1.464, p = 0.06), but significant in the other comparisons

(T = 2.428, T = 2.656 for winter vs. summer and spring vs. summer, respectively; p = 0.001 in both cases).

For the barn owl, only six categories of prey were observed, with families of small mammals (Cricetidae and Muridae) predominating and and more pronounced than in the diet of the chilla fox. In terms of diversity, summer was the season with greatest magnitude for chilla fox (table 1). When diversity of prey was compared between seasons, barn owl showed four groups of prey in all seasons (fig. 3), with significant differences between them (Permanova test, Pseudo–F = 5.261; p = 0.001). The proportion of prey differed slightly in both predators in relation to frequency expected across seasons. While in the case of barn owl all categories of prey showed this trend (table 2), in the case of chilla fox only one category of prey was consumed in a random way.

Regarding the differentiation of prey in terms of biomass, during winter and spring the chilla fox (193.17, 485.86 in winter and spring, respectively) showed higher values of geometric mean than barn owl (58.2, 22.73 in winter and spring, respectively).

However, in summer there was a change in this pattern; chilla fox had the lowest value for this parameter (23.61, for chilla fox and 36.21 for barn owl). When the weights of prey were analyzed through trophic isoclines, for chilla fox, the lagomorphs were placed above the upper isocline (fig. 4), while the echymids were placed in an intermediate isocline, and small mammals (murids and cricetids) were placed in the lowest isocline. In contrast, for the barn owl we found that two groups, murids and cricetids, were the most highly represented prey located in the intermediate isocline, while birds and arthropods were placed in the lowest isocline (fig. 5). Reptiles were not incorporated in this layout due to their low frequency in all seasons, The dietary overlap for the different seasons was respectively 0.6, 0.27 and 0.46 for winter, spring,and summer . In these periods, we found a trend of segregation around lagomorphs and rodents. In winter, seven groups of prey consumption were observed, (fig. 6); Pseudo–F = 3.190, p = 0.011), as in spring (Pseudo–F = 7.281, p = 0.001), while in summer, six groups were present (Pseudo–F = 15.873, p = 0.001).

Discussion The dietary composition for both predators differed in relation to sites with less transformed landscape, where native rodents and marsupials were the most common prey (Martínez et al., 1993; Zúñiga et al., 2008; Muñoz–Pedreros et al., 2016). This finding could be explained by the high degree of habitat loss in the study area, where environmental homogeneity would affect the occurrence of the two species.

Both species are present in sites with less human intervention (Muñoz–Pedreros et al., 1990), and their spatial habits are linked to a greater structural complexity (Murúa and González, 1982; Vásquez, 1996). It can be expected that local diversity of prey is affected, with low abundances of native species, such as rodents (Fernández and Simonetti, 2013),

Animal Biodiversity and Conservation 44.1 (2021)

A

Bolivia

B

Paraguay Chile Uruguay Study area

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Santiago de Chile

Chile

Argentina Concepción Study area

200 km C

2 km Fig. 1. Study area: A, sub–continental scale; B, regional scale; C, local scale.

Fig. 1. Zona de estudio: A, escala subcontinental; B, escala regional; C, escala local.

and an increase in exotic species, such as murids and lagomorphs (Jaksic et al., 2002). Despite this, patches of native forest scattered throughout the study area could sustain an important source of specialist prey species. This would allow both predators to maintain a diverse profile of food sources, and it emphasizes the importance of conserving these environments in the long term.

The dietary pattern of both species showed diversity across season. Their respective frequency of consumption which would likely be explained by differences in the reproductive patterns of prey. This has been reported in fall for rodents (González and Murúa, 1983) and in spring for birds and insects (Daan et al., 1989; Peña, 1987). It can therefore be expected that the rate of predation will be greater

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Table 1. Dietary composition of both predators through the sampled seasons. The columns indicates observed abundance of each prey and their percentage.

Tabla 1. Composición de la dieta de ambos depredadores durante las estaciones estudiadas. En las columnas se indican la abundancia observada de cada presa y su porcentaje.

Predators

Chilla fox

Prey

Barn owl

Winter Spring Summer

Winter

Spring Summer

Mammals Rodents, Cricetidae Abrothrix longipilis

2 (6.89)

Abrothtix olivaceus

1 (3.44)

Oligoryzomys longicaudatus 7 (24.13)

1 (3.84) 6 (11.53)

5 (19.23)

7 (13.46) 45 (32.37)

–

1 (1.92)

2 (7.69)

6 (11.53) 13 (9.35)

1 (3.84)

1 (1.92)

5 (19.23)

8 (15.38) 21 (15.10)

Irenomys tarsalis

–

–

–

1 (3.84)

–

–

Phyllotis darwini

–

–

–

–

–

6 (4.31)

–

–

–

4 (15.38)

5 (9.61)

10 (7.19)

7 (26.92)

8 (15.38) 25 (17.98)

Rodents, Muridae Rattus norvegicus Rattus rattus

4 (13.79) 2 (7.69) 7 (13.46)

Rodents, Echymidae Myocastor coypus

1 (3.44) 4 (15.38)

–

–

–

–

8 (27.58) 9 (34.61) 7 (13.46)

–

1 (1.92)

1 (0,71)

7 (26.92) 7 (26.92) 8 (15.38)

2 (7.69)

4 (7.69)

5 (3.59)

Lagomorpha Lepus europaeus Birds Unidentified birds Reptiles Liolaemus sp.

–

2 (7.69)

–

–

2 (3.84)

–

Cratomelus armatus

–

–

5 (9.61)

–

10 (19.23)

9 (6.4)

Brachysternus viridis

–

–

–

–

1 (1.92)

–

Unidentified insect

–

–

13 (25)

–

–

2 (1.4)

–

–

4 (7.6)

–

–

2 (1.43)

18

18

17

26

27

48

Insecta

Vegetables Vegetal tissue Total scats/pellets Dietary breadth (β) Standardized niche (Bsta)

5.8 ± 1.54 4.33 ±1.77 6.59 ±1.37 0.58

0.55

during these seasons. Likewise, the non–random pattern of frequencies of consumption observed in the goodness–of–fit tests illustrated the population changes of the respective types of prey. This finding should be taken with caution, however, and further studies on the demographic pattern of these species in human dominated landscapes are needed. In the case of chilla fox, the high consumption of cricetids in winter increased even further in summer, suggesting continuity in their reproductive dynamics throughout

0.69

5.82 ±1.43 8.24 ±1.08 5.50 ±2.05 0.80

0.65

0.45

the seasons. This possibility could be explained by interannual variations in population sizes, where demographic dynamics of rodents can fluctuate year to year (Murúa et al., 1986), expanding periods of greatest abundance, and allowing their greater capture by predators. On the other hand, murids have a broad spatial pattern, with intra–annual reproductive dynamics that would facilitate their consumption over the seasons (King et al., 1996; Douangboupha et al., 2009). Their low frequency of consumption, however,

Animal Biodiversity and Conservation 44.1 (2021)

95

40

Chilla fox

35

Percentage

30 Winter Spring Summer

25 20 15 10 5 0

Cric

Mur

Lag Echim Bd Prey categories

Lz

Ins

70

Veg.tis

Barn owl

Percentage

60 50

Winter Spring Summer

40 30 20 10 0

Cric

Mur

Lag Bd Lz Prey categories

Ins

Veg.tis

Fig. 2. Percentage representation of the prey captured by chilla fox Lycalopex griseus and barn owl Tyto alba in the study area, through the sampled seasons, year 2019: Cric, cricetids; Mur, murids; Lag, lagomorphs; Bd, birds; Lz, Lizards; Ins, insects; Veg.tis, vegetable tissues Fig. 2. Representación del porcentaje de las presas capturadas por el zorro chilla Lycalopex griseus y la lechuza común Tyto alba en la zona de estudio, durante las estaciones estudiadas del año 2019: Cric, cricétidos; Mur, múridos; Lag, lagomorfors; Bd, aves; Lz, lagartos; Ins, insectos; Veg.tis, tejidos vegetales.

could be attributed to changes in the use of space, minimizing the likelihood of encounters.

The consumption of lagamorphs was greater than previously detected (Zúñiga et al., 2018a), suggesting the progressive incorporation of this group into the dietary spectrum with replacement of native prey (Simonetti, 1986; Novaro et al., 2000). This pattern has also been found in other fox species, where periods of trong population growth of hares was linked to high rates of consumption by red foxes (Vulpes vulpes) and lower rates of predation on smaller mammals (Goszczyński and Wasileski, 1992). The absence of statistical differences in the frequency of consumption between seasons suggests a certain degree of regular consumption, with a proportion that did not vary along across seasons (Jaksic, 1989).

Nevertheless, this observation should be examined

with caution because it is necessary to monitor their abundance. It is important to note that apart from cougar (predators that are occasionally detected in the study area) records of other mammal predators that capture lagomorphs are lacking. Predation pressure on lagomorphs could be low due to the low number of predators, which would account for a low impact on its population size and allowing chilla fox to consume them with frequency across the the seasons. Reports on the demographic fluctuation of hares during inter–annual periods (Wasilewski, 1991; Sokos et al., 2016) makes it necessary to systematically monitor hare populations so as to determine how the trophic response of chilla fox is affected.

Seasonal variation in the diet of the barn owl also showed changes in the composition of prey, although their dependence on small mammals was

Zúñiga et al.

96

A

Resemblance: S17 Bray–Curtis similarity 2D Stress: 0.24

50

O.long Bd

A.long

MSD2

A.oliv Veg.tis

0

Arthr R.r

–50

–150

B

Lz

Lp.eu

Cr

Echym

–100

SIMPROF Winter Spring Summer

–50

0 MSD1

50

100 2D Stress: 0.24

50

R.n

A.oliv

MSD2

Bd

0

Arthr Lp.eu Ph.d Lz A.long Veg.tis Br Cr

O.long

Arthr

–50

SIMPROF Winter Spring Summer

R.r

–100

–50

0 MSD1

50

100

Fig. 3. Dissimilarities represented by Metric multidimensional scaling (MDS) between the types of prey consumed seasonally by chilla fox Lycalopex griseus (A) and barn owl Tyto alba (B): A.long, A. longipilis; A.oliv, A. olivaceus; Arthr, arthropods; Bd, birds; Br, Brachisternus viridis; Cr, Cratomelus armatus; Echym, Echymids; Lp.eu, Lepus europaeus; Lz, lizards; O.long, Oligoryzomys longicaudatus; Ph.d, Phyllotis darwini; R.n, Rattus norvegicus; R.r, Rattus rattus; Veg.tis, vegetable tissue.

Fig. 3. Diferencias representadas mediante el escalamiento multidimensional métrico (MDS en su sigla en inglés) entre los tipos de presa consumidos de forma estacional por el zorro chilla Lycalopex griseus (A) y la lechuza común Tyto alba (B): A.long, A. longipilis; A.oliv, A. olivaceus; Arthr, artrópodos; Bd, aves; Br, Brachisternus viridis; Cr, Cratomelus armatus; Echym, equímidos; Lp.eu, Lepus europaeus; Lz, lagartos; O.long, Oligoryzomys longicaudatus; Ph.d, Phyllotis darwini; R.n, Rattus norvegicus; R.r, Rattus rattus; Veg.tis, Tejido vegetal.

more marked, as evidenced in the high frequency of capture. Even though barn owl consumption of cricetidae was consistent with previous reports (Correa and Roa, 2005; Zúñiga et al., 2018b), differences were observed in terms of diversity across seasons.

These differences could be explained by the incorporation of other groups of cricetids associated with native forest. This is the case of the mice Chilean Irenomys tarsalis and Phyllotis darwini, which are in the limit of southern distribution (Muñoz–Pedreros

and Gil, 2009). However, their abundances reflect a low contribution to the total dietary spectrum. It is therefore necessary to determine the population dynamics of these two species to understand their real contribution across seasons. On the other hand, the appearance of murids in the diet would be associated with opportunistic feeding behavior on small rodents due to the occurrence of this group in sites with low forest cover (Teta et al., 2012). The low consumption of hares would be explained by their size. The fact

Animal Biodiversity and Conservation 44.1 (2021)

97

Table 2. Values of chi–square analysis (x2) and their respective statistical significance (p) for comparisons of frequencies of prey consumption through the seasons surveyed.

Tabla 2. Valores del análisis de la x2 y su significación estadística (p) respectiva para comparaciones de frecuencias de consumo de presas durante las estaciones estudiadas.

Chilla fox

x2

Cricetids Murids

Barn owl p

x2

p

17.47

0.0002

53.33

< 0.0001

15.23

0.0005

35.67

< 0.0001

Lagomorphs

1.81

0.404

121.65

< 0.0001

Echymids

47.57

< 0.0001

–

–

Birds

17.17

0.0002

61.47

< 0.0001

Arthropods

104.94

< 0.0001

73.65

< 0.0001

that they are usually larger than this raptor (Pavez, 2004) suggests an age–based segregation for their capture, with juveniles being more vulnerable, as has been reported for rabbits (Oryctolagus cuniculus) in Central Chile (Simonetti and Fuentes, 1983).

Differences in the co–use of resources between the two predators across the seasons account for changes in responses used under a scenario of fluctuation of

70

resources, where prey size appeared to be an important factor to minimize trophic overlap. Likewise, although the relatively high trophic overlap observed in winter suggests that small mammals were a critical resource for both species, consumption of larger prey seems to favor the partitioning of resources. The presence of lagomorphs in the upper isocline in the case of chilla fox highlights the importance of this prey in

Lag

Chilla fox

60

Biomass (%)

50 40 30 20 10 0

50 %

Ech Art

20 %

Bd Mur Cric 10 20 30 Frequency (%)

40

5 % 1 % 50

Fig. 4. Trophic isoclines for prey consumed by chilla fox Lycalopex griseus in the study area: Art, arthropods; Bd, birds; Cric, cricetids; Ech, echymids; Lag, lagomorphs; Mur, murids.

Fig. 4. Isoclinas tróficas de las presas consumidas por el zorro chilla Lycalopex griseus en la zona de estudio: Art, artrópodos; Bd, aves; Cric, cricétidos; Ech, equímidos; Lag, lagomorfos; Mur, múridos.

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98

Barm owl

50 Lag 40 Biomass (%)

Mur 30

50 %

20 Cric 10

0

20 %

Art Bd 10

20 30 40 Frequency (%)

50

5 % 1 % 60

Fig. 5. Trophic isoclines for prey consumed by Barn owl Tyto alba in the study area: Art, arthropods; Bd, birds; Cric, cricetids; Lag, lagomorphs; Mur, murids.

Fig. 5. Isoclinas tróficas de las presas consumidas por la lechuza común Tyto alba en la zona de estudio: Art, artrópodos; Bd, aves; Cric, cricétidos; Lag, lagomorfos; Mur, múridos.

the trophic spectrum, considering that the weight of L. europaeus is greater than the rest. On other hand, the presence of Myocastor coypus, whose size is about to 10 kg (Muñoz–Pedreros and Gil 2009), similar to chilla fox, suggests that these records would be the resultof scavenging. Such scavenging can be explained by the occasional presence of Puma concolor (60 kg) in the study area, which has consumption reports of M. coypus (Iriarte and Jaksic, 2012; Zúñiga and Muñoz–Pedreros, 2014), contributing therefore to the food subsidy of other predators (Wilson and Wollkowich, 2011). In the case of the barn owl, the presence of both murid and cricetid rodents in the intermediate isocline accounts for the importance of both these groups in the diet, despite their different spatial habits. This can be explained due to the energy requirements of the barn owl –a minimum of 55g/day (Hamilton and Neill, 1981)– and its flexibility to capture rodents, with variations in selectivity of species according to seasonal availability (Tores et al., 2005).

It should also be noted, however, that although both predators consumed arthropods, the taxonomic level achieved may be underrepresentative of the supply in the environment (Greene and Jaksic, 1983); caution is therefore called for regarding the diversity in types of prey (Peña, 1987).

The use of space is a key aspect in the ecological differentiation of the two predators. The lower number of feces of chilla fox collected in relation to barn owl pellets suggests that this canid uses the agroecosystem in a marginal way, with extensive roaming in

search of food in sites adjacent to the study area.

This possibility is supported by reports that account for a low frequency of use of this habitat, in relation to native forest and commercial plantations (Zúñiga et al., 2009) and their home range (Silva–Rodríguez et al., 2010). In contrast, barn owl have a greater degree of territoriality than chilla fox because their home range smaller (Tomé and Valkarna, 2001; Hafdzi et al., 2003). Particularities about the type of movement associated with their hunting activities (Massa et al., 2015) could favor a finer degree of differentiation between the two predators.

The low geometric mean observed for chilla fox in summer has its minimum value in relation to other seasons, showinga noticeable decrease in the size of the prey consumed. This could be due to low availability of large prey, compensated only by a high consumption of arthropods. This illustrates the different strategies of the two predators. This diet is considered as suboptimal for the species because its low biomass contribution would not support its energy requirements, as has been reported for its congeneric culpeo fox, Lycalopex culpaeus (Silva et al., 2005).

The low abundance of rodents suggests the forced displacement of chilla fox towards patches with greater availability of resources. Considering that the study area is a mosaic of agricultural landscape with forest plantations and native forest, there is a high probability that these canids may converge with domestic dogs, which could interfere in their spatio–temporal patterns (Silva–Rodríguez et al., 2010). Knowledge about the

Animal Biodiversity and Conservation 44.1 (2021)

99

Standardise samples by total Resemblance: S17 Bray–Curtis similarity

Winter

2D Stress: 0.25

MSD2

50

0

O.long A.oliv Bd Veg.tis Echym

Lp.eu

I.tr Arthr

R.r

R.n

–50

A.long

SIMPROF Chilla fox Barn owl

–100

Spring

–50

0 MSD1

50

100 2D Stress: 029

MSD2

50

0

O.long

Echym

Lz

Bd

Br

R.r

Arthr R.n

Cr A.long

–50

Lp.eu A.oliv

SIMPROF Chilla fox Barn owl

–100

–50

0 MSD1

Summer

50

100 2D Stress: 0.22

R.r

MSD2

50

Ph.d

0

Veg.tis Arthr Lp.eu

A.long

Bd O.long

Cr A.oliv R.n

–50

SIMPROF Chilla fox Barn owl

–100

–50

0 MSD1

50

100

Fig. 6. Dissimilarities represented by Metric multidimensional scaling (MDS) between the types of prey consumed by chilla fox Lycalopex griseus and barn owl Tyto alba (both species together) in the study area, across the seasons surveyed: A.long, A. longipilis; A.oliv, A. olivaceus; Arthr, arthropods; Bd, birds; Br, Brachisternus viridis; Cr, Cratomelus armatus; Echym, echymids; I.tr, I. tarsalis; Lp.eu, Lepus europaeus; Lz, lizards; O.long, Oligoryzomys longicaudatus; Ph.d, Phyllotis darwini; R.n, Rattus norvegicus; R.r, Rattus rattus; Veg.tis, vegetable tissue.

Fig. 6. Diferencias representadas mediante el escalamiento multidimensional métrico (MDS en su sigla en inglés) entre los tipos de presa consumidos por el zorro chilla Lycalopex griseus y la lechuza común Tyto alba (ambas especies juntas) en la zona de estudio, en las estaciones estudiadas: A.long, A. longipilis; A.oliv, A. olivaceus; Arthr, arthropods; Bd, birds; Br, Brachisternus viridis; Cr, Cratomelus armatus; Echym, echymids; I.tr, I. tarsalis; Lp.eu, Lepus europaeus; Lz, lizards; O.long, Oligoryzomys longicaudatus; Ph.d, Phyllotis darwini; R.n, Rattus norvegicus; R.r, Rattus rattus; Veg.tis, tejido vegetal.

100

spatial ecology in this area, considering the potential conflict due to the proximity to human settlements, is of special importance for the implementation of conservation strategies. In conclusion, although the two studied species shared a high proportion of prey species, their rate of consumption varied over the seasons in the study period. Differences in abundance of prey, added to the particularities of the predators’ use of space, resulted in variations in the trophic overlapping. Future research should focus on whether the selectivity pattern differs between the two species.

Acknowledgements To the three reviewers that helped to improve the manuscript considerably.

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A plastic device fixed around trees can deter snakes from predating bird nest boxes H. Navalpotro, D. Mazzoni, J. C. Senar

Navalpotro, H., Mazzoni, D., Senar, J. C., 2021. A plastic device fixed around trees can deter snakes from predating bird nest boxes. Animal Biodiversity and Conservation, 44.1: 103–108, Doi: https://doi.org/10.32800/ abc.2021.44.0103 Abstract A plastic device fixed around trees can deter snakes from predating bird nest boxes. Several devices have been designed to prevent predation in nest boxes by mammals and birds. Although snakes are one of the most common predators in cavity–nesters, they have always been difficult to deter. Here we tested a method originally designed to avoid predation by tree–climbing mammals. To prevent snakes from climbing trees and predating on nest boxes, we wrapped a transparent acetate sheet of 80 cm high around tree trunks below a sample of 40 nest boxes used by tits. The acetate sheets were secured with duct tape. The remaining nest boxes (N = 74) in the study area were left as controls. The predation rate in the experimental nest boxes was 20 % and 2 % in control boxes. This method can be useful to increase bird breeding success, improving both the effectiveness of resources to obtain scientific data and the breeding success of endangered species.

Key words: Nest protectors, Snake predation, Nesting success, Nest boxes, Mediterranean Resumen Una lámina de plástico fijada alrededor de los árboles puede impedir que las serpientes ataquen las cajas nido de las aves. Se han diseñado varios artilugios para impedir que los mamíferos y las aves ataquen las cajas nido. A pesar de que las serpientes son uno de los depredadores más comunes de las aves que anidan en cavidades, siempre han sido difíciles de evitar. En el presente artículo probamos un método originalmente concebido para evitar que los mamíferos trepen a los árboles. Para impedir que las serpientes trepen a los árboles y ataquen las cajas nido, utilizamos una lámina de acetato transparente de 80 cm de altura para envolver los troncos de los árboles en los que se ubicaba una muestra de cajas nido (N = 40) utilizadas por carboneros y herrerillos. Las demás cajas nido (N = 74) se dejaron como control. La tasa de depredación en los nidos de control fue del 20 % y solo del 2 % en las cajas nidos experimentales. El método puede ser útil para aumentar el éxito reproductivo de las aves y, por lo tanto, para aumentar la eficacia de los recursos dirigidos a obtener datos científicos, y el éxito reproductor de las especies en peligro de extinción.

Palabras clave: Protectores de nidos, Depredación por serpientes, Éxito de anidación, Cajas nido, Mediterráneo Received: 13 I 21; Conditional acceptance: 20 I 21; Final acceptance: 3 II 21 Helena Navalpotro, Daniele Mazzoni, Juan Carlos Senar, Museu de Ciències Naturals de Barcelona, Castell dels Tres Dragons, Parc Ciutadella, Passeig Picasso s/n., 08003 Barcelona, España (Spain).

Corresponding author: J. C. Senar. E–mail: jcsenar@bcn.cat ORCID ID: H. Navalpotro: 0000-0003-3730-8845; D. Mazzoni: 0000-0001-7342-4857; J. C. Senar: 0000-0001-9955-3892

ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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Introduction Cavity–nesting passerines are commonly used as research subjects in many ecological studies because they can be monitored using nest boxes.

One of the main causes of reproductive failure in these species is nest predation (Nilsson, 1984; Møller, 1989; Coxet et al., 2013). The most common predators in nest boxes are usually mammals such as mustelids (Møller, 1989; Sorace et al., 2004; Suzuki, 2015), squirrels (Willson, Santo and Sieving, 2003), other birds (e.g. woodpecker) (Nilsson, 1984; Skwarska et al., 2009), and snakes (Weatherhead and Blouin–Demers, 2004; Weatherhead et al., 2010; Degregorio et al., 2015).

Several devices have been designed to deter predation in nest boxes by mammals and birds (Yamaguchi et al., 2005; Bailey and Bonter, 2017; Stojanovic et al., 2019). However, avoiding predation by snakes is more challenging due to their ease in hanging and entering through tubes or other structures. For nest boxes hanging from a branch, a cone–shaped piece of plastic put on the box can sometimes be effective (Bailey and Bonter, 2017). When the nest boxes are placed on a metal pole, a stovepipe baffle or cone baffle placed on the metal structure has also shown to prevent climbing snakes from reaching the box (Bailey and Bonter, 2017). However, when nest boxes are located on the tree trunk and near the ground, no simple device seems available.

Keo et al. (2009) fixed a plastic device around the tree from the tree base to a height of 1.5 m to prevent mammals from climbing the trunk and reaching the

nest box. They authors observed that breeding success increased and suggested that the method could also be useful to prevent snake predation. However, no quantitative data were presented on the effectiveness of the method to specifically deter snakes.

The aim of this paper was to test the effectiveness of the Keo et al.'s method (2009) to avoid nest box predation by snakes. To prevent snake climbing and consequent predation we covered tree trunks below a sample of nest boxes with a transparent acetate sheet of 80 cm in height. This sheet was attached to the trunk with duct tape. The other trees in the study area were left as controls.

The experiment was carried out in a Mediterranean forest near the city of Barcelona, where two snake species may typically be responsible for bird nest predation: Montpellier snakes (Malpolon monspessulanus) (Gutiérrez, 1994; Feriche et al., 2008) and ladder snakes (Zamenis scalaris) (Pleguezuelos et al., 2007). In our study area, both species have been reported to predate great tit and blue tit nestlings (Parus major and Cyanistes caeruleus) (fig. 1). Our results showed this device was highly effective in preventing predation by snakes, but the findings also identified additional points that should be taken into account.

Material and methods The study was carried out in the field station of 'Can Catà' within the Parc Natural de Collserola (Cerdanyola, Barcelona, NE of the Iberian Peninsula,

Fig. 1. Graphic documentation on the two snake species typically predating on tit nests in our study area while we were recording tit nest attendance. On the left, we have an adult male Montpellier snake predating on a great tit chick after capturing it in the nest. On the right, we have an adult ladder snake entering the nest box, which it later predated.

Fig. 1. Documentación gráfica de las dos especies de serpiente que atacaron con más frecuencia los nidos de carboneros y herrerillos en nuestra zona de estudio mientras grabábamos la presencia de aves en los nidos. A la izquierda, tenemos un adulto de culebra bastarda o de Montpellier depredando a un pollo de carbonero común tras capturarlo en el nido. A la derecha, tenemos un adulto de culebra de escalera entrando en la caja nido que posteriormente atacó.

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45º 27' N, 20º 8' E). The area is situated at the bottom of a valley of sclerophyllous forest dominated by holm oaks (Quercus ilex, 67 %) and, to a lesser extent, oaks (Quercus cerrioides, 17 %) and aleppo pines (Pinus halepensis, 16 %), with a highly developed understory. Aleppo pine was the predominant species on most of the hills (54 %), surrounded by shrubs and oak species (holm oaks: 31 %, oaks: 14 %). The altitude of the area ranges from 80 to 225 m above sea level. Additional information about the study area is given in Navalpotro et al. (2016). The 'Can Catà' field station has 183 titmice nest boxes distributed throughout an area of 80 ha. The size of the nest boxes is 21 cm x 32 cm with an entrance hole diameter of 30 mm. To minimize damage by woodpeckers, the wooden nest boxes are 3 cm thick. Nest boxes also include a cylindrical PVC tube of 10 cm in length and 5 cm (in diameter) designed to protect the entrance from mammal predators (such as mustelids or genets).

Nest boxes are located directly on the trunks of the trees approximately 1.30 m above ground level, and at least 25 m apart from each other.

The predator exclusion method to increase the breeding success of our studied species was applied during the spring of 2018. A transparent plastic (acetate sheet) 0.8 m in height and 1 mm thick was attached with duct tape around the trunk. After clearing the branches and bushes in a circle of 1 m radius around the tree, we placed the plastic belt below the nest box to prevent snakes from climbing up (see fig. 2). We randomly protected a sample of the occupied nest boxes (n = 40) for use as experimental boxes. The remaining occupied nest boxes (n = 74) were used as controls. The experimental nest boxes were spread throughout the study area to avoid altitude and other environmental collateral effects related to location. The device was installed on the trunk of the 40 trees as soon as we detected egg laying to prevent predation on eggs or incubating females.

All nest boxes were monitored 2–3 times a week for laying date, hatching date, number of eggs, number of chicks, and other observations. We checked chicks and broken or missing eggs for signs of predation.

Normally, snake predation is characterized by an intact nest with missing chicks or eggs because the snake ingests the prey without damaging the nest, while mammals normally disrupt the whole nest (Kibler, 1969; Christman and Dhondt, 1997; Chen et al., 2020). Nest boxes were also videotaped from inside the box to record parental investment (see Pagani–Núñez and Senar (2013) for details). This further allowed us to confirm the main nest predators in the study area (fig. 1).

Great tit and blue tit reproduction started on March 31st (first egg laid) and ended on July 10th 2018 (last fledged chick). The plastic was removed once the breeding season ended.

Statistical analyses were carried out using a log–linear analysis of frequency tables which allows to test for the interaction between more than two categorical variables (Agresti, 2019). Factors used were species (great tit vs blue tit), outcome (fledged or predated), and treatment (experimental or control).

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Fig. 2. Predator–exclusion plastic sheet (marked with white arrow) used to prevent access by snakes to nest boxes attached to tree trunks.

The plastic was fixed with duct tape around the trunk, generally in the upper part. Photo

by J. C. Senar.

Fig. 2. Cinturón de plástico contra depredadores utilizado para impedir el acceso de las serpientes a las cajas nido instaladas en árboles. El plástico se fijó alrededor del tronco con cinta adhesiva, generalmente en la parte superior.

Fotografía de J. C. Senar.

Results We video–recorded 13 instances of successful nest predation in our nest boxes (2013–2020), eight by Montpellier snakes and five by ladder snakes. We also recorded some attempts by genets Genetta genetta, stone martens Martes foina and jays Garrulus glandarius, but none of these were successful.

Results showed a significant difference between the outcome of nest boxes with plastic and those without plastic (x2 = 6.54, p = 0.01, table 1). There was only one predation event in the nest boxes with protective plastic (experimental), but 15 nest boxes in the control group were predated. Twenty percent of the nest boxes without plastic were predated whereas only two percent of protected nests were predated

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Table 1. Results of a log–linear analysis testing for partial associations between the variable species (great tit vs. blue tit), outcome (fledged or predated), and treatment (experimental or control). Only interactions between outcome and treatment are significant.

Tabla 1. Resultados de un análisis log–lineal para establecer asociaciones parciales entre la variable de la especie (carbonero común o herrerillo común), el resultado (pollos emplumados o depredados) y el tratamiento (experimental o control). Solo son significativas las interacciones entre el resultado y el tratamiento.

Tabla 2. Tabla de contingencia en la que se relaciona el tratamiento (plástico y control) y el resultado (pollo emplumado y depredado) de ambas especies. Frecuencias esperadas entre paréntesis.

Fledged Predated

df

x2

p

Species x outcome

1

0.17

0.68

Species x treatment

1

0.15

0.70

Outcome x treatment

1

6.54

0.01

Sp x out x treat

1

0.04

0.84

Table 2. Contingency table relating treatment (plastic and control) and outcome (fledged and predated) of both species. Expected frequencies are shown in parentheses.

(table 2). There was no significant three–way interaction, indicating that predation did not vary according to tit species in any of the treatments (x2 = 0.04, p = 0.84, table 1).

Discussion The results of this study indicate that wrapping the tree trunk with acetate sheeting decreased snake predation by preventing snakes from climbing up to nest boxes. The case in which we failed to deter snake predation was because the tree with the nest box was very close to another tree, so that the snake could have climbed this adjacent tree and then jumped to the nest box on the nearby tree. This also happened twice in 2020; using a camera trap, we videotaped how a Montpellier snake jumped from a neighboring tree to the nest box in an adjacent tree (see supplementary material). This observation suggests plastic sheeting should also be placed around nearby trees if it is suspected snakes could climb these to reach the nest box. In 2020, when we were videotaping parental effort with cameras located within the nest boxes (see e.g. Pagani–Núñez and Senar, 2014), we also recorded three occasions on which the snakes used the cable that connected the camera placed inside the nest box with the battery located at the base of the tree to climb up to the nest box. This indicates that any structure close to the tree trunk should also be covered with the plastic.

All the instances we video recorded of predation in our nest boxes were by Montpellier and ladder snakes (fig. 1). This not only confirms that the cylindrical tube at the entrance to the nest box was effective to protect the box from mammalian and bird predators,

Plastic

Control

39 (34)

59 (64)

1

(6)

15 (10)

but also confirms that these two snake species were responsible for the predation instances recorded in our area. The horseshoe snake Hemorrhois hippocrepis is also a common nest predator in Spain (Suárez et al., 1993), but although it was once recorded in the Collserola mountains (Cano et al., 2013), and hence it should appear in our area according to atlas data (Pleguezuelos and Feriche, 2002), it has never been recorded by Collserola Park biologists (F. Llimona, pers. comm.) and we have never recorded it in Can Catà field station.

Snakes are one of the main nestling predators in any habitats (Weatherhead and Blouin–Demers, 2004). Predation by snakes in any given locality increases with time, since it has been observed that snakes have long–term spatial memory (Miller, 2002).

In a scenario of climate warming, these reptiles will likely increase their above–ground foraging (Le Galliard et al., 2013; Capula et al., 2016). Consequently, in Mediterranean areas, where climate warming is predicted to have a higher impact (Gao and Giorgi, 2008), snake predation will have an increasing impact on cavity–nesters. Any tactics to deter snake predation may therefore be increasingly demanded.

These methods can be useful to avoid nest failures, and thus, increase the effectiveness of resources to obtain scientific data and to increase breeding success on endangered species (Keo et al., 2009).

We therefore strongly encourage researchers to try the proposed methods in different habitats with significant populations of bird–nest predators to test the generality of the method.

Acknowledgements We are grateful to the Associate Editor of Animal Biodiversity and Conservation and two anonymous referees for their useful comments to improve the manuscript. This work was supported by funds from The Ministry of Economy and Competitiveness (MINECO), Spanish Research Council to JCS (CGL-

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2016-79568-C3-3-P). We thank the late Leopoldo Gil and his family, for their constant support of our work, and for allowing us to sample birds in the Can Catà forest area. We also thank Lluïsa Arroyo, Marta Olivé, Mónica Navarro and Francesc Uribe for their help in the field and to Carolyn Newey for improving the English.

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Supplementary material

Video. The two trees, one of which contains a nest box, were protected with a plastic around the trunk to prevent snakes from climbing it and preying on the great tit chicks inside the nest box. However, the Montpellier snake managed to climb the other nearby tree, and leaning on the photo trap box, it tried to jump over the nest box. The recording does not show us how exactly it managed to get to the nest box, but finally it is clear that it reached it and preyed on the chicks it contained. At the end of the recording, it is observed how the snake hanged down and when it came down from the nest box it avoided touching the plastic that covered the trunk.

Vídeo. Los dos árboles, uno de los cuales contiene una caja nido, se protegieron con un plástico alrededor del tronco para evitar que las serpientes pudieran trepar por él y depredar a los pollos de carbonero común que había dentro de la caja nido. Sin embargo, la serpiente de Montpellier consiguió trepar por el otro árbol cercano y, apoyándose en la caja de foto trampeo, intentó saltar sobre la caja nido. En la grabación no se observa exactamente cómo consiguió llegar hasta la caja nido, pero queda claro que al final lo logró y depredó a los pollos que contenía. Al término de la grabación, se observa que la serpiente se descolgó y que, al bajar de la caja nido, evitó tocar el plástico que cubría el tronco. https://youtu.be/4RQbXNaQ6IU

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Interspecific sexual selection, a new theory for an old practice: the increase of artificial biodiversity through creation of modern, standardized breeds J. J. Negro, M. C. Blázquez, R. Fernández–Alés, Á. Martín–Vicente Negro, J. J., Blázquez, M. C., Fernández–Alés, R., Martín–Vicente, A., 2021. Interspecific sexual selection, a new theory for an old practice: the increase of artificial biodiversity through creation of modern, standardized breeds. Animal Biodiversity and Conservation, 44.1: 109–115, Doi: https://doi.org/10.32800/abc.2021.44.0109 Abstract Interspecific sexual selection, a new theory for an old practice: the increase of artificial biodiversity through creation of modern, standardized breeds. Darwin set the pillars of organismic evolution when he defined natural and sexual selection in the 19th century. Concurrently, a frenzy of selective breeding programmes, generally supported by the wealthy and aristocratic, gave rise to novel breeds of plants and animals at a rate that was previously unforeseen. Since then, breeds selected over millennia and adapted to local conditions began to disappear or were threatened with extinction, being substituted by these new, standardized breeds. It is of interest to explore how new breeds emerged and what the main criteria of the founders of these breeds were. Darwin seemed to be unaware that his contemporaries were practicing a form of interspecific sexual selection responsible for the fixation of exaggerated traits, often plainly ornamental, in the new breeds they intended to create. Parent animals were chosen by individuals who were following particular goals, often with aesthetic criteria in mind. Here we investigated who were the founders of modern breeds in five domesticated species (dogs, cats, pigs, horses and cattle), as very often a single person is credited with the creation of a breed. We found information on founders of 459 breeds, 270 of which were created after 1800. Interestingly, for these species, breed creation is overwhelmingly attributed to men. In the wild, however, the choice of mate is usually performed by the female of a species and thought to be adaptive. Breeders in the Victorian era, nevertheless, lacked such adaptive skills and had little scientific knowledge. The selection of individuals with an extreme expression of the desired traits were often close relatives, resulting in high inbreeding and a variety of genetic disorders.

Key words: Sexual selection, Artificial selection, Pleiotropic effects, Inbreeding, Domestication Resumen Selección sexual interespecífica, una nueva teoría para una vieja práctica: el aumento de la biodiversidad artificial a través de la creación de razas modernas estandarizadas. Darwin sentó los pilares de la evolución de los organismos cuando definió la selección natural y sexual en el siglo XIX. Al mismo tiempo, el entusiasmo por los programas de cría selectiva de plantas y animales, a menudo respaldados por familias adineradas y la aristocracia, dio lugar a la aparición de nuevas razas a un ritmo nunca visto y que aún se mantiene. Desde entonces, las razas seleccionadas durante milenios y adaptadas a las condiciones locales comenzaron a desaparecer o se vieron abocadas a la extinción al ser sustituidas por estas razas nuevas y estandarizadas.

Por lo tanto, vale la pena estudiar cómo surgieron las nuevas razas y cuáles fueron los criterios de quienes las crearon. Darwin parecía no darse cuenta de que sus contemporáneos estaban practicando una forma de selección sexual interespecífica que favorecía la fijación de rasgos exagerados, a menudo claramente ornamentales, en las nuevas razas que pretendían crear. La elección de los animales progenitores fue realizada por criadores que persiguieron objetivos particulares, muy a menudo con criterios estéticos en mente. Hemos investigado quiénes fueron los fundadores de las razas modernas de cinco especies domesticadas (perros, gatos, cerdos, caballos y vacunos), ya que muy a menudo se atribuye a una sola persona la creación de la raza. Encontramos información sobre los fundadores de 459 razas, de las cuales 270 fueron creadas después del año 1800. Como curiosidad, para estas especies, la creación de razas se atribuye abrumadoramente a ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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hombres, pero en la naturaleza, son las hembras quienes suelen elegir las parejas, lo que se considera un rasgo adaptativo. Sin embargo, los criadores de la época victoriana carecían de esas habilidades adaptativas y de suficientes conocimientos científicos. La selección de individuos con una expresión extrema de los rasgos deseados, que a menudo eran parientes cercanos, resultó en una alta endogamia y en trastornos genéticos.

Palabras clave: Selección sexual, Selección artificial, Efectos pleiotrópicos, Endogamia, Domesticación Received: 11 II 20; Conditional acceptance: 14 V 20; Final acceptance: 11 I 21 Juan José Negro, Department of Evolutionary Ecology, Estación Biológica de Doñana–CSIC, Avda. Americo Vespucio 26, 41092 Sevilla, Spain.– María Carmen Blázquez, Centro de Investigaciones Biológicas del Noroeste –CIBNOR, 23096 La Paz, B.C.S., México.– Rocío Fernández–Alés, Ángel Martín–Vicente, Departamento de Biología Vegetal y Ecología, Facultad de Biología, Universidad de Sevilla, c/ Profesor García González s/n., 41012 Sevilla, Spain.

Corresponding author: Juan J. Negro. E–mail: negro@ebd.csic.es ORCID ID: J. J. Negro: 0000-0002-8697-5647; M. C. Blázquez: 0000-0002-0810-749X

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Introduction Charles Darwin proposed the three basic modes of organismic evolution, namely natural, sexual and artificial selection by humans, and tried hard to combine these processes to explain the emergence of all variation in the living world around us (Darwin, 1859, 1871). Artificial selection (Darwin 1868), is an 'evolutionary process in its own right' (Larson and Fuller, 2014; Wilkins, 2020), conducive to the creation of domesticated varieties, and it is necessarily mediated by human intervention (Clutton–Brock, 2012). Domesticated animals, though captive of humans or precisely because of this, have thrived everywhere. Currently, the biomass of livestock is larger for both mammals (such as cattle, sheep, goats, horses and pigs) and birds (poultry) than for all wild mammals and birds combined (Bar–On et al., 2018).

However, and perhaps because artificial selection is perceived as completely conscious and goal–directed, and thus a cultural endeavor detached from nature, there has been little attempt to conceptually compare it to both natural and sexual selection. In this essay, we wish to challenge this uncritical state of affairs, and posit that selection of modern animal breeds (generally speaking, those with standard morphotypes and studbooks) may still be influenced in subtle and yet unexplored ways by our own biological and cultural inheritances, even with the possibility of a gender bias (Lindsey, 2015). This hypothesis may also partially explain why older local breeds, considered as valuable genetic resources, are globally disregarded in favor of less healthy and often highly inbred, standardized breeds (Mendelsohn, 2003; FAO, 2013). Our main goal was to explore how breeds are generated and to highlight that one of the foremost management goals for wild populations today (i.e., conservation of genetic diversity) was overlooked or disregarded in the selection process of most modern breeds (Sánchez et al., 1999). Some may argue that the genetic status is of little practical consequence in the case of breeds in which most individuals are destined for early sacrifice, such as chicken or pigs, but it should make us think twice before acquiring individuals of, for instance, dog breeds that have a lower than average life span or are prone to diseases which make them less healthy (Lampi et al., 2020).

The points we want to stress are the following: 1) breeders have been practicing a surrogate form of sexual selection; 2) It is paradoxical that selective breeding has been mainly attributed to men, as we are a primate species, and thus we belong to a group in which females tend to be the selective sex; 3) Breeders may have done a good job in quickly standardizing breeds by practicing line breeding, truncation selection and genetic isolation, but modern breeds often present a high incidence of serious genetic disorders due to inbreeding and pleiotropic effects. Natural populations of wild animals have mechanisms in place, such as stabilizing selection, to avoid these problems.

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Artificial selection as a model for sexual selection We will argue here that artificial selection is not just a mere model for natural selection (Clutton–Brock, 1999; Larson and Fuller, 2014), with humans acting as the surrogate of a filtering 'environment', selecting against individuals that are less productive or too aggressive (i.e., the less fit for living with and for humans). It has generally been overlooked that artificial selection is a good model for sexual selection. It is the mode of selection to which Darwin resorted when he realized natural selection did not easily explain the evolution of seemingly ornamental traits (Darwin, 1871), such as the peacock tail or the huge antlers of the extinct Irish Elk. Artificial selection follows the principles of sexual selection because human breeders base their selection on trait expression and only allow some individuals to pass genes to the next generation, thus acting as the selective sex and selecting the fertilizing males.

Captive male animals do not have to fight for access to females (for instance, by securing and defending a territory and/or providing food resources), and, in many instances, the sex–ratio is skewed by the human breeder so that there are fewer males than in natural populations. Breeders put themselves in the place of the female in choosing a male. We have termed this process 'interspecific' sexual selection, a novel concept limited to the realm of artificial selection mediated by humans, with no parallels known in the animal kingdom.

The selection of modern breeds in the last two centuries, for which there are often written records and studbooks, have been attributed to male breeders in the most cases. It was a favourite pastime of gentlemen, and even the aristocracy, during the Enlightenment and also later in the 19th and early 20th centuries (e.g., Montague et al., 2014; Wallner et al., 2017; Whitaker and Ostrander, 2019) when societies were still markedly patriarchal. Potentially male–biased selection would mainly concern standardized modern breeds, and not necessarily traditional breeds, as these slowly evolved from the first domesticated animals, and breed founders were many over the different generations.

Gender bias in the attribution of breed selection In our primate evolutionary lineage, the female is the selective sex, as in most mammals (Darwin, 1871).

Mate choice in modern humans is highly influenced by culture, and it is sometimes initiated by the male, or it is bidirectional (see, e.g., Brown, et al., 2009).

Male humans (today and almost certainly in prehistoric times, as we are a highly size–dimorphic species) often display their physical and material power so as to be chosen by prospecting females (i.e., they play the game of intersexual selection), but sometimes they may even try to eliminate rival males or to downplay their displays engaging in what is known

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Table 1. Number of domestic breeds reviewed in this study, including those originated after 1800, with an indication of the number created by women (last column to the right). The attribution of founding events to female breeders is minimal, making statistical analysis unnecessary (see table 1s in supplementay material). Sources include the Canadian Kennel Club (online information) for dogs. For cats, we used The International Cat Association (TICA: https://tica.org), The Cat Fancier's Association (http://cfa.org) and The Governing Council of the Cat Fancy (https://gccfcats.org).

Tabla 1. Número de razas domésticas revisadas en este estudio, incluidas las originadas después del año 1800, con una indicación del número de ellas que fueron creadas por mujeres (última columna a la derecha). La atribución de casos de creación de razas a criadoras es mínima, lo que conlleva que los análisis estadísticos sean innecesarios (véase tabla 1s en material suplementario). Las fuentes utilizadas son el Canadian Kennel Club (información en línea) para perros. Para los gatos utilizamos "The International Cat Association" (TICA: https://tica.org); "The Cat Fancier's Association" (http://cfa. org), y "The Governing Council of the Cat Fancy" (https://gccfcats.org).

No. breeds Domestic species Scientific name reviewed

No. breeds modified/created after 1800

Dog

Canis lupus familiaris 209

Cattle

Bos taurus

58 36 0

Pig

Sus scrofa

75 60 0

Horse

Equus caballus

33 23 1

Cat

Felis catus

Total

as intrasexual selection (Puts, 2015). In this respect, our ancestral courtship behavior may be analogous to that of deer, sea lions, or many other mammalian species (Morina et al., 2018).

If there was a gender bias among breed founders, as suggested in table 1, this may have had consequences on how artificial selection for the creation of new breeds has been practiced. In fact, gender differences in general farm management in highly developed countries such as the USA were still significant at the end of the 20th century, with very few women –only 4 %– declaring to be farm owners and operators (Zeuly and King, 1998).

Even today, and particularly in non–western rural households in Africa, Asia and Central and South America, attitudes and values concerning livestock management are highly polarized between men and women (Kristjanson et al., 2010). Women tend to be the owners of small livestock including chicken, goats and sheep, while men are typically the owners of larger livestock, such as cattle, horses or camels (Njuki and Sanginga, 2013). In most cultures, even if women tend all kind of animals, most decisions on breeding, health practices and marketing rest on men (Kristjanson et al., 2010).

We obtained the names and gender of the breeders of a wide selection of breeds of five common domestic animals, to assess whether there could be a gender bias in the creation of standardized breeds. We based our choice of domesticated species on population numbers, current cosmopolitan distribution, and their

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Women involved 4

62 44 27 459

270

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split in numerous breeds, and we also tried to include different uses by people. We therefore considered two species mainly selected as pets (the dog, of which there are indeed working lines and breeds, and the cat), two species used for consumption (cattle and pigs), and lastly the horse, used mainly for transport and recreation.

According to our breed survey (table 1), male breeders have been credited as founders in most cases, particularly in the case of modern breeds in the last two centuries. Assuming that men have been the overwhelming force behind the domesticated animal breeds we see today, we must also assume the paradox that males, the sex which is chosen by females in the primate lineage, are acting as the selective sex on behalf of the animals they keep captive.

If the attribution to men was however wrong in some cases, it is time to recognize the role of uncredited women and revise breed history records.

Mechanisms to avoid genetic problems in natural populations It has been hypothesized that female animals in wild populations adaptively select males as fathers for their progeny based on 'good genes' (Andersson, 1994).

They try to get the best possible genetic makeup to produce healthy descendants, which in turn will be preferred by future selecting females (the 'sexy–son hypothesis', Weatherhead and Robertson, 1979).

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Fig. 1. Modern breeds are plagued with genetic disorders, such as the propensity to melanoma in grey horses. However, they are none–the–less highly appreciated in numerous horse breeds, such as the Spanish Purebred in the picture, due to their aesthetic appeal and symbolic value. The wild ancestors of horses were all melanized, excepting rare color mutants.

Fig. 1. Las razas modernas están plagadas de trastornos genéticos, como la propensión al melanoma en los caballos tordos, que, sin embargo, son muy apreciados en numerosas razas de caballos, como la raza pura española que se muestra en la imagen, debido a su atractivo estético y su valor simbólico. Los ancestros salvajes de los caballos estaban todos melanizados, excepto unos pocos mutantes de color.

Females, alternatively, may try to maximize genetic diversity in their progeny by selecting genetically compatible males (Mays and Hill, 2004). In addition, in natural populations, sexual selection, through male– male competition, female choice, or an interaction of both selective processes, may result in stabilizing selection on quantitative morphological traits (Kodric– Brown and Hohmann, 1990).

But how can human breeders (whether men or women) put themselves in the skin of discerning females to select the best stallion, or the best bull?

Particularly men, with their engagement in intrasexual competition with other men, may prefer the larger, the faster, and generally the fancier, when practicing artificial selection, perhaps ignoring or downplaying potential 'side–effects' (including pleiotropic effects, Reissmann and Ludwig, 2013). As we said above, animal breeders often cherry–pick individuals sporting rare attributes, such as blue eyes (Negro et al., 2017), that may be associated with impairments such as deafness. In horses, grays (fig. 1) are known to have a higher propensity to develop melanoma than horses with other coat colors (Pielberg et al., 2008), but they were selectively bred, nonetheless, by Car-

thusian monks in Spain, for instance. And there are almost entirely gray breeds due to deliberate coat selection, such as the Lippizaner, the Camargue horse and the Kladruber. Among dogs, the Rhodesian Ridgeback has a high incidence of a serious disease called dermoid sinus (Salmon Hillbertz et al., 2007), associated with the 'ridge' along the spine. Rhodesians are traced back to a big game hunter and dog breeder named Cornelius Van Rooyen (Mann and Stratton, 1966). Brachycephalic dogs, such us pugs, boxers and bulldogs, have a ten–fold increase in the prevalence of corneal ulcerative disease (O'Neill et al., 2017) compared to crossbred dogs. In fact, almost all individuals in brachycephalic breeds are homozygous for a DVL2 mutation, reducing their quality of life (Mansour et al., 2018). Artificial selection for extremely high growth rates in giant dog breeds has seemingly led to developmental diseases that significantly shorten their life expectancy (Galis et al., 2007). Entirely white animals exist for every domesticated species.

These white individuals, whether leucistics or true albinos, are extremely rare among wild species as they are possibly the focus of predation –or easily detected by prey.

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Examples of pleiotropic detrimental effects abound (Reissman and Ludwig, 2013), but they have not deterred breeders from producing 'defective' animals that would not survive well in nature, and whose wellness is compromised through their lifetime. In the wild, animals have evolved numerous mechanisms to avoid inbreeding, such as kin–recognition, sex– biased dispersal and extra–pair copulations (Pusey and Wolf, 1996), mechanisms that are overridden in captivity. Modern breeders, contrary to the developers of traditional breeds of the past, are typically more interested in breed uniformity, with the consequence that domestic animals often present a high incidence of genetic disorders due to inbreeding and pleiotropic effects. This may also affect animal welfare and even increase susceptibility to infectious diseases (Luong et al., 2007). It remains to be seen, however, whether female breeders would have different selection goals, perhaps less prone to extreme trait selection, as too few women seem to have participated (or at too few have been given credit; a limitation inherent to our study) in the creation of modern breeds.

Acknowledgements This research did not receive any financial support. We thank two anonymous reviewers for their comments, and Christopher Swann for revising the English text.

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Supplementary material Table 1s. Breeds of dogs (A), cattle (B), pigs (C), horses (D) and cats (E) reviewed in this study. We include date and country of origin, as well as the putative founders (individual ot collective).

Tabla 1s. Razas de perros (A), ganado vacuno (B), cerdos (C), caballos (D) y gatos (E) revisadas en este estudio. Se incluyen fecha y país de origen, así como los presuntos fundadores (individuos o colectividades).

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A contribution to the earthworm diversity (Clitellata, Moniligastridae) of Kerala, a component of the Western Ghats biodiversity hotspot, India, using integrated taxonomy S. S. Thakur, A. R. Lone, N. Tiwari, S. K. Jain, S. W. James, S. Yadav Thakur, S. S., Lone, A. R., Tiwari, N., Jain, S. K., James, S. W., Yadav, S., 2021. A contribution to the earthworm diversity (Clitellata, Moniligastridae) of Kerala, a component of the Western Ghats biodiversity hotspot, India, using integrated taxonomy. Animal Biodiversity and Conservation, 44.1 117–137, Doi: https://doi.org/10.32800/ abc.2021.44.0117 Abstract A contribution to the earthworm diversity (Clitellata, Moniligastridae) of Kerala, a component of the Western Ghats biodiversity hotspot, India, using integrated taxonomy. Earthworms (Clitellata, Moniligastridae) of Chaliyar River Malappuram, Eravikulam National Park, Neyyar Wildlife Sanctuary, Parambikulam Tiger Reserve, Peppara Wildlife Sanctuary, Periyar National Park, Shendurney Wildlife Sanctuary and Wayanad Forest, Kerala, a component of the hotspot of Western Ghats, India, were studied by the standard method of taxonomy, and their DNA barcode signatures using the mitochondrial gene cytochrome c oxidase I (COI) were generated for the first time. This study represents eleven species of earthworms of the family Moniligastridae: Drawida brunnea Stephenson, Drawida circumpapillata Aiyer, Drawida ghatensis Michaelsen, Drawida impertusa Stephenson, Drawida nilamburensis (Bourne), Drawida robusta (Bourne), Drawida scandens Rao, Drawida travancorense Michaelsen, Moniligaster aiyeri Gates, Moniligaster deshayesi Perrier, and Moniligaster gravelyi (Stephenson). In the phylogenetic analysis all the species were recovered in both neighbour–joining (NJ) and maximum likelihood (ML) trees with high clade support. The average K2P distance within and between species was 1.2 % and 22 %, whereas the clear barcode gap of 2–5 % was suggested by barcode gap analysis (BGA) of studied species, reflecting the accuracy of characterization. The study presents the first step in the molecular characterization of the native earthworm family Moniligastridae of India.

Data published through GBIF (Doi: 10.15470/l2nlhz) Key words: COI, Genomic signature, DNA barcoding, Earthworms biodiversity, Moniligastridae, Western Ghats, Kerala Resumen Una contribución a la diversidad de lombrices (Clitellata, Moniligastridae) de Kerala, un componente de la gran diversidad en Western Ghats, en la India, utilizando taxonomía integrada. Las lombrices (Clitellata, Moniligastridae) del río Chaliyar de Malappuram, el Parque Nacional de Eravikulam, el refugio de especies silvestres de Neyyar, la reserva de tigres de Parambikulam, el refugio de especies silvestres de Peppara, el Parque Nacional de Periyar, el refugio de especies silvestres de Shendurney y el bosque de Wayanad, en Kerala, que son una parte de la elevada diversidad de Western Ghats, en la India, se estudiaron mediante el método convencional de taxonomía, y su código de barras del ADN utilizando el gen de la oxidasa I del citrocromo c (COI). El estudio representa 11 especies de lombrices de la familia Moniligastridae, a saber: Drawida brunnea Stephenson, Drawida circumpapillata Aiyer, Drawida ghatensis Michaelsen, Drawida impertusa Stephenson, Drawida nilamburensis (Bourne), Drawida robusta (Bourne), Drawida scandens Rao, Drawida travancorense Michaelsen, Moniligaster aiyeri Gates, Moniligaster deshayesi Perrier y Moniligaster gravelyi (Stephenson). En el análisis filogenético, todas las especies se recuperaron tanto en los árboles producidos mediante el método de unión de vcinos como en los árboles basados en la máxima verosimilitud, con un elevado apoyo de los clados.

La distancia media calculada con el modelo K2P dentro de una misma especie y entre especies fue del 1,2 % y el 22 %, respectivamente, mientras que el análisis de deficiencias del código de barras (BGA) de las especies ISSN: 1578–665 X eISSN: 2014–928 X

© [2021] Copyright belongs to the authors, who license the journal Animal Biodiversity and Conservation to publish the paper under a Creative Commons Attribution 4.0 License.

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estudiadas sugirió una brecha del 2–5 %, lo que refleja la precisión de la caracterización. En el estudio se presenta el primer paso en la caracterización molecular de la familia de lombrices Moniligastridae, autóctona de la India.

Datos publicados en GBIF (Doi: 10.15470/l2nlhz) Palabras clave: COI, Estructura genómica, Código de barras del ADN, Biodiversidad de lombrices, Moniligastridae, Western Ghats, Kerala Received: 18 I 21; Conditional acceptance: 23 II 21; Final acceptance: 23 III 21 Samrendra Singh Thakur, Department of Biotechnology, School of Biological Sciences, Dr. Harisingh Gour, Vishwavidyalaya (A Central University), Sagar, 470003, Madhya Pradesh, India.– Azhar Rashid Lone, Nalini Tiwari, Subodh Kumar Jain, Shweta Yadav, Department of Zoology, School of Biological Sciences, Dr. Harisingh Gour, Vishwavidyalaya (A Central University), Sagar, 470003, Madhya Pradesh, India.– Samuel Wooster James, Department of Regenerative Agriculture, Maharishi International University, Fairfield, Iowa, 52557 United States.

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Introduction

Material and methods

Moniligastridae is a family of earthworms indigenous to southeast and eastern Asia. It is believed that the family Moniligastridae originated in the Malaya Archipelago’s geographical region (Gates, 1972; Blakemore, 2014), but later Jamieson (1977) sug– gested an origin near Myanmar. Its natural range encompasses south, southeast and east Asia, from peninsular India to Japan through Myanmar, China, the extreme southern portion of far Eastern Russia, Korea, the Philippines, Borneo, and Sumatra (Gates, 1972). Moniligastrids are dominant members of the earthworms fauna in India especially in the South and North East Regions. Three genera Desmogaster Rosa, 1890; Drawida Michaelsen 1900; and Moniligaster Perrier, 1872 are known from India (www.earthwormsofindia.com). Among them Drawida is most diverse with 73 species in India. Earthworms of this family have drawn the attention of earthworm biologists as they retain the single layered clitellum characteristic of Clitellata other than earthworms (Crassiclitellata) yet function ecologically as do the crassiclitellate earthworms.

The Moniligastridae have a broad size range, just like earthworms sensu stricto. The family is characterized by simple pointed setae, four pairs per segment, a clitellum beginning on segment 9 or 10 and extending over 3 to 10 segments, including those bearing genital pores; male pores one pair (Drawida, Moniligaster) or two pairs (Desmogaster) in or near grooves 10/11, 11/12 or 12/13; female pores one pair in 11/12 or XII or XIV. The spermathecal pores are one or two pairs in 7/8 or 8/9 or 7/8 and 8/9; the oesophagus with two gizzards anterior to X or two to ten gizzards at the beginning of the intestine. The last hearts are two segments in front of the ovarian segment; they are holonephridial. Testes and funnels one or two pairs enclosed in one or two pairs of testis sacs. Vasa deferentia opening into prostate glands. One pair of ovaries in the segment immediately in front of the groove or segment on which the female pores are situated, one pair of ovisacs extending backwards from the ovarian segment. One or two pairs of spermathecae with long tubular ducts. Without typhlosole, calciferous glands, supra–intestinal glands and seminal vesicles.

The use of these morpho–anatomical characteristics has often been a barrier to the identification of these earthworms, leading to imprecise identification of taxa. The present study is the first attempt to provide a means for rapid assessment of some moniligastrids by using molecular data. The study was performed in the Kerala state, as half of its area falls under the Western Ghats, one of the world's eight most important biodiversity hotspots (Myers et al., 2000; Mittermeier et al., 2011). Therefore, the present study aimed to assess the earthworm diversity and the phylogenetic relationship of some moniligastrids with the use of DNA barcodes as a standard genetic marker for identification of earthworm species of Kerala.

Study site Kerala is a small state in the south–western tip of India. It is a narrow strip of coastal plain that borders the Arabian Sea from the north to south, next to the neighbouring states of Karnataka and Tamil Nadu. The state is recognized for its lush greenery, highly dense forests, diversified ecological habitats, topography, and the high biodiversity. It is bounded by the thickly wooded and forested hills of the Western Ghats to the east and the Arabian Sea to the west. Kerala occupies 38,863 sq. km and comprises approximately 1.18 % of India’s landmass (Sreedharan, 2004). Out of the total length of the Western Ghats, Kerala covers around 600 km. Nearly 56 % of the total geographical area of the state has an annual average temperature ranging between 31 to 37 oC and annual rainfall of 3,500 mm, mainly due to the windward location to the Ghats (Rao, 1976).

Due to the integration and combination of different climatic conditions, like warmer climate, altitudinal variations, two different rainfall patterns and seasons (Southwest monsoon and North–East monsoon), several soil types and agro–ecological zones, Kerala has a variety of macro environments that vary from tropical rain forests to hot dry deciduous forests.

These diversified habitats and local ecological niches contributed to a variety of macro and micro environments conducive for a variety of flora and fauna requiring contrasting environment. Of the biota of India, the state sustains over 24 % of the plant species, 30 % of the animal species, and 35 % of the freshwater fish species (Sreedharan, 2004).

Collection of earthworm samples Earthworm samples analysed in the present study were collected from different sampling sites in Kerala (fig. 1; see also the dataset published through GBIF (Doi: 10.15470/l2nlhz). The locations, species names, coordinates, and their BOLD accession numbers are provided in table 1. Samples were collected by digging and hand–sorting according to the method described by Satchell (1969). The specimens were anesthetized in 30 % (v/v) ethanol. Small pieces of muscle tissue from the tail region were then cut and preserved in 100 % (v/v) ethanol solution for molecular investigation. Next the earthworm samples were fixed in 10 % (w/v) formalin for morphological identification. 100 % ethanol preserved tissue of each sample was placed in the Museum of Dr. Harisingh Gour Vishwavidyalaya (A Central University), Sagar, Madhya Pradesh, India as reference.

Sample management and morphological classification Prior to applying the molecular technique for evaluation, we identified earthworms on the basis of specific diagnostic morphological characters under a stereoscopic zoom microscope (Leica Model No. M60) using the available literature (Stephenson, 1923; Aiyer,

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120

75º 10'

75º 50'

76º 30'

77º 10' Drawida brunnea

12º 15'

India

Kasaragod

Drawida circumpapillata 12º 15'

Drawida impertusa

Kannur

11º 40'

Drawida ghatensis Drawida nilamburensis

Wayanad

11º 40'

Drawida scandens

Kozhikode

Drawida travancorense

Malappuram

11º 05'

11º 05'

Thrissur

10º 30'

Ernakulam

9º 55'

Moniligaster aiyeri Moniligaster deshayesi

Palakkad

10º 30'

Drawida robusta

Moniligaster gravelyi

9º 55'

Idukki Kottayam

9º 20'

Albppuzha

Pathanamthita

9º 20'

Kollam

8º 45' 0 75º 10'

50 km 75º 50'

8º 45' Thiruvananthapuram

76º 30'

77º 10'

Fig. 1. Study area with distribution of Moniligastrids in Kerala.

Fig. 1. Study area with distribution of Moniligastrids in Kerala.

1929; Gates, 1972; Julka, 1988; Narayanan et al., 2016, 2017). A camera lucida was used for drawings and abbreviations: spp, spermathecal pore; mp, male pore; atr, atrium; spd, spermathecal duct; amp, ampulla; tss, testis sac; vd, vas deferens; prs, prostate; atrgl, atrial gland were used in the figures. Voucher specimens are housed in the Museum, Department of Zoology, Dr. Harisingh Gour Vishwavidyalaya (A Central University), Sagar, Madhya Pradesh, India.

DNA sequencing For DNA sequencing the small pieces of muscle tissue from tail region were used. A total of 28 samples of moniligastrids were sent to Barcode of Life Data Systems (BOLD System), Biodiversity Institute of Ontario, University of Guelph, Canada (Ratnasingham and Hebert, 2007) following appropriate protocol to obtain DNA sequences, accession numbers and Barcode. All the data used in present study is available on BOLD website under the project entitled 'Diversity studies in earthworms of India' (IEW). In addition, 28 COI sequences were retrieved from the

NCBI and BOLD free public domain for molecular analysis (see table 2 for more details).

Sequence alignment and data analysis The alignment of 56 COI data matrix [28 COI from this study (table 1) and 28 additional from NCBI and free public domain of BOLD (table 2) were analysed in MEGA X (Kumar et al., 2018). For intraspecific and interspecific genetic distances within and between species, the best substitution model i.e., Kimura two–parameter (K2P) (Kimura, 1980) was used. For phylogenetic analysis we used the COI matrix to generate the neighbour–joining (NJ) and maximum likelihood (ML) trees using MEGA X, with a graphic depiction for the evolutionary distances between species. Node robustness was inferred with 1,000 bootstrap replicates. The barcoding gap analysis was also inferred in the barcode gap analysis (BGA) tool available on BOLD, but only 28 COI sequences generated in this study were used. Similarly, the calculation of sequence composition was computed in MEGA X.

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Table 1. The list of moniligastrid species from Kerala along with sample IDs, locations, GPS coordinates, and their BOLD accession numbers (BAN): CCR, Close to Chaliyar River, Malapuram, Areekode, Malappuram; ENP, Eravikulam National Park, Kannan Devan Hills; NWS, Neyyar Wildlife Sanctuary, Trivandrum; PNP, Periyar National Park, Idukki; PTR, Parambikulam Tiger Reserve, Palakkad; PWS, Peppara Wildlife Sanctuary, Thiruvananthapuram; SWS, Shendurney Wildlife Sanctuary, Kollam; WFA, Wayanad Forest Area near to Agraharam Resort, Wayanad.

Tabla 1. La lista de especies de moniligástridos de Kerala con el código de identificación de la muestra, la ubicación, las coordenadas GPS y los números de accesión de la base de datos de registros de código de barras BOLD (BAN): CCR, cerca del Río Chaliyar, Malapuram, Areekode, Malappuram; ENP, Parque Nacional de Eravikulam, Kannan Devan Hills; NWS, Refugio de fauna silvestre de Neyyar, Trivandrum; PNP, Parque Nacional de Periyar, Idukki; PTR, Reserva de tigres de Parambikulam, Palakkad; PWS, Refugio de fauna silvestre de Peppara, Thiruvananthapuram; SWS, Refugio de fauna silvestre de Shendurney, Kollam; WFA, bosque de Wayanad cerca del complejo Agraharam Resort Wayanad, Wayanad.

Num.

Exact site

GPS coordinates

BAN

1 KERL269A2 D. brunnea

Sample ID

Species

PWS

8.62075, 77.1676

ADH0514

2 KERL273A5 D. circumpapillata

ENP

10.1158, 77.089

ADH2327

3 KERL0268A3 D. ghatensis

NWS

8.53344, 77.1482

ADH1313

4 KERL0275A4 D. ghatensis

NWS

8.55006, 77.2425

ADH1313

5 KERL0275A5 D. ghatensis

NWS

8.55006, 77.2425

ADH1313

6 KERL0275A6 D. ghatensis

NWS

8.55006, 77.2425

ADH1313

7 KERL0275A7 D. ghatensis

NWS

8.55006, 77.2425

ADH1313

8 KERL0275A8 D. ghatensis

NWS

8.55006, 77.2425

ADH1313

9 KERL0269A6 D. impertusa

PWS

8.62075, 77.1676

ADH1401

10 KERL0269A8 D. impertusa

PWS

8.62075, 77.1676

ADH1401

11 KERL0274A2 D. impertusa

PWS

8.62075, 77.1676

ADH1401

12 KERL0274A4 D. impertusa

PWS

8.62075, 77.1676

ADH1401

13 KERL0274A6 D. impertusa

PWS

8.62075, 77.1676

ADH1401

14 KERL53A2

CCR

11.3179, 76.1889

ADH3257

15 KERL0270A4 D. robusta

PWS

8.62075, 77.1676

ADH1162

16 KERL0270A12 D. robusta

PWS

8.62075, 77.1676

ADH1162

17 KERL077A2

WF

11.9117, 76.0075

ADH2690

18 KERL0274A5 D. travancorense

PWS

8.64311, 77.1807

ADH1161

19 KERL0264A1 M. aiyeri

ENP

10.1156, 77.0871

ADH1655

20 KERL0276A1 M. aiyeri

ENP

10.1109, 77.0911

ADH1655

21 KERL0276A2 M. aiyeri

ENP

10.1109, 77.0911

ADH1655

22 KERL0267A5 M. deshayesi

PTR

10.3929, 76.7756

ADH1656

23 KERL0272A5 M. deshayesi

PNP

9.45628, 77.2316

ADH1656

24 KERL0270A13 M. gravelyi

SWS

8.88436, 77.1676

ADH0515

25 KERL0270A14 M. gravelyi

SWS

8.88436, 77.1676

ADH0515

26 KERL0270A18 M. gravelyi

SWS

8.62075, 77.1676

ADH0515

27 KERL0270A19 M. gravelyi

SWS

8.88436, 77.1676

ADH0515

28 KERL0270A20 M. gravelyi

SWS

8.88436, 77.1676

ADH0515

D. nilamburensis

D. scandens

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Table 2. Details of COI sequences retrieved from NCBI and BOLD database.

Tabla 2. Datos relativos a las secuencias del COI extraídos del Centro Nacional de Información Biotecnológica de los Estados Unidos (NCBI) y de la base de datos gratuita BOLD.

Database accession number

Num Species name

BOLD

NCBI

References

1 D. bullata

ACB6680

JN793527

BOLD system and NCBI database

2 D. bullata

ACB6680

JN887894

BOLD system and NCBI database

3 D. ghilarovi

ADR5225

KY711499

BOLD system and NCBI database

4 D. ghilarovi

ADR5225

KY711501

BOLD system and NCBI database

5 D. ghilarovi

ADR3943

KY711517

BOLD system and NCBI database

6 D. ghilarovi

ADR4360

KY711477

BOLD system and NCBI database

7 D. gisti

Not available

JQ657807

NCBI database

8 D. gisti

Not available

JQ657808

NCBI database

9 D. gracilis

ACB6701

JN887887

BOLD system and NCBI database

10

ACB6701

JN793516

BOLD system and NCBI database

11 D. hattamimizu

AAM4518

AB543219

BOLD system and NCBI database

12

D. hattamimizu

AAM4518

AB543220

BOLD system and NCBI database

13

D. hattamimizu

AAM4518

AB543224

BOLD system and NCBI database

14

D. hattamimizu

AAM4518

AB543217

BOLD system and NCBI database

15

D. hattamimizu

AAM4518

AB543214

BOLD system and NCBI database

16

D. japonica

Not available

JQ677078

NCBI database

17

D. japonica

Not available

JQ677080

NCBI database

18

D. japonica

Not available

JQ677081

NCBI database

19

D. japonica

Not available

JQ677079

NCBI database

20

D. japonica

AEG3736

MH882855

BOLD system and NCBI database

21

D. koreana

AEG3736

MH882566

BOLD system and NCBI database

22

D. koreana

AEG3736

MH845538

BOLD system and NCBI database

23

D. koreana

AEG3736

MH845504

BOLD system and NCBI database

24

D. nepalensis

ADH4589

MT570064

BOLD system and NCBI database

25

D. nepalensis

ADH4589

MT570063

BOLD system and NCBI database

26

D. nepalensis

ADH4589

MT472588

BOLD system and NCBI database

27

D. nepalensis

ADH4589

MT472587

BOLD system and NCBI database

28

Mollusca sp.

Not available

MF983247

NCBI database

D. gracilis

Results

Family Moniligastridae

The earthworm species collected and identified from the study area are arranged in alphabetical order.

Each entry gives the information in sequence: earthworms' scientific name, material examined, sample ID with accession number(s), collection site, description of species. Brief descriptions of the genera are also given.

Genus Drawida Michaelsen, 1900 Deep pigmentation or without pigmentation, clitellum on X–XIII segments, one pair of male pores in 10/11, female pores in 11/12, spermathecal pores in 7/8. Two to eight gizzards at the beginning of the intestine. Last heart in IX. Dorsal pores usually absent. One pair of tes-

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tss VII VIII IX X XI

atr

spp

mp

vd amp

spd prs

1 mm

1 mm 1 mm A B C Fig. 2. Camera lucida sketch of Drawida brunnea: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 2. Dibujo con cámara lúcida de Dawida brunnea: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

tes and funnels enclosed within setal sac which project from septum 9–10 into segment X or segment IX and X. Prostate of various forms, ovaries XI, this segment may be reduced to a special ovarian chamber of characteristic form, one pair of ovisac projecting backwards from septum 11–12. Spermathecae with or without atrium like dilation (diverticulum, function unknown) at the ectal end, without stalked glands. Penial setae and copulatory setae absent. Genital markings rarely found.

Drawida brunnea Stephenson, 1915 Material examined: KERL269A2 Sample ID with BOLD accession number: KERL0269A2 (ADH0514) Collection site: Peppara Wildlife Sanctuary (8º 37' 14.7'' N, 77º 10' 03.3'' E), Thiruvananthapuram, Kerala, India.

Date of collection: 25 X 2015 Diagnostic features: length 70 mm; diameter 5 mm, segments 180; body short and relatively broad, dorsoventrally flattened. Prostomium prolobus.

Setae small, closely paired, aa < bc and dd = ½ circumference. Male pores eye shaped bordered by prominent shape midway between b and c. Female pores nearer b. Spermathecal pores in cd, close to c. Septa 5/6–8/9 thickened. Three gizzards in XIII–XV, the first less firms than others. Testis sacs large kidney–shaped occupies in 9/10 more into X, vas deferens short without coiling; prostate opaque white, spherical/ovoid with short moderately thick stalk, smooth but no muscular iridescence. Ovarian chamber with its roof at the dorsal parietes, funnel extends upwards on each side of the gut nearly to mid–dorsal line, ovisacs in XII. Spermathecal ampulla ovoid, atrium mammillary in shape sessile

on parietes joined by the slightly coiled duct at base (fig. 2).

Drawida circumpapillata Aiyer, 1929 Material examined: KERL273A5 Sample ID with BOLD accession number: KERL0273A5 (ADH2327) Collection site: Eravikulam National Park (10º 06' 56.9'' N, 77º 05' 20.5'' E), Kannan Devan Hills, Kerala, India.

Date of collection: 29 X 2015 Diagnostic features: length 40–60 mm; diameter 3–5 mm, segments 127–150. Colour light grey.

Dorsal pores absent. Setae closely paired; aa < bc; dd equal or lesser to ½ circumference visible from III segment. Clitellum dark brown saddle–shaped in X–XIII. Nephridiopores in cd visible from IV. Male pores between b and c nearer to b, minute on a conical elevation in the centre of a large circular papillae, sometimes almost touch each other in the mid–ventral line. Each papillae extends outwards about half bc of setal zones both in X and XI segments. Female pores in ab. Spermathecal pores in d (sometimes in ab) slit–like aperture.

Septa 5/6–8/9 thickened. Three gizzards in XII– XIV. Testis sacs large ovoid sacs in X, tapered towards posterior end. Vas deferens lies on the anterior face of septum 9/10 in segment IX, where it twines round the heart and enters the prostate on its anterior side near the ectal end. Prostate large club–shaped, furry or papillose, densely covered with large granulated gland cells. Ovarian chamber present, ovisacs very long extending backwards through eight and ten segments. Spermathecal ampulla sac–like in VIII, atrium digitiform in VII, duct loosely colled entering its ectal end (fig. 3).

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tss VII

spp

spd

IX XI

atr

mp 1 mm

prs

amp

VIII X

vd

1 mm

A

1 mm B

C

Fig. 3. Camera lucida sketch of Drawida circumpapillata: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 3. Dibujo con cámara lúcida de Drawida circumpapillata A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

Drawida ghatensis Michaelsen, 1910 Material examined: KERL268A1; KERL268A3; KERL275A4; KERL275A5; KERL275A6; KERL275A7; KERL275A8 Sample ID with BOLD accession number: KERL0268A1 (ADH1313); KERL0268A3 (ADH1313); KERL0275A4 (ADH1313); KERL0275A5 (ADH1313); KERL0275A6 (ADH1313); KERL0275A7 (ADH1313); KERL0275A8 (ADH1313) Collection site: Neyyar Wildlife Sanctuary (8º 33' 00.2'' N, 77º 14' 33.1'' E), Trivandrum, Kerala, India.

Date of collection: 27 XI 2015 Diagnostic features: length 80–190 mm; diameter 2–7 mm, segments 140–186. Colour bluish grey.

Prostomium prolobous. Dorsal pores absent. Setae visible from III segment, closely paired; aa equal or slightly greater than bc; dd slightly greater than ½ circumference. Nephridiopores usually in cd.

Male pores transverse slit like aperture between b and c. Female pores in ab. Spermathecal pores minute aperture slightly at b or lateral to b. Five gizzards in XVI–XXII. Testis sacs ovoidal in XIII– XVI. Vas deferens highly coiled and forms a cluster equal or larger than testis sac. Prostate ovoid or thickly pear–shaped, with investment of glandular cells. Ovarian chamber present. Spermathecal ampulla pear–shaped. Atrium with bilobed cavity, duct highly coiled entering atrium in the depression between the lobes (fig. 4).

Drawida impertusa Stephenson, 1920 Material examined: KERL269A6, KERL269A8, KERL274A2, KERL274A4, KERL274A6 Sample ID with BOLD accession number: KER-

L0269A6 (ADH1401), KERL0269A8 (ADH1401), KERL0274A2 (ADH1401), KERL0274A4 (ADH1401), KERL0274A6 (ADH1401) Collection site: Peppara Wildlife Sanctuary (8º 37' 14.7'' N, 77º 10' 03.3'' E), Thiruvananthapuram, Kerala, India.

Date of collection: 25 X 2015 Diagnostic features: length 45–100 mm; diameter 4 mm, segments 165. Colour dark bluish olive, darker dorsally. Prostomium small, prolobous. Dorsal pores absent. Setae visible in III, closely paired, aa less than bc, except at hinder end. Nephridiopores in cd. Clitellum on X–XIII. Male pores between b and c bounded by narrow lips; a pair of fairly whitish papillae on the segment in front of the male pores.

Female pores in b. Spermathecal pores in c. Four gizzards in XIV–XVII. Testis sacs ovoid projecting in IX and X. Vas deferens slightly coiled. Prostate spherical (sometimes pear–shaped), glandular, duct joins at its anterior end. Ovaries in segment XI, sessile, almost circular. Ovarian chamber present, ovisacs present extending back to XIII or XIV. Spermathecae with pear–shaped ampulla, long coiled duct and no atrial dilation (fig. 5).

Drawida nilamburensis (Bourne, 1894) Material examined: KERL53A2 Sample ID with BOLD accession number: KERL53A2 (ADH3257) Collection site: Close to Chaliyar River (11º 19' 04.6'' N, 76º 11' 19.9'' E) Malapuram, Areekode, Malappuram, Kerala, India.

Date of collection: 09 IX 2014 Diagnostic features: length 500–700 mm; diameter 7 mm, segments 550–600, secondary annulation

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amp

VII

spp

spd

VIII IX

mp

X XI

tss

prs

atr

1 mm

vd

1 mm

1 mm

A

B

C

Fig. 4. Camera lucida sketch of Drawida ghatensis: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 4. Dibujo con cámara lúcida de Drawida ghatensis: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

VII VIII

spp

IX X XI

vd prs

tss

spd

mp 1 mm

amp

1 mm

A

1 mm

B

C

Fig. 5. Camera lucida sketch of Drawida impertusa: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 5. Dibujo con cámara lúcida de Drawida impertusa: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

present. Slightly pigmented. Prostomium broad.

Setae long, aa greater than bc; dd greater than ½ circumference visible from IV segment. Nephridiopores in cd. Male pores between b and c or at b or nearer b. Female pores in ab. Spermathecal pores in cd. Septa 5/6–8/9 strongly thickened.

Five gizzards in XXVII–XXXI. Testis sacs ovoid.

Prostate not glandular, ovoidal in appearance, vas deferens long, very coiled. Ovarian chamber present. Spermathecal ampulla pear–shaped, atrium as a dilation of the end of the duct, small

(not clearly visible to draw under camera lucida) embedded in the body wall (fig. 6).

Drawida robusta (Bourne, 1886) Material examined: KERL270A4, KERL2701 Sample ID with BOLD accession number: KERL0270A4 (ADH1162); KERL027012 (ADH1162) Collection site: Peppara Wildlife Sanctuary (8º 37' 14.7'' N, 77º 10' 03.3'' E) Thiruvananthapuram, Kerala, India.

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VII spp

VIII IX

vd tss

prs

amp

X mp

XI

spd

1 mm A

1 mm

1 mm

B

C

Fig. 6. Camera lucida sketch of Drawida nilamburensis: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 6. Dibujo con cámara lúcida de Drawida nilamburensis: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

Date of collection: 25 X 2015 Diagnostic features: length 80–180 mm; diameter 4–6 mm, segments 150–160. Colour bluish to greenish brown. Setae closely paired, very small aa greater than bc; dd greater than ½ circumference visible from III segment. Nephridiopores in cd.

Male pores between b and c nearer to c. Female pores in ab. Spermathecal pores in cd very minute aperture. Number of gizzards four in XII–XV. Testis sacs large sub–ovoidal or spherical in X–XI. Vas deferens long and highly coiled. Prostate hemispherical, glandular, duct joins at its posterior region.

Ovarian chamber present, ovisacs small, tubular confined to XII. Spermathecal ampulla pyriform to oval. Atrium bilobed, duct (not much coiled) entering in the depression between the lobes (fig. 7).

Drawida scandens Rao, 1921 Material examined: KERL77A2 Sample ID with BOLD accession number: KERL077A2 (ADH2690) Collection site: Wayanad Forest area near Agraharam Resort (11º 54' 42.2'' N, 76º 00' 27.0'' E), Wayanad, Kerala, India.

Date of collection: 08 IX 2014 Diagnostic features: length 38–45 mm; diameter 1.5–2 mm, segments 144–161. Colour dark bluish brown or olive. Prostomium prolobous. Setae closely paired, large and prominent especially in the ventral bundles of III–XII; aa = bc or in the anterior part of the body is rather greater; dd = ½ circumference Male pores two pairs, the anterior in 9/10, rather outside the line of setae b, on a median transverse somewhat dumbbell–shaped cushion, extending on each side to between the line of b

and c; posterior male pores on 10/11, in line/just outside of setae b, in the antero–lateral angles of a thickened median patch which occupies the ventral surface (almost entire) of XI. Female pores in 11/12 between the lines a and b. Spermathecal pores in ab or slightly lateral to b. Septa 6/7–8/9 considerably thickened, 5/6 thin, 9/10 and a few following slightly thickened. Two gizzards in XIII and XIV, sometimes three in XIII–XV. Testis sacs extending into IX and X. Prostate two pairs in IX and X, elongated, cylindrical or pear–shaped, surface soft, minutely papillated. No ovarian chamber, spermathecal atrium ovoid and sac like, duct entering towards the ectal end (fig. 8).

Drawida travancorense Michaelsen, 1910 Material examined: KERL274A5 Sample ID with BOLD accession number: KERL0274A5 (ADH1161) Collection site: Peppara Wildlife Sanctuary (8º 38' 35.2'' N, 77º 10' 50.6'' E), Trivandrum, Kerala, India.

Date of collection: 26 XI 2015 Diagnostic features: length 60–110 mm; diameter 3 mm, segments 127. Colour light grey. Dorsal pores absent. Setae closely paired, begin from II, aa lesser than bc; dd greater than ½ circumference visible from II segment. Clitellum saddle–shaped, interrupted between the lines a, including X–XIII. Nephridiopores in cd visible from IV. Male pores comma like slits, the broader end towards the middle line between b and c nearer to b. Female pores in ab. Spermathecal pores in c slit like aperture. Septa 5/6–8/9 strongly thickened. Two gizzards in XI–XV. Testis sacs large irregular in

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spp VII VIII IX X XI

mp

amp spd atr

prs 1 mm

1 mm

vd

tss

A

1 mm

B

C

Fig. 7. Camera lucida sketch of Drawida robusta: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 7. Dibujo con cámara lúcida de Drawida robusta: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

tss vd

spd VII VIII IX X XI

spp mp 1 mm A

atr amp

prs

1 mm

1 mm B

C

Fig. 8. Camera lucida sketch of Drawida scandens: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 8. Dibujo con cámara lúcida de Drawida scandens: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

shape in X–XI (sometimes IX–XI). Vas deferens short, not much coiled, confined in X. Prostate large pear–shaped, pigmented reddish with fine grooves. Ovarian chamber present, ovisacs thick, short extending backwards through one or two segments. Spermathecal ampulla pear–shaped or ovoid, atrium club–shaped sac in VII, duct entering its ental end (fig. 9).

Genus Moniligaster Perrier, 1872 One pair of male pores in 10/11, one pair of female pores in 11/12, one pair of spermathecal pores in 7/8.

Gizzards 4 or 5 in front of the intestine. Last pair of hearts in IX. One pair of testis sacs on septum 9/10.

Prostates with duct distinguishable from glandular part, ovisacs in XI. Ovisacs extending backwards

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VII VIII

tss spp

amp

vd spd

IX X

atr

prs

mp

XI 1 mm

1 mm

A

1 mm

B

C

Fig. 9. Camera lucida sketch of Drawida travancorense: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 9. Dibujo con cámara lúcida de Drawida travancorense: vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

from 11/12. Spermathecae with a bifid muscular atrial chamber (fig. 10), each horn of which bears a lobulated glandular mass. Genus differs from Drawida in the presence of two horns of atrial chamber (one pair of glands discharging by its own canal into a common duct; fig. 10) and mostly found in South India.

Moniligaster aiyeri Gates, 1940 Material examined: KERL264A1, KERL276A1, KERL276A2 Sample ID with BOLD accession number: KERL0264A1 (ADH1655), KERL0276A1 (ADH1655), KERL0276A2 (ADH1655) Collection site: Neyyar Wildlife Sanctuary (10º 06' 39.2'' N, 77º 05' 28.1'' E), Trivandrum, Kerala, India.

Date of collection: 27 XI 2015 Diagnostic features: length 400–600 mm; diameter 8–10 mm, segments 310. Colour dark reddish brown. Dorsal pores absent. Setae closely paired, aa = bc; dd = ½ circumference. Nephridiopores usually at ab. Clitellum annular extending on X–XIIII. Male pores transversely placed elliptical apertures on 10/11 in bc nearer to b, each aperture protuberant to the exterior an antero–posteriorly flattened, penis like structure with transversely slit like aperture on the ventral face. Female pores minute on b. Spermathecal pores transversely placed slits in cd or d. Septa 6/7 is thickly muscular, 7/8–8/9 very thickly muscular. Three–five gizzards in XVI–XXII. Testis sacs smaller than the cluster of vas deferens which is much thicker, very long, loop of slender portion in IX and X, thickened portion in a cluster of loops in IX which is larger

than the testis. Prostate large mushroom–shaped, muscular, thick, opaque and lined internally with white material which is raised into irregular ridges.

Ovarian chamber present, ovisacs with thick wall extending into XVI. Spermathecal duct is 20 mm long and passes into the base of posterior atrial gland. Two atrial glands with the usual mammillated surface. Ectally two glands appear united but can be separated after removal of the investing tissues, the common duct of atrial glands is thick, short, lateromesially flattened (fig. 11).

Moniligaster deshayesi Perrier, 1872 Material examined: KERL267A5, KERL0272A5 Sample ID with BOLD accession number: KERL0267A5 (ADH1656), KERL0272A (ADH1656) Collection site: Parambikulam Tiger Reserve (10º 23' 34.6'' N, 76º 46' 32.0'' E), Kerala, India.

Date of collection: 17 IX 2015 Diagnostic features: length 120–150; diameter 6 mm, segments 167–180. Colour dark blue. Dorsal pores absent. Setae closely paired, aa = bc; dd = slightly more than ½ circumference. Nephridiopores in ab or cd, no regular alternation. Clitellum not well marked. Male pores small in bc nearer to b.

Female pores indistinct in b. Spermathecal pores at c. Septa 4/5 and 5/6 fused at their peripheral attachment; 6/7–8/9 much thickened. Four gizzards in XV–XVIII. Testis sacs tubular sac like in 9/10.

Vas deferens very long, twisted into a number of hair–pin loops under the sac and passes down into a vertical column of leaflets. Prostate very large, sausage–shaped, extending back through several segments. Ovarian chamber present, ovisacs large

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extending back through several segments. Spermathecae with ovoid ampulla and coiled duct, which joins a bifurcation of the atrial gland in VII, which is large, bifid, each half compact and rounded with a yellowish mammillated surface, the stalk of the two halves unite to form a common duct (fig. 12).

Moniligaster gravelyi Stephenson, 1915 Material examined: KERL270A13, KERL270A14, KERL270A18, KERL270A19, KERL270A20 Sample ID with BOLD accession number: KERL0270A13 (ADH0515), KERL0270A14 (ADH0515), KERL0270A18 (ADH0515), KERL0270A19 (ADH0515), KERL0270A20 (ADH0515) Collection site: Shendurney Wildlife Sanctuary (8º 53' 03.7'' N, 77º 10' 03.3'' E), Kollam, Kerala, India.

Date of collection: 26 X 2015 Diagnostic features: length 80–120 mm; diameter 6 mm, segments 100–130. Colour dark bluish grey.

Dorsal pores absent. Setae very closely paired, aa = bc; dd = ½ circumference. Nephridiopores in ab or cd, no regular alternation. Male pores transversely placed slits on 10/11 in bc nearer to b, each aperture surrounded by finely wrinkled, annular band. Female pores nearer to b. Spermathecal pores median to c. Septa 6/7 is thickly muscular, 7/8–8/9 very thickly muscular. Five gizzards in XIII–XVII. Testis sacs ovoidal in IX–X. Vas deferens clusters of hair pin loops, enters prostate at its ectal end. Prostate extends back to XIII, large flattened, strap like with slight incisions of the lateral margins, narrower at the ectal end.

Ovarian chamber present, ovisacs large extending back through several segments. Atrial gland confi-

VII

1 mm Fig. 10. Microphotograph of atrial gland in Moniligaster sp.

Fig. 10. Microfotografía de la glándula accesoria de Moniligaster sp.

ned to VII, single or indistinctly bifid (demarcated by transverse furrow) with mamillated surface, a short moderately stout duct being given off from its under surface, spermathecal duct joins atrial gland on its upper end of demarcation (fig. 13).

spp

atr

VIII IX X XI

amp mp

spd

1 mm A

prs

atrgl

1 mm

vd

B

1 mm C

Fig. 11. Camera lucida sketch of Moniligaster aiyeri: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 11. Dibujo con cámara lúcida de Moniligaster aiyeri: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

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atr

VII

tss vd

spp

VIII IX X

mp

XI

amp 1 mm

1 mm

1 mm

prs

spd

A

B

C

Fig. 12. Camera lucida sketch of Moniligaster deshayesi: A, ventral view; B, spermathecae; C, testis sac with prostate. (For abbreviations, see Material and methods).

Fig. 12. Dibujo con cámara lúcida de Moniligaster deshayesi: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

Molecular characterization and census of Moniligastrids of the study area From the study area, the investigation revealed eleven species belonging to the family Moniligastridae. Out of them eight species were recorded in genus Drawida (D. brunnea, D. circumpapillata, D. ghatensis, D. im-

pertusa, D. nilamburensis, D. robusta, D. scandens, D. travancorense) and three in the genus Moniligaster (M. aiyeri, M. deshayesi, M. gravelyi). The average nucleotide compositions were G = 18.18 %, C = 23.43 %, A = 25.21 %, T = 32.43 % and mean GC% detected was 42.43%, which is normally observed in earthworms (Thakur et al., 2020). The 56 COI

atr VII

vd

spp

tss

amp

VIII IX X XI

1 mm A

prs

spd

mp 1 mm

B

1 mm C

Fig. 13. Camera lucida sketch of Moniligaster gravelyi: A, ventral view; B, spermathecae; C, testis sac and prostate. (For abbreviations, see Material and methods).

Fig. 13. Dibujo con cámara lúcida de Moniligaster gravelyi: A, vista ventral; B, espermateca; C, saco testicular con próstata. (Para las abreviaturas, véase Material and methods).

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Table 3. The average percentage of K2P intra (shaded diagonally) and interspecific distance at 1,000 bootstrap replicates of moniligastrids from Kerala, Western Ghats.

Tabla 3. El porcentaje medio de la distancia calculada con el modelo K2P dentro de una misma especie (celdas sombreadas en diagonal) y entre especies con 1.000 réplicas bootstrap de los moniligástridos de Kerala, en Western Ghats.

dataset with average intraspecific as well as average interspecific evolutionary distances revealed by K2P distance summary were 1.2 % and 22 %. The lowest interspecific K2P distance recorded was 5.58 % between D. ghatensis and D. impertusa. The highest interspecific distance was 35 % between D. japonica and M. deshayesi. Similarly, the highest intraspecific distance was 7.5 % in D. ghilarovi followed by D. japonica (6.9 %) and D. impertusa (4 %). Furthermore, the average K2P distance at 1,000 bootstrap replicates of moniligastrids is shown in table 3. Barcode gap analysis suggested a clear barcode gap of 2–5 % showing no overlapping interactions between evolutionary distances of sequences (table 4, fig. 14). The phylogenetic analysis showed full support for each taxon and there were minor differences in topologies of NJ (fig. 15) and ML (fig. 16) trees. In addition, all the species represented separate clades and were fully recovered on both NJ and BI trees.

Discussion Earthworms are one of the most valuable soil animals but their characteristics and burrowing nature makes their taxonomy difficult, resulting in a massive underestimation of the true level of earthworm diversity (Sket, 1999). The DNA barcodes combined with the classical morpho–anatomic screening, the

integrative approach, would aid in better estimate earthworm diversity (Dayrat, 2005; Lone et al., 2020).

The reliability of the DNA barcode as a data source for species delimitation depends on the barcode gap, which is a marked discontinuity between the values of intraspecific and interspecific divergences.

A clear break between intraspecific and interspecific divergences improves confidence of species delimitation and identification (Hebert et al., 2004; Meier et al., 2008). In our study, BGA suggested a barcode gap of 2–5 % with no overlap, which support the accuracy of DNA barcoding to delimit moniligastrid taxa. Furthermore, in DNA barcoding, species are distinct from their nearest neighbours (NN) if their maximum intraspecific distance is less than the distance to their nearest neighbour sequence (Ashfaq et al., 2014). Similar observations were seen in our report (table 4) where all the intraspecific distances were less than to their nearest neighbour (NN), which further support DNA barcoding for species delimitation of earthworms. The interspecific K2P genetic distances among the moniligastrid species ranged between 5.6 % and 34.0 % (table 3). The smallest K2P interspecific distance was 5.6 %, observed between D. impertusa and D. ghatensis.

Owing to their smallest interspecific distances they appeared closest on ML and NJ trees. Conversely, the highest interspecific K2P distance was 34.0 % between D. japonica and M. deshayesi followed

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Table 4. Barcode gap analysis based on K2P showing distances to nearest neighbour (NN). (If the species is a singleton, intra–specific values are shown with N/A).

Tabla 4. Análisis de deficiencias del código de barras basado en el modelo K2P en el que se muestran las distancias al vecino más cercano (NN). (Si la especie solo cuenta con un individuo, el valor intraespecífico se indica con 'N/A').

Species N

Mean intra–specific distance (%)

Min inter–specific distance (%) NN

D. brunnea 1 N/A D. circumpapillata 1 N/A D. ghatensis 6 0.25 D. impertusa 5 0.36 D. nilamburensis 1 N/A D. robusta 2 0.16 D. scandens 1 N/A D. travancorense 1 N/A M. aiyeri 3 0 M. deshayesi 2 0.31 M. gravelyi 5 0.1

by D. japonica and D. gracilis 33.9 %. The highest K2P intraspecific distance was found in D. ghilarovi.

This could be explained by the presence of different morphs and therefore a species complex (Blakemore et al., 2014). Moreover, except for D. japonica and D. ghilarovi, all the studied moniligastrids had low intraspecific genetic distances. Moreover, the NJ and ML phylogenetic trees' topologies further confirmed that these eleven species were distinct evolutionary units. All species were recovered as clade. However, it appears that Moniligaster may need revision, as the representatives used here nested within Drawida. In recent times, the use of molecular identification has increased, along with morphological characteristics, to differentiate earthworm species and to detect cryptic species (Decaëns et al., 2013).

Progress in molecular taxonomy of earthworms of India has been ad hoc. The fact that we do not know the full systematic inventory the soil biota generally, and especially the key earthworms, is an oversight that urgently needs to be redressed. Each ecosystem is composed of populations of species and each species has its particular ecological requirements and responses. Earthworms in general are keystone animals in nutrient cycling processes due to their role as major detritivores (i.e., feeding on dead and decaying matter, including dung). Correct species identification is important to accurate ecological study that we need as a first step to fully understanding, appreciating and utilizing this natural and national resource appropriately. DNA barcoding is an indispensable tool for its speed and accuracy, but only after the initial vouchers are correctly identified. Thus, the present study has been taken to provide a baseline status survey of ear-

0 0 0.47 0.63 0 0.16 0 0 0 0.31 0.16

Distance to NN

M. aiyeri 23.06 M. gravelyi 19.5 D. impertusa 5.53 D. ghatensis 5.53 D. travancorense 19.62 D. impertusa 16.43 M. aiyeri 23.1 M. aiyeri 19.27 D. travancorense 19.27 D. nilamburensis 22.72 D. circumpapillata 19.5

thworm diversity using molecular tools. Identification using molecular data helps to morphologically identify variable individuals of the same species, juvenile specimens and cocoons. In the case of earthworms, the classical standards of taxonomy are mainly based on genital structures, while the collection of the sexually developed worms is uncertain. Therefore, the generation of a DNA database of sequences of earthworms is advantageous and inevitable. The study presents eleven earthworm species belonging to two genera of the family Moniligastridae, represents about 55 % of this family (20 species) (Blakemore, 2007; Narayanan et al., 2016) and about 2.5 % (435 species/subspecies) of the country (Thakur and Yadav, 2018). It is noteworthy that Kerala possesses about 50.5 % of the earthworm diversity found in the Western Ghats biodiversity hotspot (Julka et al., 2009; Nair et al., 2010). The giant earthworm species Drawida nilamburensis about 75 cm body length, native to Kerala, is reported in this study.

The study explored eight different sites in the State of Kerala. Other regions, especially western and south–western parts of the state remain unexplored and need to be investigated further. All recorded species were endemic, indicating undisturbed habitats within the protected areas of Kerala. Moreover, of the eleven earthworm species reported in this study, COI sequences of only three species (D. ghatensis, D. impertusa and D. travancorense) are available in the NCBI database, which indicates limited availability of molecular analysis and assessment of earthworm diversity in Kerala. Some recent reports on earthworm diversity are available, however, based on morphological observations (Narayanan et al., 2016,

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A

Mean intraspecific

80 60 40 20 0

100 90 80 70 60 50 40 30 20 10 0

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 Genetic divergence (%, K2P) Distance to NN

Frequency (%)

B

133

100 90 80 70 60 50 40 30 20 10 0 1 2 3 4 5 6 7 Genetic

Intraspecific Interspecific

Frequency (%)

C

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 Genetic divergence (%, K2P)

8 9 10 11 12 13 14 15 16 17 18 19 20 divergence (%, K2P)

Fig. 14. Histogram of barcode gap analysis of Moniligastrids based on K2P distance from Kerala: A, mean intraspecific genetic divergence; B, distance to nearest neighbour; C, distributions of intraspecific and interspecific genetic divergences based on 28 mitochondrial COI sequences for 11 species of Moniligastrids.

Fig. 14. Histograma del análisis de deficiencias del código de barras de los moniligástridos de Kerala basado en la distancia calculada con el modelo K2P: A, promedio de la divergencia genética intraespecífica; B, distancia al vecino más cercano; C, distribución de las divergencias genéticas interespecíficas e intraespecíficas basadas en 28 secuencias mitocondriales COI para 11 especies de Moniligastridos.

2017). The present study fills the gap of molecular taxonomy of earthworms, with 28 COI datasets of endemic earthworms of Kerala having been generated. The findings may serve as a reference library of genomic signatures of earthworms in the study area, providing data for taxonomic assessments, phylogeny, molecular identification, dispersal, and population dynamics. Yet, in total of 83 species of moniligastrids are known from India, but none ones given here are barcoded and published. An integrative taxonomic classification, incorporating morphological classification, DNA barcoding and phylogeny is especially useful when working on a

huge variety of endemic fauna, where records are scanty. Furthermore, threats to biodiversity have already raised alarms with respect to the conservation of biodiversity and much emphasis has been given to endemic species. Considering the high diversity of earthworms (e.g. Blakemore, 2000; Chang et al., 2008), biomass (e.g. Brockie and Moeed, 1986) and ecosystem functioning (Boyer and Wratten, 2010) are likely to be threatened with extinction. The genomic signature of these species may not only delimit earthworm species but could be used in various other fields such as conservation strategies, toxicological research, and bioremediations.

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IEW433–17 | Drawida ghatensis IEW434–17 | Drawida ghatensis 99 IEW386–17 | Drawida ghatensis Drawida ghatensis IEW435–17 | Drawida ghatensis 47 IEW432–17 | Drawida ghatensis 99 47 IEW436–17 | Drawida ghatensis 52 IEW391–17 | Drawida impertusa IEW393–17 | Drawida impertusa Drawida impertusa 99 IEW448–17 | Drawida impertusa 47 IEW424–17 | Drawida impertusa 80 IEW447–17 | Drawida impertusa IEW444–17 | Drawida robusta Drawida robusta 99 IEW445–17 | Drawida robusta GBAN41623–13 | Drawida gracilis 99 GBMIN1572–12 | Drawida gracilis Drawida circumpapillata IEW420–17 | Drawida circumpapillata 60 IEW404–17 | Moniligaster gravelyi IEW446–17 | Moniligaster gravelyi Moniligaster gravelyi 99 IEW410–17 | Moniligaster gravelyi 57 IEW405–17 | Moniligaster gravelyi 36 IEW409–17 | Moniligaster gravelyi 99 IEW382–17 | Moniligaster deshayesi Moniligaster deshayesi IEW415–17 | Moniligaster deshayesi Drawida scandens IEW451–17 | Drawida scandens IEW437–17 | Moniligaster aiyeri 99 Moniligaster aiyeri IEW438–17 | Moniligaster aiyeri IEW369–17 | Moniligaster aiyeri Drawida travancorense IEW425–17 | Drawida travancorense Drawida nilamburensis IEW459–17 | Drawida nilamburensis 99 GBMIN1576–12 | Drawida bullata GBAN4160–13 | Drawida bullata IEW388–17 | Drawida brunnea Drawida brunnea GBMNC21048–20 | Drawida nepalensis GBMNC21044–20 | Drawida nepalensis 99 GBMNC21045–20 | Drawida nepalensis 95 GBMNC21049–20 | Drawida nepalensis 99 GBAN13883–19 | Drawida ghilarovi GBAN13885–19 | Drawida ghilarovi GBAN13901–19 | Drawida ghilarovi 99 GBAN13861–19 | Drawida ghilarovi GAHAP1854–14 | Drawida hattamimizu 99 GAHAP1601–14 | Drawida hattamimizu 80 GAHAP1856–14 | Drawida hattamimizu 93 GAHAP1645–14 | Drawida hattamimizu 69 GAHAP1649–14 | Drawida hattamimizu GBAN10080–19 | Drawida gisti 99 GBAN10081–19 | Drawida gisti 39 GBAN10093–19 | Drawida japonica 36 GBAN10095–19 | Drawida japonica 99 GBAN10094–19 | Drawida japonica GBAN10096–19 | Drawida japonica 92 GBMNC20866–20 | Drawida koreana GBMNC20864–20 | Drawida koreana 99 GBMNC20863–20 | Drawida koreana 68 GBMNC20867–20 | Drawida koreana Out–group MF983247.1 Mollusca sp.

54 49

85 36 19

54 65

20

29 44

19

1 49 6 56

99 54

97

0.05

Fig. 15. Neighbour–joining tree containing 56 COI dataset at 1,000 bootstrap analysis in MEGA X with Mollusca sp. as out–group.

Fig. 15. Árbol producido mediante el método de unión de vecinos que contiene el conjunto de datos de 56 COI obtenido con un análisis de bootstrap de 1.000 réplicas en MEGA X con especies del filo Mollusca como grupo externo.

Animal Biodiversity and Conservation 44.1 (2021)

95 69

0.20

IEW433–17 | Drawida ghatensis IEW434–17 | Drawida ghatensis 99 IEW386–17 | Drawida ghatensis IEW435–17 | Drawida ghatensis 99 IEW432–17 | Drawida ghatensis 51 IEW436–17 | Drawida ghatensis 60 IEW391–17 | Drawida impertusa IEW393–17 | Drawida impertusa 64 IEW448–17 | Drawida impertusa 99 IEW424–17 | Drawida impertusa 84 IEW447–17 | Drawida impertusa 34 IEW444–17 | Drawida robusta 99 IEW445–17 | Drawida robusta GBAN4163–13 | Drawida gracilis 27 99 GBMIN1572–12 | Drawida gracilis IEW420–17 | Drawida circumpapillata 69 IEW404–17 | Moniligaster gravelyi IEW446–17 | Moniligaster gravelyi 73 15 IEW405–17 | Moniligaster gravelyi 99 IEW409–17 | Moniligaster gravelyi IEW410–17 | Moniligaster gravelyi 35 IEW425–17 | Drawida travancorense 6 IEW459–17 | Drawida nilamburensis IEW382–17 | Moniligaster deshayesi 18 99 IEW415–17 | Moniligaster deshayesi GBMNC21048–20 | Drawida nepalensis 59 GBMNC21044–20 | Drawida nepalensis 99 GBMNC21045–20 | Drawida nepalensis GBMNC21049–20 | Drawida nepalensis 99 IEW437–17 | Moniligaster aiyeri IEW438–17 | Moniligaster aiyeri IEW369–17 | Moniligaster aiyeri 25 6 IEW451–17 | Drawida scandens IEW388–17 | Drawida brunnea 23 GBMIN1576–12 | Drawida bullata 36 99 GBAN4160–13 | Drawida bullata 99 GBAN13883–19 | Drawida ghilarovi 60 GBAN13885–19 | Drawida ghilarovi 99 GBAN13901–19 | Drawida ghilarovi 99 GBAN13861–19 | Drawida ghilarovi GAHAP1854–14 | Drawida hattamimizu 56 GAHAP1601–14 | Drawida hattamimizu 99 GAHAP1645–14 | Drawida hattamimizu 98 GAHAP1649–14 | Drawida hattamimizu GAHAP1856–14 | Drawida hattamimizu GBAN10080–19 | Drawida gisti 99 GBAN10081–19 | Drawida gisti 34 GBAN10093–19 | Drawida japonica 51 GBAN10095–19 | Drawida japonica 99 GBAN10094–19 | Drawida japonica GBAN10096–19 | Drawida japonica GBMNC20866–20 | Drawida koreana GBMNC20864–20 | Drawida koreana GBMNC20863–20 | Drawida koreana GBMNC20867–20 | Drawida koreana MF983247.1 Mollusca sp.

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Drawida ghatensis

Drawida impertusa

Drawida robusta

Drawida circumpapillata Moniligaster gravelyi Drawida travancorense Drawida nilamburensis Moniligaster deshayesi

Moniligaster aiyeri Drawida scandens Drawida brunnea

Out–group

Fig. 16. Maximum likelihood tree containing 56 COI dataset at 1,000 bootstrap analysis in MEGA X with Mollusca sp. as out–group.

Fig. 16. Árbol producido mediante el método de la máxima verosimilitud que contiene el conjunto de datos de 56 COI obtenido con un análisis de bootstrap de 1.000 réplicas en MEGA X con especies del filo Mollusca como grupo externo.

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Conclusion This study used the DNA sequence of a 650 bp fragment of the COI gene to delimit the species of native moniligastrid earthworms in the state of Kerala, a component of the Western Ghats biodiversity hotspot. The genomic signatures of eight Drawida species (D. brunnea, D. circumpapillata, D. ghatensis, D. impertusa, D. nilamburensis, D. robusta, D. scandens, and D. travancorense) and three Moniligaster species (M. aiyeri, M. deshayesi, and M. gravelyi) are provided.

The results of this study may serve as a reference library for moniligastrid earthworms within Kerala State and help to strengthen the fidelity of morpho–anatomical identification.

Acknowledgements The authors are thankful to Principal Chief Conservator Forest (PCCF), Kerala and Department of Biotechnology, Ministry of Science and Technology, Government of India, New Delhi for the financial support to carry out the study.

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Comunicacions breus Les comunicacions breus seguiran el mateix procediment que els articles i tindran el mateix procés de revisió. No excediran de 2.300 paraules incloent–hi títol, resum, capçaleres de taula, peus de figura, agraïments i referències. El resum no ha de passar de 100 paraules i el nombre de referències ha de ser de 15 com a màxim. Que el text tingui apartats és opcional i el nombre de taules i/o figures admeses serà de dos de cada com a màxim. En qualsevol cas, el treball maquetat no podrà excedir les quatre pàgines.

Animal Biodiversity and Conservation 44.1 (2021)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (antes Miscel·lània Zoològica) es una revista interdisciplinar, publicada desde 1958 por el Museu de Ciències Naturals de Barcelona. Incluye artículos de investigación empírica y teórica en todas las áreas de la zoología (sistemática, taxonomía, morfología, biogeografía, ecología, etología, fisiología y genética) procedentes de todas las regiones del mundo. La revista presta especial interés a los estudios que planteen un problema nuevo o introduzcan un tema nuevo, con hipòtesis y prediccions claras, y a los trabajos que de una manera u otra tengan relevancia en la biología de la conservación. No se publicaran artículos puramente descriptivos, o artículos faunísticos o corológicos en los que se describa la distribución en el espacio o en el tiempo de los organismes zoológicos. Esos trabajos deben redirigirse a nuestra revista hemana Arxius de Miscel·lània Zoològica (www.amz. museucienciesjournals.cat). Los estudios realizados con especies 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 registrada en todas las bases de datos importantes y además está disponible gratuitamente en internet en www.abc.museucienciesjournals.cat, 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 garantizar su calidad. El proceso de revisión es rápido y constructivo, y se realiza vía correo electrónico siempre 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 propiedad de la revista. Ésta se reserva los derechos de autor, y ninguna parte del trabajo podrá ser reproducida sin citar su procedencia.

Los derechos de autor quedan reservados a los autores, quienes autorizan a la revista a publicar el artículo. Los artículos se publican con una Licencia Creative Commons Atribución 4.0 Internacional: no se podrá reproducir ni reutilizar ninguna de sus partes sin citar la 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. Debe incluirse, con el artículo, una carta donde conste que el trabajo versa sobre inves­ tigaciones originales no publi­cadas an­te­rior­mente y que se somete en exclusiva a Animal Biodiversity and Conservation. En dicha carta también debe constar, para trabajos donde sea necesaria la manipulación ISSN: 1578–665X eISSN: 2014–928X

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de animales, que los autores disponen de los permisos necesarios y que han cumplido la normativa de protección animal vigente. Los autores pueden enviar también sugerencias para asesores.

Las pruebas de imprenta enviadas a los autores deberán remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Publicar en Animal Biodiversity and Conservation es gratuito para los autores, sin embargo los gastos debidos a modificaciones sustanciales en las pruebas de im­pren­­ta, introducidas por los autores, irán a ­cargo de los mismos.

El primer autor recibirá una copia electrónica del trabajo en formato 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 ninguno, 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.

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. Se evitará el uso de términos extranjeros (p. ej.: latín, aleman,...).

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 designaciones 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, resultados y discusión). Se evitarán las © 2021 Museu de Ciències Naturals de Barcelona Papers are published under a Creative Commons Attribution 4.0 International License

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especulaciones y las citas bibliográficas. Irá encabezado por el título del trabajo en cursiva.

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.

Direccion postal del autor o autores, se publicarán tal como se indique en el manuscrito recibido.

Identificadores de investigador (ORCID, ResearchID…, al menos del investigador principal y de quien asuma la correspondencia posterior.

(Título, Nombre de los autores, Abstract, Key words, Resumen, Palabras clave, Direcciones postalo e Identificadores de investigador conformarán la primera página.)

Introducción. En ella se dará una idea de los antecedentes del tema tratado, así como de los objetivos del trabajo.

Material y métodos. Incluirá la información referente a las especies estudiadas, aparatos utilizados, metodología de estudio y análisis de los datos y zona de estudio.

Resultados. En esta sección se presentarán únicamente los datos obtenidos que no hayan sido publicados previamente.

Discusión. Se discutirán los resultados y se compararán 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 species 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 conservation 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 variation 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. Animal Biodiversity and Conservation.

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 y 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.

Grandes cantidades de datos o tablas numéricas muy largas se publicarán como material suplementario. Este material suplementario sólo acompañará a la versión online del artículo, en ningún caso a la versión impresa.

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 fascículos recientes de la revista para seguir sus directrices.

Comunicaciones breves Las comunicaciones breves seguirán el mismo procedimiento que los artículos y serán sometidas al mismo proceso de revisión. No excederán las 2.300 palabras, incluidos título, resumen, cabeceras de tabla, pies de figura, agradecimientos y referencias.

El resumen no debe sobrepasar las 100 palabras y el número de referencias será de 15 como máximo.

Que el texto tenga apartados es opcional y el número de tablas y/o figuras admitidas será de dos de cada como máximo. En cualquier caso, el trabajo maquetado no podrá exceder las cuatro páginas.

Animal Biodiversity and Conservation 44.1 (2021)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an interdisciplinary journal published by the Museu de Ciències Naturals de Barcelona since 1958. It includes empirical and theoretical research from around the world that examines any aspect of Zoology (Systematics, Taxonomy, Morphology, Biogeography, Ecology, Ethology, Physiology and Genetics). It gives special emphasis to studies that expose a new problem or introduces a new topic, presenting clear hypotheses and predictions, and to studies related to Cconservation Biology. Papers purely descriptive or faunal or chorological describing the distribution in space or time of zoological organisms will not be published.

These works should be redirected to our sister magazine Arxius de Miscel·lània Zoològica (www.amz.museucienciesjournals.cat). 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 registered in all principal data bases and is freely available online at www.abc.museucienciesjournals.cat 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 property of the journal, which reserves copyright, and no published material may be reproduced or cited without acknowledging the source of information.

All rights are reserved by the authors, who authorise the journal to publish the article. Papers are published under a Creative Commons Attribution 4.0 International License: no part of the published paper may be reproduced or reused unless the source is cited.

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 document. 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 authorisations. Authors may suggest referees for their papers.

Proofs sent to the authors for correction should be returned to the Editorial Board within 10 days.

Publishing in Animal Biodiversity and Conservation is free of charge, but expenses due to any substantial ISSN: 1578–665X eISSN: 2014–928X

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alterations of the proofs will be charged to the authors.

The first author will receive electronic version of the article in PDF format.

Manuscripts 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 accepted.

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 untranslatable 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. Foreing terms (e.g. Latin, German,...) should not be used.

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 are proper nouns (e.g.

Iberian rock lizard).

Place names may appear either in their original form or in the language 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 consecutive days, e.g. 28th to 30th).

Footnotes should not be used.

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. © 2021 Museu de Ciències Naturals de Barcelona Papers are published under a Creative Commons Attribution 4.0 International License

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Author’s address will be published as they appear in the manuscript file.

Researcher’s identifiers (ORCID, ResearchID,…), at least from the first and the corresponding authors.

(Title, Name, Abstract, Key words, Resumen, Palabras clave and Author’s address and Researcher’s identifiers must constitute the first page) Introduction. Should include the historical background of the subject as well as the aims of the paper.

Material and methods. This section should provide relevant information on the species studied, materials, 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 bibliography 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 species 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 conservation biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt, J. D. Nichols, Eds.). Oxford University Press, Oxford. * PhD thesis: Merilä, J., 1996. Genetic and quantitative trait variation in natural bird populations. PhD 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. Animal Biodiversity and Conservation.

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 and 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, photographs) 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 tridimensional. 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.

Large amounts of data or long tables will be published as supplementary material. This supplementary material will accompany the online version of the article only, not the printed version.

Main headings (Introduction, Material and methods, Results, Discussion, Acknowledgements and References) 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.

Brief communications Brief communications should follow the same procedure as other articles and they will undergo the same review process. They should not exceed 2,300 words including title, abstract, figure and table legends, acknowledgements and references. The abstract should not exceed 100 words, and the number of references should be limited to 15. Section headings within the text are optional. Brief communications may have up to two figures and/or two tables but the whole paper should not exceed four published pages.

Animal Biodiversity and Conservation 44.1 (2021)

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Welcome to the electronic version of Animal Biodiversity and Conservation

Rec ele omme ctr nd o to you nic a c r li bra cess r y!

this

https://abc.museucienciesjournals.cat

Animal Biodiversity and Conservation joins the worldwide Open Access Initiative of providing a permanent online version free of charge and access barriers This is the result of the growing consensus that open access to research is essential for efficient and rapid scientific communication ABC alert, a free alerting service, provides e–mail information on the latest issue To sign on for this service, please send an e–mail to: abc@bcn.cat

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Animal Biodiversity and Conservation 44.1 (2021)

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 Abstracts, BIOSIS Previews, CiteFactor, Current Primate References, Current Contents/Agriculture, Biology & Environmental Sciences, Essential Science Indicators, Dialnet, DOAJ, DULCINEA, Ecological Abstracts, Ecology Abstracts, Entomology Abstracts, Environmental Abstracts, Environmental Periodical Bibliography, FECYT, Genetic Abstracts, Geographical Abstracts, Índice Español de Ciencia y Tecnología–ICYT, International Abstracts of Biological Sciences, International Bibliography of Periodical Literature, International Developmental Abstracts, Latindex, Marine Sciences Contents Tables, MIAR, Oceanic Abstracts, RACO, Recent Ornithological Literature, REBIUN, REDIB, Referatirnyi Zhurnal, ResearchGate, Responsible Journals, Science Abstracts, Science Citation Index Expanded, Scientific Commons, SCImago, SCOPUS, Serials Directory, SHERPA/RoMEO, Transpose, Ulrich's International Periodical Directory, WoS, Zoological Records

Consorci format per / Consorcio formado por / Consortium formed by:

Índex / Índice / Contents Animal Biodiversity and Conservation 44.1 (2021) ISSN 1578–665 X eISSN 2014–928 X 1–16 García–González, R. Herrero, J. Nores, C. The names of southwestern European goats: is Iberian ibex the best common name for Capra pyrenaica?

17–29 Dardanelli, S. Bellis, L. M. Nestedness structure of bird assemblages in a fragmented forest in Central Argentina: the role of selective extinction and colonization processes 31–43 Ramírez–Arrieta, V. M. Denis, D. Ferrer–Sánchez, Y. Evaluación de un protocolo automatizado para la obtención de medidas morfométricas de huevos de aves a partir de fotografías digitales 45–58 Guedes, J. J. M. Assis, C. L. Feio, R. N. Quintela, F. M. The impacts of domestic dogs (Canis familiaris) on wildlife in two Brazilian hotspots and implications for conservation 59–66 Goñi, L., González, S., Biescas, E., Villanúa, D., Arizaga, J. Variation in winter thrush abundance during the hunting season in southern Europe: the importance of hunting–free reserves 67–78 | GBIF: Data paper Popović, M., Micevski, B., Verovnik, R. Effects of elevation gradient and aspect on butterfly diversity on Galičica Mountain in the Republic of Macedonia (south–eastern Europe)

79–88 Drago, M. C., Vrcibradic, D. The importance of addressing different Red Lists in conservation studies: an analysis comparing the conservation status of Brazilian mammals 89–102 Zúñiga, A. H., Fuenzalida, V., Sandoval, R., Encina, F. Seasonal variation in the diet of two predators in an agroecosystem in southern–central Chile 103–108 Brief Communication Navalpotro, H., Mazzoni, D., Senar, J. C. A plastic device fixed around trees can deter snakes from predating bird nest boxes 109–115 Negro, J. J., Blázquez, M. C., Fernández–Alés, R., Martín–Vicente, A. Interspecific sexual selection, a new theory for an old practice: the increase of artificial biodiversity through creation of modern, standardized breeds 117–137 | GBIF: Data paper Thakur, S. S., Lone, A. R., Tiwari, N., Jain, S. K., James, S. W., Yadav, S. A contribution to the earthworm diversity (Clitellata, Moniligastridae) of Kerala, a component of the Western Ghats biodiversity hotspot, India, using integrated taxonomy

FUNDACIÓN ESPAÑOLA

Amb el suport de / Con el apoyo de / With the support of: FUNDACIÓN ESPAÑOLA PARA LA CIENCIA Y LA TECNOLOGÍA

Nº DE CERTIFICADO: FECYT-113/2020 FECHA DE CERTIFICACIÓN: 6 de octubre 2014 (4ª convocatoria) ESTA CERTIFICACIÓN ES VÁLIDA HASTA EL: 13 de julio de 2021