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Case of defensive behavior in Pelobates syriacus (Amphibia: Pelobatidae)

Defensive or antipredator behavior of amphibians can
have several forms (see Brodie, 1983; Toledo, Sazima
and Haddad, 2011). According to these authors, escape
is the most common defensive reaction, but many
species also take advantage of passive defenses. These
species utilize their cryptic coloration and body shape
to remain motionless when encountering a predator, a
defense strategy called “immobility” (e.g., Bufonidae,
Hylidae, Odontophrynidae, Megophryidae). An extreme
case of such immobility is thanatosis, death feigning,
shrinking or contracting (Toledo, Sazima and Haddad,
2010, 2011). Dispensing toxins in the skin can be also
an efficient defensive strategy. Relatively poisonous
species advertise their toxicity via bright aposematic
coloration (e.g., Dendrobatidae, Salamandridae). Other
species advertise their toxicity by specific behavior, while
they enlarge the body and expose their paratoid glands
like Bufo spp. to a predator (e.g., Sharma et al., 2011).
An exceptional antipredator strategy at amphibians
is “Unkenreflex” (Hinsche, 1926) first described for
Bombina spp. This strategy is very well known in the
literature which involves lifting and withdrawing of
the legs off the substratum, arching the body, showing
ventral aposematic colors, close eyes and produce toxic
secretions (Toledo, Sazima and Haddad, 2011). Similar
behavior has been reported in diverse evolutionary
or geographic groups of amphibians, including
salamanders [Lissotriton boscai (Marco and Leguía,
2001), Salamandrina terdigitata (Lanza, 1967)], frogs
[e.g. Boophis albilabris (Andreone, 2002), Hemisus
marmoratus (Greenbaum et al., 2012), Hypsiboas spp.
(Angulo and Funk, 2006), Lithobates capito (Means,
2004), Nyctixalus pictus (Das, Leong and Tan, 2004),
Rana spp. (Haberl and Wilkinson, 1997; Schlüpmann,
2000; Jablonski and Gvoždík, 2009; Carretero et al.,
2011), Rhacophorus spp. (Duong and Rowley, 2010;
Streicher, Smith and Harvey, 2011)] or toads [e.g.
Melanophryniscus spp. (Brusquetti, Baldo and Motte,
2007; Almeida-Santos et al., 2010), Neobatrachus
pictus (Williams et al., 2000)].
The Syrian spadefoot toad (Pelobates syriacus
Boettger, 1889; Pelobatidae) is found in the Balkans
(Bulgaria, FYROM, Greece, Romania and Serbia),
Turkey, Middle East and the Caucasus region (Arnold
and Ovenden, 2002). There, they inhabit typical
terrestrial habitats, including sandy and loamy soils with
a variety of permanent or semi-permanent ponds for
reproduction. Among other congeners of Pelobatidae,
“immobility” is only known from P. fuscus (Hinsche,
1928; Jablonski and Gvoždík, 2009).
During a trip to south-eastern Bulgaria in July
2013, coastal biotopes near the town of Primorsko
were visited. While exploring the surroundings of an
abandoned building in the pine-oak woods (north of
the town, 42.286808° N, 27.749842° E; altitude 16 m
a. s. l.) one of us (PB) found an adult specimen of P.
syriacus (approximately 45 mm SVL) under an old
wooden board. The animal was found at 17:49 (local
time) on 22 July 2013. After lifting the wooden board,
the animal remained motionless and slightly pinned to
the ground for about 10 seconds (Fig. 1A). There was
a layer of old polystyrene beneath the board, which
detached after a few seconds and fell onto the animal.
The animal immediately took up the defensive posture.
It flattened its body, closed its eyes, lifted its front limbs
and located it alongside head up the substrate (Fig. 1B).
The specimen remained in such a posture for a couple
of minutes, and then returned to a normal position just
after the direct touch by observer.
To our knowledge this is the first report of a defensive
behavior resembling the Unkenreflex in P. syriacus,
and the first report for the Pelobatidae family. Similar
Herpetology Notes, volume 7: 141-143 (2014) (published online on 11 April 2014)
Case of defensive behavior in Pelobates syriacus
(Amphibia: Pelobatidae)
Daniel Jablonski1* and Petr Balej2
1 Department of Zoology, Comenius University in Bratislava,
Mlynská dolina B-1, 842 15, Bratislava, Slovakia
2 Zdeňka Bára 114/4, 700 30 Ostrava, Czech Republic
*Corresponding author; e-mail:
Daniel Jablonski & Petr Balej
behaviors have been recorded for many species
of amphibians (see citations above). However, the
appropriate terminology of similar behavior is not
completely unified. As with our observations, not
every described case from the literature describes the
Unkenreflex (recorded for Bombina, Melanophryniscus,
Pseudophryne and Smilisca; Toledo, Sazima and
Haddad, 2011), because: (i) many species have an
absence of aposematic coloration (e.g. Hypsiboas, Rana,
Rhacophorus), (ii) many species miss specific toxins,
(iii) in many cases, specimens bow only their front
part of body instead of the whole body like the genus
of Bombina spp., (iv) not every specimen hides its eyes
in the typical Unkenreflex. That is why the description
of behaviors as the Unkenreflex is, in the majority of
described situations, inaccurate. In connection with the
characteristic posture, the new separate term for this
type of defensive reaction was coined “eye-protection”
(Toledo, Sazima and Haddad, 2011). Features during
Unkenreflex and eye-protection can be combined
(Toledo, Sazima and Haddad, 2011). For example, these
authors considered the case of the hylid species Smilisca
fodiens (Firschein, 1951) to be Unkenreflex, but this
species lacks aposematic coloration. This case is similar
to other species (Ranidae, Rhacophoridae; see citations
above), whose defensive behaviors were also described
as Unkenreflex, even though the aposematism of the
ventral body part was missing. In addition, Toledo,
Sazima and Haddad (2011) distinguished so-called
full and partial Unkenreflex on the basis presence or
absence specific features during this defensive behavior.
With regard to different presence of features, we assume
that instead of using the term full Unkenreflex, which
is a defensive behavior only with the presence of
aposematic coloration, we should use another type of
behavior described as eye-protection.
We have not answered the question regarding the
initiator of the behavior and what its function might be.
We can hypothesize that the main function is protection
of the eyes, the most important sense organ of frogs, in
the case of acute danger from predators. Jablonski and
Gvoždík (2009) found that the defensive reaction can
be more often artificially provoked in R. temporaria by
tapping on the frog’s head or back to imitate an attack
by predators from above (snakes, birds or mammals;
Stojanov, 2005; Toledo, Sazima and Haddad, 2011).
Owing to our subsequent observations (also from R.
dalmatina) it is possible that some specimens benefit
from this behavior more often at lower temperatures
(early spring, high altitude, morning etc.) when they are
hypothermic. In this case, observed specimens of ranid
frogs had slower reactions and more often preferred the
latter described defensive reaction instead of escape.
The temperature of surroundings thus can probably play
a role in the presence of this behavior (see Haberl and
Wilkinson, 1997), but it does not have to be an initiating
factor in general (e.g. at tropical species; see Streicher et
al., 2011; Roelke et al., 2011). To sum up, other reports
of similar types of behavior at various species in the
nature or systematic and experimental observation in
artificial conditions are thus very important in order
to understand the evolution of behavior patterns in
Acknowledgments. We wish to thank Eli Greenbaum (University
of Texas at El Paso, USA) and Miguel A. Carretero (University of
Porto, Portugal) for their comments on the first manuscript draft.
Figure 1. A - The found specimen Pelobates syriacus before
the defensive behavior. B – The same specimen presenting the
defensive behavior of eye-protection.
Accepted by Philip de Pous
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Case of defensive behavior in Pelobates syriacus 143
... D efensive behaviours in frogs and toads have been well reviewed (e.g. Toledo et al., 2011;Jablonski & Balej, 2014;Jablonski, 2017) indicating different families of amphibians are reported to show different types of defense against potential threats. This includes the Ranidae (Toledo et al., 2011;Carretero et al., 2011) and here we describe the first observation of defensive behaviour in Rana graeca. ...
... However, such explanation may be misleading and observed behaviour could be only a part of complex defensive mechanisms that are currently understudied. Similar behaviour is well known for the genus Bombina (unkenreflex) but is usually attributed to warning colouration of skin toxins when on land and to fish swimming below when floating on the surface (Jablonski & Balej, 2014;Bordignon et al. 2018). The possibility that the posture would be of benefit if the individual was regurgitated seems improbable. ...
... The unken reflex posture is also generally associated with aposematic ventral colourations and with the presence of toxic substances [15]. This behaviour has been reported in many amphibian species [16,17], including the anuran genera: Bombina (Bombinatoridae) [18], Melanophryniscus (Bufonidae) [18][19][20][21], Hemisus (Hemisotidae) [22], Boana and Smilisca (Hylidae) [23,24], Neobatrachus (Limnodynastidae) [25], Boophis (Mantellidae) [26], Pseudophryne (Myobatrachidae) [25], Rana (Ranidae) [27][28][29][30][31] and Nyctixalus and Rhacophorus (Rhaphocoridae) [32][33][34]. In urodeles, the unken reflex occurs in some Salamandridae such as Lissotriton [35], Salamandrina [36,37], Taricha [38] and Triturus [39]. ...
... The unken reflex seems to have been confounded with other behaviours (e.g. eye-protection), particularly in species lacking aposematic ventral colouration or toxic substances [17]. ...
Full-text available
Aposematic signals as well as body behaviours may be important anti-predator defences. Species of the genus Melanophryniscus are characterised by having toxic lipophilic alkaloids in the skin and for presenting a red ventral colouration, which can be observed when they perform the behaviour called the unken reflex. Both the reflex behaviour and the colouration pattern are described as defence mechanisms. However, there are currently no studies testing their effectiveness against predators. This study aimed to test experimentally if both ventral conspicuous colouration and the unken reflex in Melanophryniscus cambaraensis function as aposematic signals against visually oriented predators (birds). We simulated the species studied using three different clay toad models as follows: (a) in a normal position with green coloured bodies, (b) in the unken reflex position with green coloured body and extremities and (c) in the unken reflex position with a green body and red extremities. Models were distributed on a known M. cambaraensis breeding site and in the adjacent forest. More than half of the attacks on the models were from birds; however, there was no preference for any model type. Thus, just the presence of the red colour associated with the motionless unken reflex position does not seem to prevent attacks from potential predators. It is possible that the effective aposematic signal in Melanophryniscus is achieved through the unken reflex movement together with the subsequent exhibition of the warning colouration and the secretion of toxins.
Full-text available
This note briefly summarizes some general aspects of the "Unkenreflex" in amphibians and describes possibly related defensive postures in Rana. It includes a foto of the posture in Rana temporaria.
Full-text available
Among vertebrates, defensive behaviours have been reviewed for fishes, salamanders, reptiles, birds, and mammals, but not yet for anuran amphibians. Although several defensive strategies have been reported for anurans, with a few exceptions these reports are limited in scope and scattered in the literature. This fact may be due to the lack of a comprehensive review on the defensive strategies of anurans, which could offer a basis for further studies and insights on the basic mechanisms that underlie these strategies, and thus lead to theoretical assumptions of their efficacy and evolution. Here we review the present knowledge on defensive behavioural tactics employed by anurans, add new data on already reported behaviours, describe new behaviours, and speculate about their origins. A total of 30 defensive behaviours (some with a few sub-categories) are here recognised. The terminology already adopted is here organised and some neologies are proposed. Some of the behaviours here treated seem to have an independent origin, whereas others could have evolved from pre-existent physiological and behavioural features. The role of predators in the evolution of defensive behaviours is still scarcely touched upon and this overview adds data to explore this and other evolutionary unsolved questions.
Full-text available
Descripción de un comportamiento de unkenreflex observado por nosotros en Armenia.
Full-text available
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.
“The exceptional standard of defence has been only reached through the pressure of an exceptional need” (Poulton, 1890). Poulton realized that any new defensive mechanism acquired by a prey species would be followed by the evolution of more effective predatory mechanisms or increased resistance by its predators. A result of these ever present selective pressures on both predator and prey is the evolution of intricate and efficient antipredator mechanisms.
We examined the antipredator mechanisms of 19 Australian hylid species (two genera) and 23 myobatrachid species (nine genera). Frogs of 39 of the 42 species exhibited one or more defensive mechanisms (other than escape), including postures, bright coloration, adhesive skin secretions, and/or calls. Defensive posturing occurred in individuals of 38 species, and varied in relationship to morphology and localization of skin glands. Bright colors, when present, typically were displayed during defensive postures. We documented dramatic geographic variation in the antipredator display of one species, Limnodynastes tasmaniensis. Defensive postures were accompanied by secretions from dorsal skin glands. These secretions were sometimes associated with a distinctive odor. Adhesive skin secretions were present in burrowing frogs of three genera. Defensive calls were emitted by most hylids but none of the myobatrachids. We offer a hypothesis of mimicry to explain the behavior pattern of exposing the bold black and white ventral surface in Pseudophryne and Crinia species.