Herpetology Notes, volume 12: 443-445 (2019) (published online on 01 May 2019)
Description of defensive postures of the natterjack toad Epidalea calamita (Laurenti 1768) and notes on the release of toxic secretions
Rainer Stawikowski1 and Tim Lüddecke2*
True toads of the family Bufonidae are amongst the The natterjack toad, Epidalea calamita (Laurenti 1768), most prominent amphibians on earth. Its members carry is such a non-invasive species for which descriptive specialised poison glands embedded into their skin and work on its behavioural and chemical defence has possess parotoid macroglands, glandular systems rich in been lacking so far. It is native to Southwestern and these poison glands, that are visible as parallel bulges Central Europe, including Germany (Sillero et al., at the toads temple (Duellman and Trueb, 1994). From 2014). Habitat-wise it prefers well warmed areas with their poison glands, toads are able to secrete strong light soils, such as dunes or pine forests and settles in acting skin poisons that are rich in cardiotoxic steroids shallow, warm ponds (Brinkmann and Podloucky, 1987; (Habermehl, 1994). Some representatives have been Podloucky, 1994). As typical for bufonids, E. calamita introduced to novel geographical areas (e.g. Rhinella carries a pair of prominent parotoids and a plethora of marina (Linnaeus 1758) to Australia and Duttaphrynus poison gland openings over its body, which indicates melanostictus (Schneider 1799) to Madagascar), where that the species is capable of secreting high amounts of they cause serious damage to local faunas (e.g. Hagman skin poison. et al., 2009; Shine, 2010). Naïve predators, normally Herein, we report on the observed defensive behaviour preying upon native species, often ingest these invading of German natterjack toads ranging from body inflation bufonids and succumb to their skin poison afterwards. to skin poison secretion. Since this kind of natural Through this, members of Bufonidae emerged as a group history observations for E. calamita is scarce, we of highly infamous anurans and became a concern for evaluate our report as an advance in the understanding conservationists (e.g. Tingley et al., 2017). of the defensive ecology of this species. Given this outstanding role of bufonids among other Since 2014, we surveyed amphibian populations at anurans, it is not surprising that several scientists three sites in the area of Gelsenkirchen, North Rhine recently focused their research on bufonid toxicity as Westphalia, Germany (Gelsenkirchen-Ückendorf, well as on the interaction of these toxins with their Gelsenkirchen-Erle and Gelsenkirchen-Bulmke; with potential targets (e.g. Marshall et al., 2018). Contrary permission from the nature conservation authority of to such investigations it is, however, noteworthy that Gelsenkirchen) (Stawikowski, 2019). Each amphibian natural history observations on the release of skin that was found in this context was photographed for poisons remain relatively rare for Bufonidae. This is documentation purposes. With more than 300 sightings, especially true for non-invasive species. For those, E. calamita was one of the most abundant species that it often remains largely unknown which defensive we observed in our fieldwork sites, especially during behaviours are applied and also to what extent skin the reproduction period in spring (Günther and Meyer, poisons may be secreted. 1996). In most cases the animals showed no obvious signs of agitation while the photographic documentation was performed, but sporadically a defensive behaviour was displayed (Fig. 1A and B): In that, the toad drastically 1 Siegfriedstr. 14, 45888 Gelsenkirchen, Germany. inflates its body, leading to an artificial increase of 2 Animal Venomics Research Group, Fraunhofer Institute for Molecular Biology and Applied Ecology, Winchesterstraße 2, its size. Additionally, the animal straightens its legs 35394 Gießen, Germany. whereby its body is lifted far from the ground. Together, * Corresponding author: [email protected] these mechanisms contribute to the toad appearing a lot 444 Rainer Stawikowski & Tim Lüddecke
Figure 1. Epidalea calamita displaying its defensive posture, illustrated in lateral view (A) and anterior view (B): The animal expands its body by inflation and leg stretching to appear larger, while simultaneously the toxin-rich parotoids are presented. Another strategy to defend themselves is the secretion of skin poison. Often this happens from parotoid glands directly in smaller amounts (C, poison droplets are indicated by an arrow), but can also be performed extensively from poison glands that are distributed over the animals whole body. In this case, the animal is quickly covered in several milky-white droplets (D).
larger and therefore more defensive as it actually is. For in parotoid-bearing amphibians. It was previously E. calamita it is anecdotally mentioned that this inflation described for other bufonid toads such as the common may be rarely accompanied with vocalization (Günther toad Bufo bufo (Linnaeus 1758), a close relative of E. and Meyer, 1996). We observed this vocalization calamita, but was also reported in fire salamanders frequently, often in combination with cloacal discharge (Salamandra salamandra (Linnaeus 1758)) (Kowalski (sensu Toledo et al., 2011), when animals were et al., 2018; Lüddecke et al., 2018; Lüddecke, 2019). On captured. However, we never noticed such a behaviour the other hand, amphibians that lack such macrogland when inflation was performed. Following inflation and structures usually opt for different behavioural defences, leg extension, the toad lowers its head and presents such as tail rising in marbled newts (Triturus marmoratus its prominent pair of parotoids towards the source of (Latreille 1800)) or the famous unken reflex in Bombina agitation. Since these macroglands actually store a vast species, to only name a few (e.g. Haberl and Wilkinson, proportion of the amphibians’ toxin resources, it appears 1997; Lüddecke et al., 2018). reasonable that this behaviour might protect the toad In E. calamita, the secretion of skin poison is another from some predatory assaults: If a predator would attack commonly observed reaction besides the above described the toad frontally in this posture, it would unavoidably defensive postures. The poison appears as white droplets be confronted with a high dosage of the toads chemical on the skin surface and is often released in small amounts defence. on the toads back, the legs or the parotoids (Fig. 1C and This behaviour of presenting body parts with highest D). Some toads seemingly felt outstandingly threatened loads of toxins towards predators seems to be widespread from us during their photographic documentation and Description of defensive postures of the natterjack toad 445 they released their toxic secretions quite extensively Lüddecke, T., Schulz, S., Steinfartz, S., Vences, M. (2018): A across their whole body (Fig. 1D). The secretion salamander´s toxic arsenal: Review of skin poison diversity and of skin poison on the toad’s skin surface and the function in true salamanders, genus Salamandra. The Science of Nature 105: 56. utilisation of defensive postures can be combined but Marshall, B.M., Casewell, N.R., Vences, M., Glaw, F., Andreone, can also happen independently from each other. It F., Rakotoarison, A., Zancolli, G., Woog, F., Wüster, W. (2018): is noteworthy that in some situations the secretion of Widespread vulnerability of Malagasy predators to the toxins of toxins was performed without actually manipulating the an introduced toad. Current Biology 28(11): 654–655. animals. Such a behavior represents a rare observation Mailho-Fontana, P. L., Antoniazzi, M.M., Toledo, L.F., Verdade, since usually secretion is performed only after active V.K., Sciani, J.M., Barbaro, K.C., Pimenta, D.C., Rodrigues, squeezing of the glandular systems (e.g. when the toad M.T., Jared, C. (2014): Passive and active defense in toads: the parotoid macroglands in Rhinella marina and Rhaebo guttatus. is captured by a predator). Comparative observations Journal of Experimental Zoology 321: 65–77. of voluntary release of skin poison are rare, but were Mebs, D. (2010): Gifttiere. 3rd. Edition, Wissenschaftliche described from S. salamandra and the bufonid Rhaebo Verlagsgesellschaft Stuttgart. guttatus (Schneider 1799)(Mailho-Fontana et al., 2014; Podloucky, R. (1994): Verbreitung und Situation der Kreuzkröte Lüddecke et al., 2018). However our observations in E. in Niedersachsen. Berichte des Landesamtes für Umweltschutz calamita indicate that such a behaviour might be more Sachsen Anhalt 14: 6–8. common among amphibians, or at least in bufonid toads, Shine, R. (2010): The ecological impact of cane toads (Bufo marinus) in Australia. The Quarterly Review of Biology 85(3): than previously thought. 253–291. The skin poison of Bufonidae contains, among other Sillero, N., Campos, J., Bonardi, A., Corti, C., Creemers, R., compounds, high amounts of cardiotoxic steroids that Crochet, P.A., Crnobrnja Isailovic, J., Denoël, M., Ficetola, cause severe intoxications in vertebrates (Mebs, 2010). G.F., Goncalves, J., Kuzmin, S., Lymberakis, P., de Pous, P., The impressive amount of such highly toxic skin poison Rodriguez, A., Sindaco, R., Speybroeck, J., Toxopeus, B., that is released by E. calamita and on which we report Vieites, D.R., Vences, M. (2014): Updated distribution and here, represents a good example of the toxic potential biogeography of amphibians and reptiles of Europe. Amphibia- Reptilia 35: 1–31. of the family. Stawikowski, R. (2019): Beobachtungen zur Absonderung giftiger Hautsekrete bei Kreuzkröten. Feldherpetologisches Magazin References 11:17–23. Brinkmann, R., Podloucky, R. (1987): Vorkommen, Gefährdung Tingley, R., Ward-Fear, G., Schwarzkopf, L., Greenlees, M.J., und Scutz der Kreuzkröte (Bufo calamita Laur.) in Niedersachsen Phillips, B.L., Brown, G., Clulow, S., Webb, J., Capon, R., unter besonderer Berücksichtigung von Abgrabungen Sheppard, A., Strive, T., Tizard, M., Shine, R. (2017): New – Grundlagen für ein Artenhilfsprogramm.Berichte der Weapons in the Toad Toolkit: A Review of Methods to Control Naturhistorischen Gesellschaft Hannover 129: 181–207. and Mitigate the Biodiversity Impacts of Invasive Cane Toads Duellman, W.E., Trueb L. (1994): Biology of amphibians. JHU, (Rhinella marina). The Quarterly Review of Biology 92(2): Baltimore 123149. Günther, R., Meyer, F. (1996): Kreuzkröte – Bufo calamita Toledo, L.F., Sazima, I., Haddad, C.F.B. (2011): Behavioural Laurenti, 1768. In: Günther, R. (Ed.): Die Amphibien und defences of anurans: an overview. Ethology Ecology and Reptilien Deutschlands: 302–321, Jena. Evolution 23: 1–25. Haberl, W., Wilkinson, J.W. (1997): A note on the unkenreflex and a similar defensive postures in Rana temporaria (Anura, Amphibia). British Herpetological Society Bulletin 61: 16–20. Habermehl, G. (1994): Gift-Tiere und ihre Waffen. 5 Aufl. Springer. Berlin Hagman, M., Phillips, B.L., Shine, R. (2009): Fatal attraction: adaptions to prey and on native frogs imperil snakes after invasion of toxic toads. Proceedings of the Royal Society B: Biological Sciences 276(1668): 2813–2818. Kowalski, K., Sawościanik, O., Rychlik, L. (2018): Do Bufonids Employ Different Anti-Predator Behaviors Than Ranids? Comparison Among Three European Anurans. Copeia 106: 120–129. Lüddecke, T. (2019): Über das Hautgift beim Feuersalamander. Feldherpetologisches Magazin 11: 9–16. Accepted by Wouter Beukema