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

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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@balcanica.cz
Daniel Jablonski & Petr Balej
142
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
amphibians.
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]. ...
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