Defensive behavior in Leptodactylus vastus A. LuTZ, 1930 ... - Zobodat

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Nov 16, 2015 - Leptodactylus vastus A. LuTZ, 1930, in northeastern Brazil. The entire defensive repertoire of a species or a population typically evolves.

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J. C. & GRiffiTHS, R. A. (2000): Amphibians and reptiles: A natural history of the British herpetofauna. London (HarperCollins), pp. 270. BiLLE, T. (2008): Danmarks padder og krybdyr – en feltguide fra danske-dyr. dk; Næstved (ConDidact), pp. 55. BuSCHENDORf, J. (2004): Ringelnatter – Natrix natrix (LiNNAEuS, 1758); pp. 179-185. in: MEyER, f. & BuSCHENDORf, J. & ZuPPkE, u. & BRAuMANN, f. & SCHäDLER, M. & GROSSE, W.-R. (Eds.): Die Lurche und kriechtiere Sachsen-Anhalts – Verbreitung, Ökologie, Gefährdung und Schutz.- Supplement der Zeitschrift für feldherpetologie 3. Bielefeld (Laurenti). DüRiGEN, B. (1897): Deutschlands Amphibien und Reptilien. Eine Beschreibung und Schilderung sämmtlicher in Deutschland und den angrenzenden Gebieten vorkommenden Lurche und kriechthiere. Magdeburg (Creutz’sche Verlagsbuchhandlung), pp. 676. ECkSTEiN, H.-P. (1993): untersuchungen zur Ökologie der Ringelnatter (Natrix natrix LiNNAEuS, 1758).- Jahrbuch für feldherpetologie, Beiheft; 4: 1-145. fELLENBERG, W. (1981): Ringelnatter Natrix natrix (LiNNAEuS, 1758); pp. 137-150. in: fELDMANN, R. (Ed.): Die Amphibien und Reptilien Westfalens.- Abhandlungen aus dem Landesmuseum für Naturkunde zu Münster in Westfalen, Münster; 43. kABiSCH, k. (1999): Natrix natrix (LiNNAEuS, 1758) – Ringelnatter; pp. 513-580. in: BÖHME, W. (Ed.): Handbuch der Reptilien und Amphibien Europas; Band 3/iiA: Schlangen ii; Serpentes ii: Colubridae 2 (Boiginae, Natricinae). Wiebelsheim (AuLA-Verlag). ROLLiNAT, R. (1946): La vie des reptiles de la france Centrale; Paris (Librairie Delagrave), pp. 343. SCHLEiCH, H. H. & käSTLE, W. & kABiSCH, k. (1996): Amphibians and reptiles of North Africa; koenigstein (koeltz Scientific Books), pp. X, 1201. SMiTH, M. (1951): The British amphibians & reptiles; London (Collins), pp. xiv, 318. STEWARD, J. W. (1971): The snakes of Europe; Newton Abbot (David & Charles), pp. 238. STREET, D. (1979): The reptiles of northern and central Europe; London (B. T. Batsford), pp. 268. VAuGHAN, R. (2008): An incidence of Natrix natrix helvetica observed in arboreal mating.- Herpetological Bulletin, London; 103: 3738. VAuGHAN, R. (2012): Grass Snakes. Third Edition; Privately published, pp. 116. VEiTH, G. (1991): Die Reptilien Bosniens und der Herzegowina, Teil ii.Herpetozoa, Wien; 4: 1-96. WAiTZMANN, M. & SOWiG, P. (2007): Ringelnatter Natrix natrix (LiNNAEuS, 1758); pp. 667-686. in: LAufER, H. & fRiTZ, k. & SOWiG, P. (Eds.): Die Amphibien und Reptilien Baden-Württembergs; Stuttgart (Eugen ulmer). WiLDSCREEN ARCHiVE (2016): Grass snake (Natrix natrix). WWW document (movie), available at < http://www.arkive.org/grasssnake/natrix-natrix/video-06b.html > (Last accessed: March 28, 2016). ZiMMERMANN, R. (1908): Der deutschen Heimat kriechtiere und Lurche; Stuttgart (fritz Lehmann), pp. 191 pp. ZiMMERMANN, R. (1909): Zur Schlangenfauna von Rochlitz i. S.- Lacerta: Zeitschrift für Aquarien- und Terrarienkunde, Braunschweig; 21: 81-83, 22: 85-86. kEy WORDS: Reptilia: Squamata: Serpentes: Colubridae; Natrix natrix, height-seeking, climbing ability, arboreality, behavior, Denmark SuBMiTTED: November 16, 2015 AuTHORS: Henrik BRiNGSøE (Corresponding author, < [email protected] >) – irisvej 8, Dk-4600 køge, Denmark & Peter AASTRuP – Aarhus university, Department of Bioscience, frederiksborgvej 399, Dk4000 Roskilde, Denmark.

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Defensive behavior in Leptodactylus vastus A. LuTZ, 1930, in northeastern Brazil The entire defensive repertoire of a species or a population typically evolves due to strong selective pressure exerted by their natural predators (GREENE 1997; VAMOSi 2005). The most common defensive strategies of mobile animals are either to remain motionless or to try to escape from potential predators. However, a variety of defensive strategies can be used depending on the risk posed by the predator (TOLEDO et al. 2011). Anurans exhibit a variety of defensive behaviors (DODD 1976; WiLLiAMS et al. 2000; TOLEDO et al. 2005, 2010, 2011), including combinations of ecological, morphological, physiological, or behavioral characteristics (DuELLMAN & TRuEB 1994; TOLEDO & JARED 1995), and this flexibility may improve their chances of survival (MARCHiSiN & ANDERSON 1978). The skin of amphibians plays an important role in defense against predators and microorganisms possessing dermal mucous and granular glands responsible for the secretion of mucus and toxins, respectively (STEBBiNS & COHEN 1995; TOLEDO & JARED 1995; BARBOSA et al. 2015). A great variety of chemical compounds can be found in the secretion of granular glands. in many species these glands form aggregates, or macroglands (TOLEDO & JARED 1995), which are strategically placed on the body surface. in frogs of the family Leptodactylidae, macroglands are present on the skin of the dorsum (TOLEDO & JARED 1995) and usually exhibit bright colors that are exposed during deimatic behavior. This is a report on three observations of defensive behaviour exhibited by Leptodactylus vastus A. LuTZ, 1930, recorded in an area of the type “Brejo de Altitude”, in northeastern Brazil. Leptodactylus vastus is a leaf-litter frog of the L. pentadactylus group (LAuRENTi, 1768), and like other members of this group it is large, reaching about 20 cm snout-vent length (SVL) (HEyER 2005; DE Sá et al. 2014). This species is often found near water bodies in areas with typical Atlantic

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fig. 1: Leptodactylus vastus A. LuTZ, 1930, performing thanatosis. Photo by D. P. Castro.

forest and Caatinga phytophysiognomies (fROST 2015). it is widely distributed in the Brazilian state of Ceará, occurring in areas of Caatinga (BORGES-NOJOSA et al. 2010; SANTANA et al. 2015), coastal regions (BORGES-LEiTE et al. 2014) and “Brejos de Altitude” (BORGES-NOJOSA 2007; LOEBMANN & HADDAD 2010; RiBEiRO et al. 2012). On April 14, 2015, working in a project on beta diversity of litter amphibians in ubajara National Park (PARNA-ubajara), Ceará (03°50’24.9” S / 040°54’41.6” W), the authors observed an individual of L. vastus performing three types of defensive behavior when it was manipulated for taking photographs and body measurements in the laboratory. The first behavioral strategy was thanatosis (death feigning) by exposing its abdomen and retracting the front feet close to the body (fig. 1). This behavior lasted

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about seven minutes, after which the individual returned to a normal body position. After thanatosis, the specimen performed partial body-raising (TOLEDO et al. 2011), stretching its legs and lifting the body from the ground while keeping its snout in contact with the substrate. The individual remained motionless in this position for about five minutes, while the reddish color in its inguinal region was exposed (figs. 2 and 3). immediately after the specimen exhibited this posture, the manipulators began to feel their eyes and noses become irritated. Thanatosis is often displayed by amphibians (GALLy et al. 2014), and has been reported for multiple families, including Bufonidae (ZAMPROGNO et al. 1998), Cycloramphidae (HARTMANN et al. 2003), Hylidae (AZEVEDO-RAMOS 1995), Microhylidae (BORGES-LEiTE et al. 2012) and Odontophrynidae (BEZERRA et al. 2010; BORGES-NOJOSA et al. 2016). Remaining motionless can help avoid predators that are visually oriented or divert predator attention (MiyATAkE et al. 2009; TOLEDO et al. 2010). Records of thanatosis among leptodactylid frogs are common (TOLEDO et al. 2005) and have been recorded for Leptodactylus chaquensis CEi, 1950 (LOuRENçO-DE-MORAES et al. 2014), Leptodactylus fuscus (SCHNEiDER, 1799) (TOLEDO et al. 2010) and Leptodactylus mystacinus (BuRMEiSTER, 1861) (TOLEDO et al. 2010). Among the species of the L. pentadactylus group, only L. labyrinthicus (SPiX, 1824) has been reported to perform thanatosis (TOLEDO et al. 2005). However, to our knowledge, there are no previous reports of thanatosis behavior for L. vastus in the literature. The behavior of body-raising is cited by TOLEDO et al. (2011), as one of 30 defensive behaviors performed by amphibians. This behavior is usually exhibited by toxic species, and can be displayed in two different modes: (1) partial, when the individual stretches the legs vertically and maintains the snout close to or touching the ground and (2) full, when the individual extends both anterior and posterior limbs and raises its belly and snout (TOLEDO et al. 2011). This behavior is reported for the families Aromobatidae (TOLEDO et al. 2011) and Bufonidae (ESCOBAR-LASSO & GONZáLEZ-

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fig. 2: Leptodactylus vastus A. LuTZ, 1930, performing partial “body-raising”, keeping its snout touching the substrate while the hind legs remain extended. Photo by D. P. Castro.

fig. 3: Behavior of “body-raising” in Leptodactylus vastus A. LuTZ, 1930, showing how the individual exposes the reddish regions of the inguinal region while releasing noxious substances that irritate the mucous membranes of potential predators. Photo by D. P. Castro.

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DuRAN 2012), and is probably used to make subjugation more difficult when the individual is captured (TOLEDO et al. 2011) and seems to be closely associated with the presence of noxious or odoriferous skin secretions (HÖDL & AMéZquiTA 2001). The production of secretions which is also considered a method of defense for amphibians (TOLEDO et al. 2011) is described in Leptodactylidae (HADDAD et al. 2013), such as the species group of Leptodactylus latrans (STEffEN, 1815), the latter producing noxious secretions that leave the skin slippery (LOuRENçO-DE-MORAES et al. 2014). Members of the L. pentadactylus group, including L. vastus, also produce and secrete toxic substances from the skin (HADDAD et al. 2013). These substances can cause sensations of severe burning when in contact with the mouth, eyes or nostrils (TOLEDO et al. 2011; HADDAD et al. 2013), which is probably why frogs of this group are referred to as “pepper-frogs”. Combining different defensive strategies can increase the chances of escape from a predators’ attack (TOLEDO et al. 2011). According to TOLEDO et al. (2005), species within a group of closely related amphibian species can exhibit similar defensive strategies, which is a result of phylogenetic relationships rather than ecological niches. However, lack of knowledge of anti-predator behavior in different families of amphibians limits meta-analyses regarding defensive strategies (LOuRENçO-DE-MORAES et al. 2014). ACkNOWLEDGMENTS: The authors thank G. J. B. MOuRA and E. WiLD for reviewing the manuscript, field assistants and students of the NuROf-ufC for collaboration in the fieldwork; iCMBiO for issuing collection permits No. 39073; CAPES for doctoral scholarships granted to D. P. CASTRO; M. J. BorgesLeite and CNPq for financing of the project “Beta diversity of amphibians and lizards in altitudinal gradient in Northeast Brazil: implications for conservation of endangered species”. REfERENCES: AZEVEDO-RAMOS, C. (1995): Defensive behaviors of the Neotropical tree frog Hyla geographica (Anura, Hylidae).- Revista Brasileira de Biologia, Río de Janeiro; 55 (1): 45-47. BARBOSA, E. A. & iEMBRO, T. & MARTiNS, G. R. & SiLVA L. P. & PRATES, M. V. & ANDRADE, A. C. & BLOCH, C. (2015): Skin secretion peptides: The molecular facet of the deimatic behavior of the four-eyed frog, Physalaemus nattereri (Anura, Leptodactylidae).- Rapid Communications in Mass Spectrometry, Chichester; 29 (21): 2061-2068. BEZERRA, L. & AGuiAR, f. & CASCON, P.

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(2010): Odontophrynus carvalhoi (Carvalho’s Escuerzo) - defense.- Herpetological Review, New york; 41: 477. BORGES-LEiTE, M. J. & BORGES-NOJOSA, D. M. & RODRiGuES, J. f. M. & PRADO, f. M. V. (2012): On the occurrence of thanatosis in Elachistocleis piauiensis CARAMASCHi & JiM, 1983 (Anura: Microhylidae).- Herpetology Notes, Braunschweig; 5: 9-10. BORGES-LEiTE, M. J. & RODRiGuES, J. f. M. & BORGES-NOJOSA, D. M. (2014): Herpetofauna of a coastal region of northeastern Brazil.- Herpetology Notes, Braunschweig; 7: 405-413. BORGES-NOJOSA, D. M. & CARVALHO Jr., R. R. & BORGES-LEiTE, M. J. & LiMA, D. C. & MELO, J. C. L. (2016): Defensive behavior in two species of Odontophrynus REiNHARDT & LuTkEN, 1862 (Anura: Odontophrynidae).- Herpetology Notes, Braunschweig; 9: 67-71. BORGES-NOJOSA, D. M. & PRADO, f. M. V. & BORGES-LEiTE, M. J. & GuRGELfiLHO, N. M. & BACALiNi, P. (2010): Avaliação do impacto do manejo florestal sustentável na herpetofauna de duas áreas de caatinga nos municípios de Caucaia e Pacajus no Estado do Ceará; pp. 315.330. in: GARiGLiO, M. A. & SAMPAiO, E. V. S. B & CESTARO, L. A. & kAGEyAMA, P. y. (Org.): uso sustentável e conservação dos recursos florestais da Caatinga. Brasilia (Serviço Brasileiro florestal). DE Sá, R. O. & Grant, T. & CAMARGO, A. & HEyER, W. R. & PONSSA, M. L & STANLEy, E. (2014): Systematics of the Neotropical genus Leptodactylus fiTZiNGER, 1826 (Anura: Leptodactylidae): Phylogeny, the relevance of non-molecular evidence, and species accounts.- South American Journal of Herpetology, Washington; 9 (1): 1-128. DODD, C. k. (1976): A bibliography of anuran defensive mechanisms.- Smithsonian Herpetological information Service, Washington; 37: 1-10. DuELLMAN, W. E. & TRuEB, L. (1994): Biology of amphibians. Baltimore, London (Johns Hopkins university Press), pp. 670. ESCOBAR-LASSO, S. & GONZáLEZDuRAN, G. A. (2012): Strategies employed by three Neotropical frogs (Amphibia: Anura) to avoid predation.- Herpetology Notes, Braunschweig; 5: 79-84. GALLy, M. & ZiNA, J. & MiRA-MENDES, C. V. & SOLé, M. (2014): Legs-interweaving: An unusual defense behavior of anurans displayed by Agalychnis aspera (PETERS, 1893).- Herpetology Notes, Braunschweig; 7: 623-625. GREENE, H. W. (1997): Snakes. The evolution of mystery in nature. Berkeley (university of California Press), pp. 351. HADDAD, C. f. B. & TOLEDO, L. f. & PRADO, C. P. A. & LOEBMANN, D. & GASPARiNi, J. L. & SAZiMA, i. (2013): Guia dos anfíbios da Mata Atlântica: Diversidade e biologia. São Paulo (AnolisBooks), pp. 544. HARTMANN, M. T. & HARTMANN, P. A. & PRADO, C. P. A. & GARCiA, P. C. A. (2003): Cycloramphus boraceiensis (flattened Waterfall frog). Defensive behavior.- Herpetological Review, New york; 33: 198. HEyER, W. R. (2005): Variation and taxonomic clarification of the large species of the Leptodactylus pentadactylus species group (Amphibia: Leptodactylidae) from Middle America, northern South America, and Amazonia.- Arquivos de Zoologia, São Paulo; 37: 269-348. HÖDL ,W. & AMéZquiTA, A. (2001): Visual signaling in anuran amphibians; pp. 21-141. in: RyAN, M. J. (Ed.): Anuran communication. Washington (Smithsonian institution Press). LOEBMANN, D. & HADDAD, C. f. B. (2010): Amphibians and reptiles from a highly diverse area of the Caatinga domain: composition and conservation implications.- Biota Neotropica, Campinas; 10 (3):

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227-256. LOuRENçO-DE-MORAES, R. & BATiSTA, V. G. & fERREiRA, R. B. (2014): Defensive behaviors of Leptodactylus chaquensis (Anura: Leptodactylidae).Herpetology Notes, Braunschweig; 7: 391-392. MARCHiSiN, A. & ANDERSON, J. D. (1978): Strategies employed by frogs and toads (Amphibia, Anura) to avoid predation by snakes (Reptilia, Serpentes).- Journal of Herpetology, Houston; 12 (2): 151-155. MiyATAkE, T. & NAkAyANA, S. & NiSHi, y. & NAkAJiMA, S. (2009): Tonically immobilized selfish prey can survive by sacrificing others.- Proceedings of the Royal Society, London; (B) 276: 2762-2767. RiBEiRO, S. C. & ROBERTO, i. J. & SALES, D. L. & áViLA, R. W. & ALMEiDA, W. O. (2012): Amphibians and reptiles from the Araripe bioregion, northeastern Brazil.- Salamandra, Mannheim; 48 (3): 133-146. SANTANA, D. J. & MâNGiA, S. & SiLVEiRA-fiLHO, R. R. & BARROS, L. C. S. & ANDRADE, i. & NAPOLi, M. f. & JuNCá, f. & GARDA, A. A. (2015): Anurans from the middle Jaguaribe River region, Ceará state, northeastern Brazil.- Biota Neotropica, Campinas; 15 (3): 1-8. STEBBiNS, R. C. & COHEN, N. W. (1995): A natural history of amphibians. Princeton (Princeton university Press), pp. 316. TOLEDO, R. C. & JARED, C. (1995): Cutaneous granular glands and amphibian venoms.- Comparative Biochemistry and Physiology, London; 111A (1): 1-29. TOLEDO, L. f. & SAZiMA, i. & HADDAD, C. f. B. (2011): Behavioral defences of anurans: an overview.Ethology Ecology & Evolution, Abingdon; 23: 1-25. TOLEDO, L. f. & TOZETTi, A. M. & ZiNA, J. (2005): Leptodactylus labyrinthicus (Pepper frog): Repertoire of defensive behavior.- Herpetological Bulletin, London; 91: 30-31. TOLEDO, L. f. & SAZiMA, i. & HADDAD, C. f. B. (2010): is it all death feigning? Case in anurans.- Journal of Natural History, London; 44 (31-32): 1979-1988. VAMOSi, S. M. (2005): On the role of enemies in divergence and diversification of prey: a review and synthesis.- Canadian Journal of Zoology, Ottawa; 83: 894-910. WiLLiAMS, C. R. & BRODiE Jr. E. D. & TyLER, M. J. & WALkER, S. J. (2000): Antipredator mechanisms of Australian frogs.- Journal of Herpetology, Houston; 34 (3): 431-443. ZAMPROGNO, C. & ZAMPROGNO, M. G. f. & TEiXEiRA, R. L. (1998): Bufo paracnemis (Sapo-boi). Death feigning.- Herpetological Review; New york; 29 (2): 96-97. kEy WORDS: Amphibia: Anura: Leptodactylidae; Leptodactylus vastus; ethology, antipredator behavior, body-raising, thanatosis; Brazil SuBMiTTED: May 30, 2016. AuTHORS: Déborah P. DE CASTRO 1, 2) (Corresponding author, < [email protected] >), Diva M. BORGES-NOJOSA 1, 2), John A. A. OLiVEiRA 2), Maria J. BORGES-LEiTE 1, 2), Margarida M. X. DA SiLVA 2), Tiago A. DE SOuSA 1, 2) & David James HARRiS 3) 1) Programa de Pós-Graduação em Ecologia e Recursos Naturais, universidade federal do Ceará. Campus do Pici, Bloco 906, CEP 60.455-760, fortaleza - CE, Brazil; 2) Núcleo Regional de Ofiologia, universidade federal do Ceará (NuROf-ufC) Campus do Pici, Bloco 905, CEP 60.455-760, fortaleza - CE, Brazil; 3) Centro de investigação da Biodiversidade e Recursos Genéticos (CiBiO). universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando quintas, CEP 4485-661, Vairão, Portugal.

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first record of bluish Podarcis muralis (LAuRENTi, 1768) Lizard coloration depends on the combined action of three classes of pigment or light-reflecting cells (i.e., chromatophores) located in the dermal layer of the skin. The xantophores are the most superficial and contain pigments (i.e., pteridines and/or carotenoids) that absorb short-wavelength light and reflect long wavelengths. iridophores contain intracellular guanine platelets that scatter the incident light. Melanophores occupy a basal position in the dermis and contain eumelanin that absorbs all light transmitted by the xantophores and the iridophores (COOPER & GREENBERG 2002; GRETHER et al. 2004). Variation in the abundance and in the spatial arrangement of these cell types can produce the great array of skin colors found in lizards (e.g., SAENkO et al. 2013). Blue coloration has long attracted the attention of researchers and herpetoculturists due, among other reasons, to the fact that blue pigments are almost absent in nature (BAGNARA 2007; uMBERS 2013; but see GODA & fuJi 1995). in vertebrates, blue is generally thought to be a structural color that results from selective light scattering by nanoscale elements that differ in refractive index (BAGNARA 2007). in particular, shortwavelength colors (blue and ultravioletblue) in lizards are structural colors produced by light scattering in the iridophores, although these colors also depend on interactions with xanthophores and the underlying layer of melanophores (MENTER et al. 1979; kuRiyAMA et al. 2006; BAGNARA et al. 2007). in Anolis carolinensis VOiGT, 1832, the isolated iridophores appear blue-green under reflected light, and the color intensifies if a layer of melanophores is added under the iridophores (presumably due to absorption of longer wavelengths, ROHRLiCH & PORTER 1972; ROHRLiCH 1974). The addition of xanthophores containing yellow pigments results in the normal brown-green skin color of the species. These results suggest that blue colors are produced when xanthophores contain few or no pigments (allowing almost all wavelengths of the incident light to interact directly with the iridophores). Consequently, the term axan-

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