Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
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, 3741 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 Is it all death feigning? Case in anurans 0022-2933 TNAH Journal 1464-5262 of Natural History History, Vol. 1, No. 1, February 2010: pp. 0–0 Luís Felipe Toledoa*, Ivan Sazimaa and Célio F.B. Haddadb Journal L.F. Toledo of Natural et al. History a Museu 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 Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 (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 complement 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 species, 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 selective 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. Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 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). Results The review of literature and observations in nature yielded information on 334 individuals 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. Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 Family/Species Aromobatidae Allobates femoralis Arthroleptidae Leptopelis rufus Brachycephalidae Ischnocnema guentheri Ischnocnema juipoca Ischnocnema parva Bufonidae Dendrophryniscus berthalutzae Dendrophryniscus brevipollicatus Dendrophryniscus minutus Incilius occidentalis Melanophryniscus moreirae* Rhinella abei* Rhinella icterica* Rhinella jimi* Rhinella marina* Rhinella ocellata* Rhinella ornata* Rhinella rubescens* Rhinella schneideri* Centrolenidae Hyalinobatrachium uranoscopum Craugastoridae Haddadus binotatus Cycloramphidae Odontophrynus americanus* Odontophrynus carvalhoi* Proceratophrys boiei Proceratophrys melanopogon Rhinoderma darwini Dicroglossidae Hoplobatrachus tigerinus Hylidae Aplastodiscus arildae Aplastodiscus cochranae Aplastodiscus perviridis Bokermannohyla circumdata Bokermannohyla hylax Dendropsophus elegans Dendropsophus elianeae Dendropsophus giesleri Dendropsophus microps Thanatosis – Shrinking – References Vaz-Silva and Frota 2004 X present study 4 2 1 present study present study present study 1 2 – – 1 – – 2 1 8 5 X X 3 2 3 present study present study Russel 2002 Abbadié-Bisogno et al. 2001 present study present study present study present study Vaz-Silva and Frota 2004 Kokubum, 2005 present study present study Zamprogno et al. 1998; present study 2 present study 1 present study 1 – A. D’Heursel personal communication present study present study present study Pough et al. 2001 – – Brodie and Nussbaum 1987 1 X 2 2 12 2 2 1 – 3 1 1 7 1 1 2 Carneiro and Rocha 2005 present study present study present study present study present study present study present study present study (Continued) 1982 L.F. Toledo et al. Table 1. (Continued). Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 Family/Species Dendropsophus minutus Dendropsophus werneri Hypsiboas albopunctatus Hypsiboas albomarginatus Hypsiboas beckeri Hypsiboas bischoffi Hypsiboas caingua Hypsiboas faber Hypsiboas geographicus Hypsiboas guentheri Hypsiboas latistriatus Hypsiboas leptolineatus Hypsiboas marginatus Hypsiboas polytaenius Hypsiboas pulchellus Hypsiboas semilineatus Thanatosis 6 1 1 1 8 Shrinking 6 10 11 1 2 65 2 1 1 2 3 1 2 Phrynomedusa marginata* Phyllomedusa azurea* Phyllomedusa bahiana* Phyllomedusa burmeisteri* Phyllomedusa centralis* Phyllomedusa distincta* Phyllomedusa nordestina* Phyllomedusa rohdei* 2 3 5 6 11 8 9 5 Phyllomedusa sauvagii* Phyllomedusa tetraploidea* Pseudacris regilla 1 6 1 Scinax alterus Scinax catharinae Scinax fuscomarginatus Scinax fuscovarius Scinax hayii Scinax hiemalis Scinax perpusillus Trachycephalus mesophaeus* Xenohyla truncata Hyperoliidae Acanthixalus spinosus Kassina fusca Leiuperidae Eupemphix nattereri* Physalaemus cuvieri 1 1 15 2 2 2 4 2 – 3 – References present study present study Sazima 1972; present study present study present study present study present study present study Angulo et al. 2007 present study present study present study present study present study present study Azevedo-Ramos 1995; present study present study present study present study present study Bokermann 1965; present study present study present study Sazima 1972, 1974; present study present study present study Brattstorm and Warren 1955; Foster 2007 present study present study Toledo, 2004b Sazima 1972; Rodrigues and Rodrigues 2007 present study present study present study present study Napoli 2001 X X present study Rödel and Braun 1999 3 5 present study present study (Continued) Journal of Natural History 1983 Table 1. (Continued). Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 Family/Species Physalaemus nanus Pseudopaludicola mystacalis Pseudopaludicola saltica Leptodactylidae Leptodactylus cunicularius Leptodactylus labyrinthicus* Leptodactylus fuscus Leptodactylus marambaiae Leptodactylus mystacinus Leptodactylus latrans Leptodactylus plaumanni Limnodynastidae Neobatrachus pictus Neobatrachys sudeli Microhylidae Elachistocleis sp.* Myobatrachidae Crinia riparia Crinia signifera Crinia georgiana Crinia glauerti Geocrinia laevis Mixophyes fasciolatus Mixophyes schevilli Pseudophryne bibronii Pseudophryne semimarmorata Ranidae Clinotarsus curtipes Lithobates pipiens Thanatosis Shrinking References 4 1 2 present study present study present study 1 X 1 – 3 6 1 – present study Toledo et al. 2005 present study Siqueira et al. 2006 present study present study present study – – – – Williams et al. 2000 Williams et al. 2000 3 Toledo 2004a, present study – – X – X – X X X – – – – – – – – Williams et al. 2000 Williams et al. 2000 Williams et al. 2000 Williams et al. 2000 Williams et al. 2000 Williams et al. 2000 Williams et al. 2000 Williams et al. 2000 Williams et al. 2000 Gramapurohit et al. 2001 Boice and Williams 1971 When the number of recorded individuals is available these are presented; otherwise an “X” indicates that one of these two behaviour types is recorded for a given species. A dash indicates that there is insufficient information about the type of behaviour recorded to categorize it as either of the two types. See text for the explanation of the two types of behaviours. Families, genera and species are presented in alphabetical order. An asterisk indicates species that are considered to have significant toxic skin secretions. moved by the observer to any position without any resistance from the frog (Figure 2A). This behaviour is displayed after a short series of jumps by the frog in response to the approach of a potential predator (present study), or after being handled by a potential predator (e.g. Toledo 2004a,b). Death-feigning is the behaviour most commonly recorded and occurs in several species, genera and families (Table 1). Shrinking, contracting This behaviour was observed for 20 out of 25 toxic species (80%) and for 20 out of 48 non-toxic species (41.6%) (Table 1). While displaying this behaviour, a frog remains Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 1984 L.F. Toledo et al. Figure 1. Percentage of species with open eyes (grey bars) and closed eyes (black bars) during display of death-feigning (41 species; 111 individuals) and shrinking (38 species; 209 individuals). Figure 2. (A) Scinax fuscomarginatus displaying death-feigning behaviour; (B) Phyllomedusa bahiana displaying shrinking behaviour; (C) Acanthixalus spinosus displaying deathfeigning behaviour plus tongue protrusion; (D) Leptopelis rufus displaying death-feigning behaviour, with its mouth slightly open for the release of ammonia-like smell. Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 Journal of Natural History 1985 motionless, generally with its eyes closed, but in a few cases the eyes may remain open (Figure 1). The fore- and hindlimbs are bent and kept close to the body. If the observer tries to stretch them, the limbs are forced back by the frog to the initial position, generally against its belly (Figure 2B). Some individuals also arch the body, and the head may be ventrally flexed. This behaviour may be displayed during the approach of a potential predator, or immediately after the potential predator touches the frog or even after the subjugation phase (Sazima 1974; present study). Shrinking has been recorded for several species of bufonids, cycloramphids and hylids. It is characteristic of some hylid groups, such as the phyllomedusines (e.g. Phrynomedusa, Phyllomedusa), species of the hyline genera Hypsiboas and Aplastodiscus, and bufonids of the genus Rhinella (Table 1). There are also species that may display either of the two behaviours (Table 1). Furthermore, there are a few species that may display an intermediate pattern: forelimbs are kept loose (as in thanatosis) and the hindlimbs are kept close to the body (as in shrinking). This intermediate pattern maybe recorded for the bufonids Melanophryniscus moreirae and Rhinella icterica (Table 1). Both behaviours are passive defences that may be accompanied by odoriferous secretions (e.g. Sazima 1974; our personal observations) and aposematic (warning) colours on the ventral region (our personal observation) or on the tongue (Figure 2C). An extreme situation is exemplified by Leptopelis rufus (Arthroleptidae) while displaying thanatosis. This frog may remain with an open mouth (Figure 2D), from which it releases a strong ammonia-like smell. The smell added to the posture increases the illusion of a dead frog (see Schmitz et al. 1999). Discussion Although thanatosis and shrinking are different display forms (e.g. limb position and eye opening differ), both behaviour types are believed to be effective in distinct situations: (1) staying motionless would not stimulate predators that need movement cues to attack; (2) staying motionless would relax or divert the predator’s attention and thus allow the frog to flee; (3) while handled, remaining motionless may cause less harm to the frog than while struggling within the predator’s grip and may provide the prey with an opportunity to flee (see Edmunds 1974; Miyatake et al. 2009). Additionally, shrinking may have still another protective function. As shrinking is mostly displayed by toxic species (whereas thanatosis is mostly displayed by nontoxic species) this behaviour can be linked to species that have the ability to escape from the predator after subjugation or even during the digestive process. Therefore, to remain shrunken and motionless would protect the frog from more serious wounds while being swallowed (Sazima 1974). Later, once in the digestive tract of the predator, the frog may produce noxious secretions (such as those in parotoid glands of bufonids and in the dorsal skin of phyllomedusines and Trachycephalus spp.), which would cause it to be disgorged and to leave the predator’s gut with its skin slightly eroded but alive. This situation is recorded for some frog species (e.g. Dendrobates auratus: Brodie and Tumbarello 1978; Phyllomedusa rohdei: Sazima 1974; and Trachycephalus mesophaeus: L.F.T. unpublished data) swallowed by snakes, mostly of the genus Liophis. It is difficult to attribute a lesser or greater degree of defensive protection to either of the two behaviour types. Thanatosis seems to be a more realistic “dead-like” Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 1986 L.F. Toledo et al. posture because the frog may be put, and remains in any posture. On the other hand, shrinking probably protects vital areas, such as the belly (legs and arms close to it), eyes (kept closed), limbs (close to the body). Hence, shrinking seems to be a behaviour type with a more complex function, not only causing the displaying frog to appear dead (see also Honma et al. 2006). It is possible that shrinking has evolved from thanatosis because of the higher complexity of the former: eyes generally closed, limbs in fixed positions, and head ventrally flexed. Besides the differences in the complexity level between the two behaviour types, thanatosis is widespread in the anuran clade, whereas shrinking seems to be a synapomorphy of given phylogenic groupings, such as some groups or genera of Hylidae and Bufonidae (Table 1). This may indicate a later (and multiple) evolution of shrinking in relation to thanatosis. For anuran current and broad-spectrum phylogenetic trees see Frost et al. (2006) and Grant et al. (2006). Hence, we think that death-feigning and shrinking are distinct defensive behaviour types and we propose that these be treated as such in future studies. Questions remain about their potential or actual defensive value and plausible origins, but this is beyond the scope of the present paper, in which we provide a dataset that may be useful as a starting point for further studies. Acknowledgements André Antunes, Cynthia Prado, Daniel Loebmann, Juliana Zina, Luís Giasson, Marlies Sazima, Nanuza L. Menezes, Olívia Araújo, Otávio Cardoso de Oliveira, Rodrigo Lingnau, Werner C. A. Bokermann helped in the field expeditions. Anne D’Heursel, Itamar Martins, Rogério Bastos, Ricardo Sawaya, Andreas Schmitz, Cynthia Prado, Julián Faivovich, Louise Allcock, and Wolfgang Böhme helped with references and with valuable comments during early drafts of the manuscript. Andreas Schmitz provided the pictures of Leptopelis rufus and Acanthixalus spinosus. FAPESP and CNPq supported the Herpetology laboratory, Departamento de Zoologia, Unesp, Rio Claro, São Paulo, Brazil. The authors also thank, CNPq, FAPESP (process no. 2008/50325-5), Idea Wild, Neotropical Grassland Conservancy, and Fauna Pro Assessoria e Consultoria Ambiental for grants, scholarships, equipment donation, and supporting some of the field expeditions. IS (retired) is presently associated as a voluntary researcher with the Museu de Zoologia, Universidade Estadual de Campinas. References Abbadié-Bisogno K, Oliver-López L, Ramírez-Bautista A. 2001. Bufo occidentalis (Pine Toad). Death feigning. Herpetol Rev. 32(4):247. Angulo A, Acosta AR, Rueda-Almonacid JV. 2007. Diversity and frequency of visual defensive behaviours in a population of Hypsiboas geographicus. Herpetol J. 17:138–140. Azevedo-Ramos C. 1995. Defensive behaviors of the Neotropical treefrog Hyla geographica (Anura, Hylidae). Rev Bras Biol. 55(1):45–47. Begon M, Townsend CR, Harper JL. 1996. Ecology: from individuals to ecosystems. 4th edition. Cambridge: Blackwell Publishing. Boice R, Williams RC. 1971. Delay in onset of tonic immobility in Rana pipiens. Copeia 1971(4):747–748. Bokermann WCA. 1965. Três novos batráquios da região central de Mato Grosso, Brasil (Amphibia, Salientia). Rev Bras Biol. 25(3):257–264. Brattstorm BH, Warren JW. 1955. Observations on the ecology and behavior of the pacific treefrog, Hyla regilla. Copeia 1955(3):181–191. Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 Journal of Natural History 1987 Brodie Jr. ED. 1977. Salamander antipredator postures. Copeia 1977:523–535. Brodie Jr. ED, Tumbarello MS. 1978. The antipredator functions of Dendrobates auratus (Amphibia, Anura, Dendrobatidae) skin secretion in regard to a snake predator (Thamnophis). J Herpetol. 12(2):264–265. Brodie Jr. ED, Nussbaum RA. 1987. Antipredator responses of Rana tigerina to a crow. Herpetol. Rev. 18(1):8–9. Brodie Jr. ED, Williams CR, Tyler MJ. 1998. Evolution of aposematic behavior and coloration in the Australian frog genus Uperoleia. J. Herpetol. 32(1):136–139. Carneiro PCF, Rocha CFD. 2005. Hyla arildae (Teresópolis Treefrog). Death feigning. Herpetol Rev. 36(3):301. Cassill, DL, Vo K, Becker B. 2008. Young fire ant workers feign death and survive aggressive neighbors. Naturwissenschaften 95:617–624. Edmunds M. 1974. Defence in animals: a survey of anti-predator defences. New York. Longman. Foster CD. 2007. Pseudacris regilla (Pacific Treefrog). Death feigning. Herpetol Rev. 38(2):192. Frost DR. 2008. Amphibian species of the world: an online reference [internet]. Version 5.2. American Museum of Natural History, New York, USA. [cited 2009 November 20]. Available from: http://research.amnh.org/herpetology/amphibia/. Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, de Sá RO, Channing A, Wilkinson M, Donnellan SC, et al. 2006. The amphibian tree of life. Bull Am Mus Nat Hist. 297:1–370. Gans C. 1986. Predator–prey relationships. Chicago (IL): University of Chicago Press. Functional morphology of predator–prey relationships; pp.6–23. Gramapurohit NP, Shanbhag BA, Saidapur SK. 2001. Rana curtipes (Bicolored Frog). Death feigning. Herpetol Rev. 32(2):103. Grant T, Frost DR, Caldwell JP, Gagliardo R, Haddad CFB, Kok PJR, Means DB, Noonan BP, Schargel WE, Wheeler WC. 2006. Phylogenetic systematic of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bull Am Mus Nat Hist. 299:1–262. Hedges SB, Duellman WE, Heinicke MP. 2008. New World direct-developing frogs (Anura: Terrarana): molecular phylogeny, classification, biogeography, and conservation. Zootaxa 1737:1–182. Honma A, Oku S, Nishida T. 2006. Adaptive significance of death feigning posture as a specialized inducible defence against gape-limited predators. Proc R Soc B. 273:1631–1636. Kokubum MNC. 2005. Bufo ocellatus (NCN). Death feigning. Herpetol Rev. 36(2):160. Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M. 2004 Is deathfeigning adaptive? Heritable variation in fitness difference of death-feigning behaviour. Proc R Soc B. 271:2293–2296. Miyatake T, Nakayama S, Nishi Y, Nakajima S. 2009. Tonically immobilised selfish prey can survive by sacrificing others. Proc R Soc B. 276:2763–2767. Napoli MF. 2001. Xenohyla truncata (NCN). Antipredator behavior. Herpetol Rev. 32(1):36–37. Navas CA, Gomes FR. 2001. Time in captivity as a confounding variable in herpetological research: an example from the metabolic physiology of treefrogs (Scinax). Herpetol Rev. 32:228–230. Pough FH, Andrews RM, Cadle JE, Crump ML, Savitzky AH, Wells KD. 2001. Herpetology. 2nd ed. New Jersey: Prentice Hall. Rödel MO, Braun U. 1999. Associations between anurans and ants in a west African savanna (Anura: Microhylidae, Hyperoliidae, and Hymenoptera: Formicidae). Biotropica 31(1):178–183. Rodrigues DJ, Rodrigues VABP. 2007. Scinax fuscovarius (Snouted Treefrog). Death feigning. Herpetol Rev. 38(2):196. Downloaded By: [Toledo, Luís Felipe] At: 22:17 9 July 2010 1988 L.F. Toledo et al. Russel MJ. 2002. Dendrophryniscus minutus (Amazon toadlet). Defensive behavior. Herpetol Rev. 33(4):302. Sazima I. 1972. Nota preliminar sôbre tanatose em três espécies de Hylidae (“pererecas”). Ciênc Cult. 24:383. Sazima I. 1974. Experimental predation on the leaf-frog Phyllomedusa rohdei by the water snake Liophis miliaris. J Herpetol. 8(4):376–377. Schmitz A, Eukirchen O, Böhme W. 1999. Zur Herpetofauna einer montanen Regenwaldregion in SW-Kamerun (Mt Kupe und Bakossi-Bergland) – I. Einleitung, Bufonidae und Hyperoliidae. Herpetofauna Weinst. 21(121):5–17. Siqueira CC, Marra RV, Vrcibradic D, van Sluys M. 2006. Leptodactylus marambaiae (Marambaia White-Lipped Frog). Death feigning. Herpetol Rev. 37(4):444–445. Toledo LF. 2004a. Elachistocleis cf. ovalis (Common Oval Frog). Death feigning. Herpetol Rev. 35(4):371–372. Toledo LF. 2004b. Scinax fuscomarginatus (NCN). Defensive behavior. Herpetol Rev. 35(4):377–378. Toledo LF and Haddad CFB. 2009. Colors and some morphological traits as defensive mechanisms in anurans. Int J Zool. 910892:1–12. Toledo LF, Tozetti A, Zina J. 2005. Leptodactylus labyrinthicus (Pepper Frog): defensive repertoire. Herpetol Bull. 90:29–31. Vaz-Silva W, Frota JG. 2004. Bufo marinus (Marine Toad). Defensive behavior. Herpetol Rev. 35(4):371. Williams CR, Brodie Jr. ED, Tyler MJ, Walker SJ. 2000. Antipredator mechanisms of Australian frogs. J Herpetol. 34(3):431–443. Zamprogno C, Zamprogno MGF, Teixeira RL. 1998. Bufo paracnemis (Sapo-boi). Death feigning. Herpetol Rev. 29(2):96–97.