Death-feigning behaviour in Iphisa elegans: the second reported case in the Family Gymnophthalmidae (Reptilia: Squamata)

Comportamento de tanatose em Iphisa elegans: o segundo caso na Família Gymnophthalmidae (Reptilia: Squamata)

Paulo Roberto MACHADO-FILHO Guilherme Marson MOYA Fábio MAFFEI About the authors

ABSTRACT

Death-feigning behaviour occurs when the animal simulates a state of immobility. This behaviour is described for some lizard families, among them the family Gymnophthalmidae with only one record. Iphisa elegans is a diurnal and terrestrial Amazonian gymnophtalmid lizard. It has cryptic behavior and moves rapidly on the ground, hindering observations of its behavior. We report a case at the Comodoro Municipality, Mato Grosso State, Brazil. An adult male of I. elegans, when manipulated, turned its venter up and put itself in a death-feigning posture. This species is preyed upon by birds, snakes and other lizards¸ possibly behaving this way when the cryptic behaviour or escape attempt fails. More studies are necessary to evaluate the efficiency of this behaviour, as well as its frequency of occurrence, using individuals of both sexes. We also suggest to evaluate if the orange venter of males could have any antipredation advantage.

KEYWORDS:
reptiles; Ethology; antipredator display; lizard; thanatosis

RESUMO

Fingir-se de morto é um comportamento no qual o animal simula um estado de imobilidade. Esse comportamento é descrito em algumas famílias de lagartos, dentre as quais, a família Gymnophthalmidae com apenas um registro. Iphisa elegans é um lagarto gymnoftalmídeo amazônico diurno e terrestre. Possui comportamento críptico e move-se rapidamente pelo solo, dificultando observações de seu comportamento. Reportamos um caso no município de Comodoro, Estado do Mato Grosso, Brasil: um macho adulto de I. elegans, quando manipulado, virou seu ventre para cima e fingiu-se de morto. Esta espécie é predada por pássaros, serpentes e outros lagartos, possivelmente portando-se dessa forma quando o comportamento críptico ou tentativa de fuga falham. São necessários mais estudos para observar a eficiência desse comportamento, assim como sua frequência de ocorrência, usando indivíduos de ambos os sexos. Também sugerimos que deve ser avaliado se a coloração alaranjada no ventre dos machos poderia fornecer alguma vantagem antipredação.

PALAVRAS-CHAVE:
répteis; Etologia; comportamento antipredação; lagarto; tanatose

Death-feigning behaviour (thanatosis) occurs when the animal simulates a state of immobility (i.e. pretending to be dead) in response to external stimuli (Santos et al. 2010Santos, M.B.; Oliveira, M.C.L.M.; Verrastro, L.; Tozetti, A.M. 2010. Playing dead to stay alive: thanatosis in Liolaemus occipitalis (Squamata: Liolaemidae). Biota Neotropica, 10: 361-364. ). This behaviour could be effective against predators that do not feed on carrion or dead prey, and against those which need movement cues to find and handle further their prey (Toledo et al. 2011Toledo, L.F.; Sazima, I.; Haddad, C.F.B. 2011. Behavioural defenses of anurans: an overview. Ethology Ecology & Evolution, 23: 1-25.). For lizards, this behaviour is described for the families Crotaphytidae (Gluesing 1983Gluesing, E.A. 1983. Collared lizard predation: the effects of conspicuous morphology and movement. Copeia, 1983: 835-837.), Dibamidae (Torres-Cervantes et al. 2004Torres-Cervantes, R.J.; Hernández-Ibarra, X.; Ramírez-Butista, A. 2004. Anelytropsis papillosus (Mexican Blind Lizard). Death feigning and autotomy. Herpetological Review, 35: 384.), Gymnophthalmidae (Muscat et al. 2016Muscat, E.; Entiauspe-Neto, O.M.; Loebmann, D. 2016. Defensive behavior and predation on Placosoma glabellum (Peters, 1870) (Squamata: Gymnophthalmidae). Herpetologia Brasileira, 2: 51-52 ), Liolaemidae (Rocha 1993Rocha, C.F.D. 1993. The set of defense mechanisms in a tropical sand lizard (Liolaemus lutzae) of southeastern Brazil. Ciência e Cultura, 45: 116-122.; Santos et al. 2010), Scincidae (Langkilde et al. 2003Langkilde, T.; Schwarzkopf, L.; Alford, R. 2003. An ethogram for adult male rainbow skinks, Carlia jarnoldae. Herpetological Journal, 13: 141-148.; Patel et al. 2016Patel, H.; Naik, V.; Tank, S.K. 2016. Death-feigning behavior in two species of Lygosoma (Squamata: Scincidae) from India. Phyllomedusa, 15: 191-194.) and Tropiduridae (Galdino and Pereira 2002Galdino, C.A.B.; Pereira, E.G. 2002. Tropidurus nanuzae (NCN). Death feigning. Herpetological Review, 33: 54. ; Gomes et al. 2004Gomes, F.R.; Kohlsdorf, T.; Navas, C.A. 2004. Thanatosis in Eurolophosaurus divaricatus: temperature and habituation effects. Amphibia-Reptilia, 25: 321-325.; Kosldorf et al. 2004Kosldorf, T.; Rodrigues, M.T.; Navas, C.A. 2004. Eurolophosaurus divaricatus (NCN). Death feigning. Herpetological Review, 35: 390.; Bertoluci et al. 2006Bertoluci, J.; Cassimiro, J.; Rodrigues, M.T. 2006. TROPIDURIDAE (Tropidurid lizards). Death feigning. Herpetological Review, 37: 472-473.).

The family Gymnophthalmidae is widely distributed from southern Mexico to Argentina, comprising more than 40 genera and 235 species, with 32 genera and 92 species being found in Brazil (Costa and Bérnils 2015Costa, H.C.; Bérnils, R.S. 2015. Répteis brasileiros: Lista de espécies 2015. Herpetologia Brasileira, 4: 75-93.; Uetz et al. 2017Uetz, P; Freed, P.; Hošek, J. 2017. The Reptile Database. ( (http://www.reptile-database.org ). Accessed on 27/10/2016.
http://www.reptile-database.org...
). Iphisa elegans is a small Amazonian gymnophtalmid with mainly diurnal habits, found in leaf litter of Brazil, Bolivia, Colombia, Ecuador, Peru and the Guiana Shield (Guyana and Surinam) (Avila-Pires 1995Avila-Pires, T.C.S. 1995. Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen, 299: 1-706.; Andrade et al. 2013Andrade, S.P.; Santos, D.L.; Kawashita-Ribeiro, R.A.; Vaz-Silva, W. 2013. New records and updated distribution map of Iphisa elegans Gray, 1851 (Reptilia, Gymnophthalmidae). Herpetology Notes, 6: 395-400.).

According to recent studies, the name Iphisa elegans includes a complex of cryptic species (Nunes et al. 2012Nunes, P.M.S.; Fouquet, A.; Curcio, F.F.; Kok, P.; Rodrigues, M.T. 2012. Cryptic species in Iphisa elegans Gray, 1851 (Squamata: Gymnophthalmidae) revealed by hemipenial morphology and molecular data. Zoological Journal of the Linnean Society, 166: 361-376.). Adults of this species exhibit an antique-brown to dark yellowish dorsal surface, venter creamy grey in females and orange in males (Beebe 1945Beebe, W. 1945. Field notes on the lizards of Kartabo, British Guiana and Caripito, Venezuela. Part 3. Teiidae, Amphisbaenidae and Scincidae. Zoologica, 30: 7-31.; Avila-Pires 1995Avila-Pires, T.C.S. 1995. Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen, 299: 1-706.), which is characterized as sexual dichromatism (Rodrigues et al. 2007Rodrigues, M.T.; Pellegrino, K.C.M.; Dixo, M.; Verdade, V.K.; Pavan, D.; Argolo, A.J.S.; Sites, J.W. 2007. A new genus of microteiid lizard from the Atlantic Forests of state of Bahia, Brazil, with a new generic name for Colobosaura mentalis, and a discussion of relationships among the Heterodactylini (Squamata, Gymnophthalmidae). American Museum Novitates, 3565: 1-27.). These lizards have cryptic behavior, running into the leaf litter in response to any disturbance in their surroundings (Hoogmoed 1973Hoogmoed, M. S. 1973. Notes on the Herpetofauna of Surinam IV. The lizards and amphisbaenians of Surinam. Biogeographica 4: 14-19.; Vitt et al. 2008Vitt, L.; Magnusson, W.E.; Ávila-Pires, T.C.; Lima, A.P. 2008. Guide to the Lizards of Reserva Adolpho Ducke, Central Amazonia. Attema, Manaus, 180p.). Due to the difficulty of observing specimens of I. elegans in nature, their natural history and defensive repertoire are largely unknown. In order to enrich this knowledge for the family, we report the first case of death-feigning behaviour for this species and the second report for the whole family Gymnophthalmidae.

On September 16th, 2015, three individuals of Iphisa elegans were captured in pitfall traps during a fauna monitoring program at Comodoro Municipality, Mato Grosso State, Brazil (13º42’00.63”S 60º25’01.69”W). When manipulated, an adult male (snout-vent length, SVL = 48mm, Figure 1) turned venter up, putting itself in a death-feigning posture for 50 seconds. The same behaviour was repeated three times by the same individual, which held the position for about two minutes each time. In all situations, the lizard kept its eyes closed, and only returned to the normal position when it was put back onto the ground. The specimen was deposited in the Zoological Collection of the Universidade Federal de Goiás, municipality of Goiânia, Goiás State, Brazil (ZUFG 1221).

Figure 1
Individual of Iphisa elegans (ZUFG 1221, adult male): (A) In normal posture; (B) With exhibition of the orange venter. This figure is in color only in the electronic version.

The first record for this behaviour in the family was for Placosoma glabellum, and the behaviour was similar to the case reported here. The lizard turned its venter up and remained still, with closed eyelids, maintaining this posture for approximately 60 seconds (Muscat et al. 2016Muscat, E.; Entiauspe-Neto, O.M.; Loebmann, D. 2016. Defensive behavior and predation on Placosoma glabellum (Peters, 1870) (Squamata: Gymnophthalmidae). Herpetologia Brasileira, 2: 51-52 ).

Until now, all records of death-feigning behavior previously observed in lizards (with exception of an individual of Liolaemus lutzae and other of Lygosoma punctata), occurred after the specimens has been stimulated, including our record (Gluesing 1983Gluesing, E.A. 1983. Collared lizard predation: the effects of conspicuous morphology and movement. Copeia, 1983: 835-837.; Rocha 1993Rocha, C.F.D. 1993. The set of defense mechanisms in a tropical sand lizard (Liolaemus lutzae) of southeastern Brazil. Ciência e Cultura, 45: 116-122.; Galdino and Pereira 2002Galdino, C.A.B.; Pereira, E.G. 2002. Tropidurus nanuzae (NCN). Death feigning. Herpetological Review, 33: 54. ; Langkilde et al. 2003Langkilde, T.; Schwarzkopf, L.; Alford, R. 2003. An ethogram for adult male rainbow skinks, Carlia jarnoldae. Herpetological Journal, 13: 141-148.; Gomes et al. 2004Gomes, F.R.; Kohlsdorf, T.; Navas, C.A. 2004. Thanatosis in Eurolophosaurus divaricatus: temperature and habituation effects. Amphibia-Reptilia, 25: 321-325.; Kosldorf et al. 2004Kosldorf, T.; Rodrigues, M.T.; Navas, C.A. 2004. Eurolophosaurus divaricatus (NCN). Death feigning. Herpetological Review, 35: 390.; Torres-Cervantes et al. 2004Torres-Cervantes, R.J.; Hernández-Ibarra, X.; Ramírez-Butista, A. 2004. Anelytropsis papillosus (Mexican Blind Lizard). Death feigning and autotomy. Herpetological Review, 35: 384.; Bertoluci et al. 2006Bertoluci, J.; Cassimiro, J.; Rodrigues, M.T. 2006. TROPIDURIDAE (Tropidurid lizards). Death feigning. Herpetological Review, 37: 472-473.; Santos et al. 2010Santos, M.B.; Oliveira, M.C.L.M.; Verrastro, L.; Tozetti, A.M. 2010. Playing dead to stay alive: thanatosis in Liolaemus occipitalis (Squamata: Liolaemidae). Biota Neotropica, 10: 361-364. ; Muscat et al. 2016Muscat, E.; Entiauspe-Neto, O.M.; Loebmann, D. 2016. Defensive behavior and predation on Placosoma glabellum (Peters, 1870) (Squamata: Gymnophthalmidae). Herpetologia Brasileira, 2: 51-52 ; Patel et al. 2016Patel, H.; Naik, V.; Tank, S.K. 2016. Death-feigning behavior in two species of Lygosoma (Squamata: Scincidae) from India. Phyllomedusa, 15: 191-194.).

Iphisa elegans is preyed upon by birds, lizards and snakes (Cunha 1961Cunha, O.R. 1961. Lacertílios da Amazônia. II. Os lagartos da Amazônia brasileira, com especial referenda aos representados na coleção do Museu Goeldi. Boletim do Museu Paraense Emilio Goeldi, nova série Zoologia, 39:1-189.1.; Hoogmoed 1973Hoogmoed, M. S. 1973. Notes on the Herpetofauna of Surinam IV. The lizards and amphisbaenians of Surinam. Biogeographica 4: 14-19.; Duellman 1978Duellman, W.E. 1978. The biology of an Equatorial Herpetofauna in Amazonian Ecuador. Misc. Publ. Mus. Nat. Hist. Univ. Kansas, 65: 1-352.; Prudente et al. 1998Prudente, A.L.C.; Moura-Leite, J.C. de; Morato, S.A.A. 1998. Alimentação das espécies de Siphlophis Fitzinger (Serpentes, Colubridae, Xenodontinae, Pseudoboini). Revista Brasileira de Zoologia, 15: 375-383.). It is possible that I. elegans uses the death-feigning posture when the cryptic behaviour or scape attempt fails. Besides, it is suggested that this behaviour could be used to confuse visually oriented predators, such as birds. However, more studies are necessary to observe the efficiency of this behaviour, as well as its frequency of occurrence, using individuals of both sexes. In some species of lizards, the orange belly may be related to hormonal cycles in breeding males (Cox et al. 2005Cox, R.M.; Skelly, S.L.; Leo, A.; John-Alder, H.B. 2005. Testosterone regulates sexually dimorphic coloration in the eastern fence lizard, Sceloporus undulatus. Copeia. 2005: 597-608.). We also suggest to evaluate if the orange venter in males could have any antipredation advantage.

ACKNOWLEDGEMENTS

We are grateful to Bruno G. Augusta, Paulo A. M. Goldoni, Rodrigo Castellari Gonzalez and the anonymous referees for suggestions and their critical reviews of the manuscript. We are also grateful to Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis - IBAMA for license # 617/2015 (process # 02001.000328/2009-98 and Ambientare for financial and logistical support.

  • Andrade, S.P.; Santos, D.L.; Kawashita-Ribeiro, R.A.; Vaz-Silva, W. 2013. New records and updated distribution map of Iphisa elegans Gray, 1851 (Reptilia, Gymnophthalmidae). Herpetology Notes, 6: 395-400.
  • Avila-Pires, T.C.S. 1995. Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandelingen, 299: 1-706.
  • Beebe, W. 1945. Field notes on the lizards of Kartabo, British Guiana and Caripito, Venezuela. Part 3. Teiidae, Amphisbaenidae and Scincidae. Zoologica, 30: 7-31.
  • Bertoluci, J.; Cassimiro, J.; Rodrigues, M.T. 2006. TROPIDURIDAE (Tropidurid lizards). Death feigning. Herpetological Review, 37: 472-473.
  • Costa, H.C.; Bérnils, R.S. 2015. Répteis brasileiros: Lista de espécies 2015. Herpetologia Brasileira, 4: 75-93.
  • Cox, R.M.; Skelly, S.L.; Leo, A.; John-Alder, H.B. 2005. Testosterone regulates sexually dimorphic coloration in the eastern fence lizard, Sceloporus undulatus Copeia 2005: 597-608.
  • Cunha, O.R. 1961. Lacertílios da Amazônia. II. Os lagartos da Amazônia brasileira, com especial referenda aos representados na coleção do Museu Goeldi. Boletim do Museu Paraense Emilio Goeldi, nova série Zoologia, 39:1-189.1.
  • Duellman, W.E. 1978. The biology of an Equatorial Herpetofauna in Amazonian Ecuador. Misc. Publ. Mus. Nat. Hist. Univ. Kansas, 65: 1-352.
  • Galdino, C.A.B.; Pereira, E.G. 2002. Tropidurus nanuzae (NCN). Death feigning. Herpetological Review, 33: 54.
  • Gluesing, E.A. 1983. Collared lizard predation: the effects of conspicuous morphology and movement. Copeia, 1983: 835-837.
  • Gomes, F.R.; Kohlsdorf, T.; Navas, C.A. 2004. Thanatosis in Eurolophosaurus divaricatus: temperature and habituation effects. Amphibia-Reptilia, 25: 321-325.
  • Hoogmoed, M. S. 1973. Notes on the Herpetofauna of Surinam IV. The lizards and amphisbaenians of Surinam. Biogeographica 4: 14-19.
  • Kosldorf, T.; Rodrigues, M.T.; Navas, C.A. 2004. Eurolophosaurus divaricatus (NCN). Death feigning. Herpetological Review, 35: 390.
  • Langkilde, T.; Schwarzkopf, L.; Alford, R. 2003. An ethogram for adult male rainbow skinks, Carlia jarnoldae Herpetological Journal, 13: 141-148.
  • Muscat, E.; Entiauspe-Neto, O.M.; Loebmann, D. 2016. Defensive behavior and predation on Placosoma glabellum (Peters, 1870) (Squamata: Gymnophthalmidae). Herpetologia Brasileira, 2: 51-52
  • Nunes, P.M.S.; Fouquet, A.; Curcio, F.F.; Kok, P.; Rodrigues, M.T. 2012. Cryptic species in Iphisa elegans Gray, 1851 (Squamata: Gymnophthalmidae) revealed by hemipenial morphology and molecular data. Zoological Journal of the Linnean Society, 166: 361-376.
  • Patel, H.; Naik, V.; Tank, S.K. 2016. Death-feigning behavior in two species of Lygosoma (Squamata: Scincidae) from India. Phyllomedusa, 15: 191-194.
  • Prudente, A.L.C.; Moura-Leite, J.C. de; Morato, S.A.A. 1998. Alimentação das espécies de Siphlophis Fitzinger (Serpentes, Colubridae, Xenodontinae, Pseudoboini). Revista Brasileira de Zoologia, 15: 375-383.
  • Rocha, C.F.D. 1993. The set of defense mechanisms in a tropical sand lizard (Liolaemus lutzae) of southeastern Brazil. Ciência e Cultura, 45: 116-122.
  • Rodrigues, M.T.; Pellegrino, K.C.M.; Dixo, M.; Verdade, V.K.; Pavan, D.; Argolo, A.J.S.; Sites, J.W. 2007. A new genus of microteiid lizard from the Atlantic Forests of state of Bahia, Brazil, with a new generic name for Colobosaura mentalis, and a discussion of relationships among the Heterodactylini (Squamata, Gymnophthalmidae). American Museum Novitates, 3565: 1-27.
  • Santos, M.B.; Oliveira, M.C.L.M.; Verrastro, L.; Tozetti, A.M. 2010. Playing dead to stay alive: thanatosis in Liolaemus occipitalis (Squamata: Liolaemidae). Biota Neotropica, 10: 361-364.
  • Toledo, L.F.; Sazima, I.; Haddad, C.F.B. 2011. Behavioural defenses of anurans: an overview. Ethology Ecology & Evolution, 23: 1-25.
  • Torres-Cervantes, R.J.; Hernández-Ibarra, X.; Ramírez-Butista, A. 2004. Anelytropsis papillosus (Mexican Blind Lizard). Death feigning and autotomy. Herpetological Review, 35: 384.
  • Vitt, L.; Magnusson, W.E.; Ávila-Pires, T.C.; Lima, A.P. 2008. Guide to the Lizards of Reserva Adolpho Ducke, Central Amazonia Attema, Manaus, 180p.
  • Uetz, P; Freed, P.; Hošek, J. 2017. The Reptile Database. ( (http://www.reptile-database.org ). Accessed on 27/10/2016.
    » http://www.reptile-database.org

  • ASSOCIATE EDITOR:

    Claudia Keller
  • CITE AS:

    Machado-Filho, P.R.; Moya, G.M.; Maffei, F. 2018. Death-feigning behaviour in Iphisa elegans: the second reported case in the Family Gymnophthalmidae (Reptilia: Squamata). Acta Amazonica 48: 151-153.

Publication Dates

  • Publication in this collection
    Apr-Jun 2018

History

  • Received
    14 Nov 2017
  • Accepted
    31 Dec 2017
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