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Journal of Natural History Is It All Death Feigning? Case in Anurans

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Journal of Natural History Is It All Death Feigning? Case in Anurans This article was downloaded by: [Toledo, Luís Felipe] On: 9 July 2010 Access details: Access Details: [subscription number 924058002] Publisher Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37- 41 Mortimer Street, London W1T 3JH, UK Journal of Natural History Publication details, including instructions for authors and subscription information: http://www.informaworld.com/smpp/title~content=t713192031 Is it all death feigning? Case in anurans Luís Felipe Toledoa; Ivan Sazimaa; Célio F. B. Haddadb a Museu de Zoologia “Prof. Adão José Cardoso”, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, São Paulo, Brazil b Departamento de Zoologia, Instituto de Biociências, Unesp, Rio Claro, São Paulo, Brazil Online publication date: 08 July 2010 To cite this Article Toledo, Luís Felipe , Sazima, Ivan and Haddad, Célio F. B.(2010) 'Is it all death feigning? Case in anurans', Journal of Natural History, 44: 31, 1979 — 1988 To link to this Article: DOI: 10.1080/00222931003624804 URL: http://dx.doi.org/10.1080/00222931003624804 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf This article may be used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Journal of Natural History Vol. 44, Nos. 31–32, August 2010, 1979–1988 IsTNAH0022-29331464-5262Journal of Naturalit HistoryHistory, all Vol. 1, No. 1, Februarydeath 2010: pp. 0–0 feigning? Case in anurans LuísJournalL.F. Toledo of Natural et al. History Felipe Toledoa*, Ivan Sazimaa and Célio F.B. Haddadb aMuseu de Zoologia “Prof. Adão José Cardoso”, Instituto de Biologia, Universidade Estadual de Campinas, CEP 13083-970, Caixa Postal 6109, Campinas, São Paulo, Brazil; bDepartamento de Zoologia, Instituto de Biociências, Unesp, CEP 13506-970, Caixa Postal 199, Rio Claro, São Paulo, Brazil (Received 23 July 2009; final version received 13 January 2010) Anurans are known to feign death as a way to avoid or minimize the risk of predation. However, information on this defensive strategy is scattered and we believe that there is more than one behaviour type referred to as thanatosis. Here we review the literature, add original data, and propose definitions and new names that com- plement the present knowledge on the subject. We collected information on 334 individuals of 99 species in 16 families and grouped the recorded displays into two categories of tonic immobility: (1) thanatosis, death-feigning, or playing possum, and (2) shrinking or contracting. These two categories are treated as different behaviour types because of the display pattern (position of fore- and hindlimbs, eye opening), presence of skin toxins (shrinking is mostly displayed by toxic spe- cies, whereas thanatosis is mostly displayed by non-toxic species), social context (interaction with predators), and their putative or actual functions. Keywords: Anurans; defensive behaviour; thanatosis; death feigning; shrinking; tonic immobility Introduction The dynamics between predators and their prey is one of the main issues in community ecology. For example, predators may influence the distribution and abundance of other species, either their prey or other predators, consequently influencing resource competition (Begon et al. 1996). Additionally, different selec- Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 tive pressures may be involved in the predator–prey relationship, such as those related to morphological and physiological costs of predation (Gans 1986), and those that promote the origin and evolution of several defensive strategies (Edmunds 1974; Toledo and Haddad 2009). Among this wide range of defensive strategies, animals may display so-called death-feigning, playing possum, or thanatosis, a behaviour recorded for a great range of animal types, from insects and other arthropods to vertebrates including frogs, reptiles, birds and mammals (see Edmunds 1974 for a summary and Miyatake et al. 2004, 2009; Cassill et al. 2008 for recent findings). While displaying thanatosis an animal adopts a posture that gives it the appearance of being dead with which it may inhibit or divert the attack of a potential predator. The term thanatosis was coined in allusion to Thanatos, the Greek god of death, and as far as we know, this name was first applied to anurans in the early 1970s *Corresponding author. Email: [email protected] ISSN 0022-2933 print/ISSN 1464-5262 online © 2010 Taylor & Francis DOI: 10.1080/00222931003624804 http://www.informaworld.com 1980 L.F. Toledo et al. (Boice and Williams 1971; Sazima 1972). There are several examples among anurans, with most of them based on scattered data or published as short notes (e.g. Sazima 1974; Toledo 2004a,b; Toledo et al. 2005). Thanatosis may appear simple at first glance, but it seems to be employed under a wide range of situations and may include or interact synergistically with other behaviours. Additionally, we think that so called thanatosis or tonic immobility consists of two distinct behaviour types and so should be considered a generic term. Here we review the literature on this behaviour, add original data based on observations in nature and experiments in the field and laboratory, and propose a few definitions and new names that complement the current terminology. Material and methods Major herpetological journals such as Amphibia-Reptilia, Copeia, Herpetologica, Herpetological Bulletin, Herpetological Journal, Herpetological Review and Journal of Herpetology were searched for reports on anuran defensive behaviours (both under natural and experimental conditions). Original data were obtained during several field trips from 1969 to 2007 in Brazil, mainly in the biomes of the Cerrado and Atlantic Rainforest. Staged encounters in the field were made by approaching an individual frog (which was awake and not in amplexus) and recording its reaction to close approach, handling, grasping suddenly, tapping it gently with sticks (on the head and dorsum), lightly pinching the head, forelimbs and hindlimbs with blunt forceps, or by presenting the frog to a non-venomous snake (generally the colubrid Liophis miliaris). None of these procedures injured the frogs, and such techniques are regarded as effective to simulate a predator’s attack and so to elicit defensive responses (e.g. Brodie 1977; Brodie et al. 1998; Williams et al. 2000; Toledo et al. 2005). Experiments with captive anurans were generally avoided (although a few data were obtained from frogs that had been captive for less than 1 week), because the more a frog remains captive, the more it may change its physiological traits (Navas and Gomes 2001), which may in turn lead to both quantitative and qualitative changes in defensive and other behaviours (Boice and Williams 1971; our personal observations). Scientific names of amphibians follow Frost (2008) and Hedges et al. (2008). Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 Results The review of literature and observations in nature yielded information on 334 indi- viduals of 99 species in 16 families, including juveniles and adults of both sexes (Table 1). The behaviours we retrieved and recorded are clumped under two major categories: one that we name herein as “thanatosis, death-feigning, or playing possum” and another that we name herein as “shrinking” or “contracting”; both categories are described below. The term “tonic immobility” can refer to both behaviours. Death feigning, playing possum, thanatosis This behaviour was recorded for five out of 25 toxic species (20%) and for 35 out of 48 non-toxic species (73%) (Table 1). While displaying this behaviour, a frog remains motionless even when touched, generally keeps its eyes open, although in some cases the eyes may be closed (Figure 1). The fore- and hindlimbs are kept loose and can be Journal of Natural History 1981 Table 1. Anurans that display death-feigning (thanatosis) and/or shrinking. Family/Species Thanatosis Shrinking References Aromobatidae Allobates femoralis – – Vaz-Silva and Frota 2004 Arthroleptidae Leptopelis rufus X present study Brachycephalidae Ischnocnema guentheri 4 present study Ischnocnema juipoca 2 present study Ischnocnema parva 1 present study Bufonidae Dendrophryniscus berthalutzae 1 1 present study Dendrophryniscus brevipollicatus 2 present study Dendrophryniscus minutus – – Russel 2002 Incilius occidentalis – – Abbadié-Bisogno et al. 2001 Melanophryniscus moreirae* 2 present study Rhinella abei* 1 present study Rhinella icterica* 8 present study Rhinella jimi* 5 present study Rhinella marina* X Vaz-Silva and Frota 2004 Rhinella ocellata* X Kokubum, 2005 Rhinella ornata* 3 present study Rhinella rubescens* 2 present study Rhinella schneideri* 3 Zamprogno et al. 1998; present study Centrolenidae Hyalinobatrachium uranoscopum 2 present study Craugastoridae
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