Journal of Natural History Is it all death feigning? Case in anurans

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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
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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.
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