Predation has been important in the evolution of many defensive strategies in anurans, such as toxic and distasteful skin secretions, cryptic and aposematic coloration, and a variety of defensive postures and behaviours (Wells, 2007; Vitt and Caldwell, 2009). Predation is an event that can be divided into six phases: localization, identification, approach, subjugation, ingestion, and digestion (Toledo, Sazima and Haddad, 2011). Anurans display a wide variety of defensive strategies that can act in one or more of these phases (Edmunds, 1974). Toledo, Sazima and Haddad (2011) made a broad review of the defensive behaviours in anurans, registering a total of 30 different types of behaviours (some with sub-categories). Among this wide range of defensive behaviours, anurans may display so-called “tonic immobility”. Toledo, Sazima and Haddad (2010) suggest that behaviour includes two different types of defensive behaviour: thanatosis or death feigning and contracting or shrinking.

Thanatosis occurs when an animal adopts a posture that gives it the appearance of being dead, which it may inhibit or divert the attack of a potential predator (Honma, Oku and Nishada, 2006; Toledo, Sazima and Haddad, 2010). This behaviour is found in a wide variety of animals such as insects (e.g. Acheampong and Mitchell, 1997), mites (e.g. Ebermann, 1991), fishes (e.g. Howe, 1991), amphibians (e.g. Toledo, Sazima and Haddad, 2010), reptiles (e.g. Santos et al., 2010), birds (e.g. Sargeant and Eberhardt, 1975) and mammals (e.g. Francq, 1969). Thanatosis would probably be effective against predators that do not feed on dead animals and against those which need movement cues to locate preys (Toledo, Sazima and Haddad, 2011). This behaviour

may avoid subjugation (Toledo, Sazima and Haddad, 2010). In anurans, this behaviour is usually displayed by non-toxic species and occurs in at least 16 anuran families (reviews in Toledo, Sazima and Haddad, 2010, 2011).

Contracting occurs when a frog remains motionless, the fore and hind limbs are bent and kept close to the body; some individuals also arch the body, and the head may be ventrally flexed (Toledo, Sazima and Haddad, 2010). If the observer tries to stretch them, the limbs are forced back by the frog to the initial position, generally against its belly. It may avoid injuries during subjugation and ingestion (Toledo, Sazima and Haddad, 2010). Contracting has been recorded for several species of bufonids, cycloramphids and hylids, and is characteristic of the Hylid genus Phyllomedusa (review in Toledo, Sazima and Haddad, 2010).

Although recent studies have contributed substantially to knowledge of the strategies used by anurans to avoid predation (see Wells, 2007; Toledo and Haddad, 2009a, 2009b; Toledo, Sazima and Haddad, 2010, 2011), several species remain without any information about its defensive strategies. The aim of this manuscript is to describe the first reports of the defensive behaviour of two Andean bufonids, Osornophryne percrassa (Ruíz-Carranza and Hernández-Camacho, 1976) and Rhinella sp. (undescribed), and one hylid, Phyllomedusa venusta (Duellman and Trueb, 1967).

Osornophryne percrassa (Fig. 1) is endemic to the Andean mountains of Colombia, found only in Tolima, Caldas and Quindio Departments, on the central Andes, between 2700 and 3700 m (Acosta-Galvis, 2000; Mueses-Cisneros, 2003; Bolívar and Lynch, 2004). It occurs in leaf litter and under rocks on the ground in the Andean forests and páramos, and has not been recorded from anthropogenic habitats (Bolívar and Lynch, 2004). This frog has been listed by the IUCN as Endangered (EN) (Bolívar and Lynch, 2004). Rhinella sp. (Fig. 2) is a toad that lives in leaf litter and is known only in the private reserve “Forest of the CHEC” between 2500

Herpetology Notes, volume 5: 79-84 (2012) (published online on 21 April 2012)

Strategies employed by three Neotropical frogs (Amphibia: Anura)to avoid predation

Sergio Escobar-Lasso1,* and Gustavo A. González-Duran1,2

1 Fundación R.A.N.A (Restauración de Ambientes Neotropica-les Alterados), Calle 61ª Nº 24A 45, (Manizales, Colombia).

2 Departamento de Ciencias Biológicas, Universidad de Caldas, Manizales, Caldas, Colombia.

*Corresponding author; e-mail: biosergiobike@gmail.com.

Sergio Escobar-Lasso & Gustavo A. González-Duran80

and 2700 m, in the municipality of Manizales, Caldas, Colombia (pers. obs). Phyllomedusa venusta (Fig. 3) is endemic to Colombia and Panama and it occurs from sea level up to 1300 m (Acosta-Galvis, 2000; Acosta-Galvis, Huertas-Salgado and Rada, 2006). It is an arboreal species, living on vegetation in humid lowland forest, including dry forest and degraded habitats with forest patches (Renjifo et al., 2004).

We documented the defensive behaviour displayed by three species (O. percrassa, Rhinella sp., and Phyllomedusa venusta) when facing the approach and handling by the authors.

We observed three individuals of O. percrassa displaying defensive behaviour. The individuals were observed by SEL, from 9 to 11 September 2011, between 0900 and 1700 h, in the high Andean forests, in the private reserve “Forest of the CHEC” (5°01’29.06’’ N, 75°22’30.75’’W; ca 3021 m), municipality of

Villamaria, Caldas, Colombia. Individuals of Rhinella sp. were observed by GGD, from 18 to 21 March 2009, between 0900 and 1400 h, in patches of the Andean forests, around the private reserve “Forest of the CHEC” (Vereda “Montaño”, 4° 59.528’ N, 75° 27.399’ W; ca 2526 m), municipality of Villamaria, Caldas, Colombia. Individuals of P. venusta were observed by GGD, from 12 to 20 May 2010, between 1900 and 2200 h, in the humid lowland forest, around the private reserve “Rio Manso”, municipality of Norcasia, Caldas, Colombia (5°39’57.6’’N, 74°46.4’3’’W; ca 220 m).

We observed three individuals of O. percrassa displaying defensive behaviour. The first individual remained motionless during approach. When it was manipulated it displayed body-raising with its legs extended laterally (sensu Toledo, Sazima and Haddad, 2011), keeping the head in contact with the ground. During this display the frog inflated its

Figure 1. Defensive behaviour of Osornophryne percrassa. (A) Two synergistic defensive behaviours: body-raising with legs laterally stretched and puffing up the body. (B) Synergistic defensive behaviours: Thanatosis and flipping onto the back. (C) Synergistic defensive behaviours: thanatosis, flipping onto the back and Puffing up the body. The frog remains motionless in a position with the belly up, raising its belly with the help of its limbs. Note that in this position, the yellow patches of the frog belly are more visible. (D) Typical posture. Note the difference in the position of the trunk and extremities with regard to the defensive postures.

Antipredator strategies in three Neotropical frogs 81

body (Fig. 1A). The deployment of the defensive behaviour lasted 5 minutes. The second individual also remained motionless during the approach. When it was manipulated it remained motionless in a position with the belly up and the limbs extended and oriented in different directions (Fig. 1B), even when it was repeatedly touched and manipulated. When we tried to move the limbs of the toad to another position we found no resistance from it. The individual remained with their eyes open and it remained in this posture for 7 minutes. The third remained motionless during the approach. When the individual was touched, it remained motionless in a position with the belly up; at this time, the individual inflated its body and raised its belly with the help of its limbs (Fig. 1C). In this position, yellow patches of the frog belly become more conspicuous. The individual remained motionless even when it was constantly touched and manipulated. When we tried to move the limbs of the toad to another position, we found no resistance from it, and it remained in this posture for 6 minutes. After returning to its typical posture (Fig. 1D), it was handled again displaying the same defensive behaviour described above once more. Throughout the defensive behaviour, the individual remained with its eyes open. According to the terminology proposed by Toledo, Sazima and Haddad (2011) the three individuals of O. percrassa displayed five types of defensive behaviours: immobility, thanatosis, puffing up the body, body-raising and flipping onto the back.

We observed seven individuals of Rhinella sp.

displaying defensive behaviour. The seven individuals did not differ in their defensive displays. The initial defensive behaviour against approach was to remain motionless. When they were manipulated, the individuals exhibited thanatosis, remained immobile in the observer’s hand, and maintained this posture when they were placed with the belly up on the ground (Fig. 2A). Individuals remained in that position for an average of 596.7 ± 169.2 s (range = 302-756, n = 7) even when constantly touched or handled. When we tried to move the limbs of the toads to another position, we found no resistance from them. After returning to their typical posture (Fig. 2B), individuals were handled again and they displayed the same defensive behaviour described above. Throughout the defensive behaviour, the individuals remained with their eyes closed. According to the terminology proposed by Toledo, Sazima and Haddad (2011), these individuals displayed immobility and thanatosis.

We observed six individuals of P. venusta displaying defensive behaviour. The individuals did not differ in their defensive behaviour. When individuals were found, their initial defensive behaviour was to remain motionless. When individuals were caught, the fore and hind limbs were bent and kept close to the body; the same applies to the fingers (Fig. 3A). Individuals were kept in a rigid position, arching the body and head ventrally (Fig. 3B). The individuals always remained with their eyes closed. When the individuals were released and placed on the leaf blades, they remained in

Figure 2. Individual of Rhinella sp. displaying thanatosis or death feigning (A) and in its typical posture (B). Note the difference in the position of the trunk and extremities with regard to the defensive postures.

that position for an average of 279.16 ± 56.2 s (range = 209-346, n = 6). After returning to their typical posture (Fig. 3C), they were handled again and displayed the same defensive behaviour described above. According to the terminology proposed by Toledo, Sazima and Haddad (2011), these individuals displayed immobility and contracting.

This is the first report of defensive behaviour of O. percrassa (see review in Toledo, Sazima and Haddad, 2011). Our observations suggest that the defensive behaviour of this species is complex as, with few tested individuals we were able to record five different behaviours, which can be displayed independently or synergistically.

According to the terminology proposed by Toledo, Sazima and Haddad (2011), body-raising has two sub-categories, depending on the position of the legs to extend: body-raising with legs vertically stretched and body-raising with legs laterally stretched. In the family Bufonidae, the body-raising is known only in two species (see review in Toledo, Sazima and Haddad, 2011). In both species the legs are extended vertically. The behaviour observed in one individual of O. percrassa is therefore the first record of body-raising with legs laterally stretched for the family Bufonidae and it is the first record of such behaviour for the genus Osornophryne (see review in Toledo, Sazima and Haddad, 2011). Body-raising of both types

Sergio Escobar-Lasso & Gustavo A. González-Duran82

Figure 3. Contracting behaviour in Phyllomedusa venusta with eyes partially closed: the individual in hands (A) and placed in a leaf (B), and P. venusta in typical posture (C). Note the difference in the position of the trunk and extremities with regard to the defensive postures.

is common to occur synergistically with puffing up the body (sensu Toledo, Sazima and Haddad, 2011). For the family Bufonidae, puffing up the body is known in six species of the genera Anaxyrus, Dendrophryniscus and Osornophryne (Toledo, Sazima and Haddad, 2011; in this work).

For the family Bufonidae, thanatosis has been reported in species of the genus Dendrophryniscus, Osornophryne and Rhinella (Toledo, Sazima and Haddad, 2010; in this work). Thanatosis observed here was similar to that described for Melanophryniscus moreirae (Bufonidae) by Toledo and Haddad (2009a). However, the thanatosis observed for another individual has some novel components, as the individual raised its belly with the help of its limbs and inflated its body. This behaviour may be novel for anurans.

Osornophryne percrassa is characterized by cryptic coloration on the back (usually dark brown or black) and a conspicuous aposematic coloration in the belly (with patches of bright yellow) (Ruiz-Carranza and Hernández-Camacho, 1976; Mueses-Cisneros, 2003). Several species have a conspicuously coloured belly (or other underside parts; e.g. Paratelmatobius spp., Leptodactylus pustulatus, or Melanophryniscus spp.), and some of these species were observed displaying flipping onto the back and remaining motionless (see Toledo and Haddad, 2009a). This position displays the aposematic coloration of their bellies. We believe that the same happens to O. percrassa, since this species always displays thanatosis with the belly up and in this position the yellow patch is highly visible (see Fig. 1B, C). Our hypothesis is that the yellow patch of O. percrassa evolved as a strategy to avoid predation.

Many species of Rhinella display contracting and only in two species have been observed thanatosis (see review in Toledo, Sazima and Haddad, 2010). Therefore, the present study is the first record of the defensive behaviour of Rhinella sp. and is the third record of thanatosis for the genus Rhinella.

Toledo, Sazima and Haddad (2010) suggest that thanatosis is a defensive behaviour to avoid subjugation. The observations made in O. percrassa and Rhinella sp. agree with the above, because individuals of both species displayed thanatosis only when they were touched or handled. Thanatosis behaviour observed in O. percrassa differs from the behaviour observed in Rhinella sp., since the latter species were not observed displaying thanatosis with the belly up. However, when the observer places the individuals of Rhinella sp. on the floor in the belly up position, they remain in that position

(see Fig. 2A), but this is not their natural behaviour. This is the first record of defensive behaviour of P.

venusta. Toledo, Sazima and Haddad (2010) suggest that contracting or shrinking is characteristic of the genus Phyllomedusa. Our observations support the above. However, of the 32 species in the genus Phyllomedusa (Faivovich et al., 2005), only for 10 (31.25%) contracting have been reported (see review in Toledo, Sazima and Haddad, 2010). We believe it is necessary to describe the defensive behaviour in all species of Phyllomedusa, to understand whether “contracting” is shared by all species of the genus and whether it has some degree of plasticity. For example, in some species of hylids as in Aplastodiscus perviridis, Dendropsophus microps, Hypsiboas albopunctatus, H. bischoffi, have been observed that they display both thanatosis and contracting, and they can even display an intermediate between the two types of behaviour (Toledo, Sazima and Haddad, 2010).

Acknowledgements. We express our sincere thanks to Professor John Harold Castaño, for providing the logistics and access to the reserve Rio Manso, Carlos Sanchez for providing us the entrance to his farm and Ferley Leyniker Celis for helping with the revision of the spelling and grammar of the English language.

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Accepted by Philip de Pous