sign in sign up
<<
Home , Echinotriton, Notophthalmus, Ommatotriton, Paramesotriton, Taricha, Triturus

Herpetology Notes, volume 14: 509-512 (2021) (published online on 11 March 2021)

Unken reflex – a new defensive behaviour for dobrogicus (Kiritzescu, 1903)

Alexandra E. Telea1,2, Florina Stănescu1,2,3,*, and Dan Cogălniceanu1

Escape from predation is a vital survival skill since individual might display only a partial reflex (Löhner, predation is considered one of the top causes of 1919; Bajger, 1980; Toledo et al., 2011). In and mortality. in particular have evolved a wide , Brodie (1983) classified the Unken reflex range of escape behaviours. Brodie (1983) performed as ‘low-intensity’ when only the tail but not the chin is a thorough review and described about 30 defensive elevated, and ‘high-intensity’ when both tail and chin strategies in newts and salamanders, ranging from biting are elevated to display most of the ventral colouration. or vocalizing to tail lashing, tail autotomy, and display Brodie and Howard (1972) proposed the term “U-shaped of the ‘Unken reflex’ (see below). Similarly, Toledo Unken reflex” for newts and salamanders, since these et al. (2011) described and categorized 30 defensive adopt a rigid U-shaped posture to better expose behaviours in , some of them being also reported their ventral pigmentation. from newts and salamanders. Triturus dobrogicus (Kiritzescu, 1903) is part of One of the many strategies is to remain motionless the T. cristatus (Laurenti, 1768) . It while signalling toxicity (aposematic signalling). is distributed in parts of central and eastern , Specific bright colouration (i.e., aposematic colouration) where it occurs mostly along the floodplain of the combined with defensive postures warn predators of a Danube River and its tributaries (Arntzen et al., 2009). possible high cost to their intentions, and may deter them Grillitsch (1984) mentioned Unken reflex-like and other from attacking (Toledo et al., 2011; Vitt and Caldwell, defensive behaviours, such as turning upside down and 2014). Perhaps the best-known example of this behaviour immobile posture in T. cristatus and curling-up of the is the Unken reflex, first described in the genusBombina tail in a juvenile T. dobrogicus. Here, we provide the first (Löhner, 1919; Vitt and Caldwell, 2014). Since then, this observation of the Unken reflex inT. dobrogicus. type of posturing has been described in other amphibians, We observed the Unken reflex on two occasions in including salamanders and newts (Table 1). An individual a population of T. dobrogicus from Peceneaga Lake, displaying this defensive behaviour will usually arch its Romania (45.0119°N, 28.1548°E), on 17 March 2019 back and elevate the head and limbs, while remaining and on 24 October 2020, both instances occurring perfectly immobile, thus flashing its bright lateral and/ during daytime. On both occasions, we found adults and or ventral colours. In anurans, the eyes are closed in full subadults of Danube crested along the shoreline, Unken position, with the limbs covering them (Löhner, hidden under rocks and scattered garbage and debris. 1919). In some cases (e.g., in low temperatures) the When uncovered, some of the individuals displayed a specific defensive behaviour. At the beginning of the display, the individuals would take on an immobile posture and coil their tail (Fig. 1A), coil their body to 1 Ovidius University Constanţa, Faculty of Natural and move the snout close to the vent, elevate the coiled tail, Agricultural Sciences, Aleea Universității 1, Campus B, head, and limbs (Fig. 1B, C), and finally arch their back, 900470 Constanța, Romania; and Chelonia Romania, Pașcani in this posture, to fully expose their ventral colour pattern 5 Bucharest, Romania. (Fig. 1D). This full display is characteristic of the high- 2 Ovidius University Constanţa, CEDMOG Center, Tomis Avenue 145, Constanța, Romania intensity Unken reflex, as previously described in other 3 Ovidius University Constanţa, Black Sea Institute for newts and salamanders (e.g., Brodie, 1983; Table 1). Development and Security Studies, Aleea Universității 1, Other individuals observed at the same site displayed 900470 Constanța, Romania. different defensive behaviours when uncovered, * Corresponding author. E-mail: [email protected] including (1) adopting an immobile posture for a short © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. period of time and, in the absence of further stimuli, 510 Alexandra E. Telea et al.

Table 1. Literature records of Unken reflex (U) or similar behaviour (S) in newts and salamanders. “Similar behaviour” refers to descriptions that agree with the Unken reflex, but for which the authors did not apply the name Unken reflex.

Species Behaviour References Cynops pyrrhogaster U Brodie and Howard, 1972; Brodie, 1977; Mochida, 2009 Cynops sp. U Brodie, 1983 andersoni U Brodie, 1983 Echinotriton sp. U Brodie, 1983 alpestris U Brodie, 1977, 1983; Herrero and Zimnić, 2015 boscai U Marco and Leguia, 2001 Lissotriton helveticus U Brodie, 1977 Lissotriton vulgaris U Brodie, 1977 Lissotriton sp. U Brodie, 1983 [as part of Triturus] Brodie and Howard, 1972; Brodie, 1977, 1983; Mochida, 2009; viridescens U Tanaka and Means, 2017 Notophthalmus perstriatus U Brodie, 1977 Notophthalmus meridionalis U Bare and Guadiana, 2019 Notophthalmus sp. U Brodie, 1983 vittatus S Yakin et al., 2019 hongkongensis U Brodie and Howard, 1972; Brodie ,1977 Paramesotriton longliensis U Nishikawa, 2014 Paramesotriton sp. U Brodie, 1983 Salamandrina terdigitata U Lanza, 1966 Salamandrina sp. U Brodie, 1983 granulosa U Brodie, 1977, 1983 Taricha rivularis U Brodie, 1983 Taricha torosa U Brodie, 1977 Taricha sp. U Brodie, 1983 Triturus cristatus U, S Brodie, 1977; Grillitsch, 1984; Denton, 1990 Triturus ivanbureschi U, S Jablonski, 2014; Yakin et al., 2019 Triturus karelinii S Tarkhnishvili and Gokhelashvili, 1999 Triturus sp. U Brodie, 1983 verrucosus U Brodie, 1983 Tylototriton sp. U Brodie, 1983

slowly moving towards other available hiding places; of factors such as distance to the potential predator, (2) displaying a partial or low-intensity (Brodie, 1983) temperature, distance to shelter, reproductive state, Unken reflex by coiling their tail and body, with the satiety (Vitt and Caldwell, 2014). Immobility is snout positioned near the vent, covering the head with usually adopted as an avoidance response if the one forearm, and with tail and hindlimbs partially raised potential predator is positioned at a greater distance. on one side to expose the ventral colouration (Fig. 2). In case of direct stimuli, like grabbing or poking, an Although we found both adults and subadults at this site, immobile posture might also be adopted in order to only subadults (n = 3) displayed the Unken reflex. minimize stimulation for further attack. Combined with The “flight or fight” responses of amphibians toa aposematic colouration, this is a useful strategy to warn potential threat vary widely and depend on a number and deter potential predators (Brodie et al., 1974; Vitt Unken reflex: a New Defensive Behaviour forTriturus dobrogicus 511

Figure 1. High-intensity Unken reflex in a Triturus dobrogicus subadult. (A) Immobile posture with coiled tail. (B) Body coiled, snout close to vent, elevated coiled tail. (C) Elevated limbs and head. (D) Arched body and complete Unken reflex display. Photos by Dan Cogălniceanu. and Caldwell, 2014). In some cases, an individual will displays are preferred at lower temperatures. They also adopt two or more defensive strategies simultaneously, suggested that aposematic postures are triggered by to benefit from higher chances of escape (Toledo et al., stronger stimuli. We suggest that T. dobrogicus in our 2011). study area adopted the observed defensive strategies Our observations were made during cold weather because of the relatively low temperature that affected (ranging from 2–19°C during a 24-h period), both their physiological performance. immediately after and before , and the defence responses were triggered by direct stimuli Acknowledgements. This work was supported by Asociația (i.e., sudden flipping of the shelter). Haberl and pentru Dezvoltare Durabilă Dakia in the framework of the project Wilkinson (1997) suggested that the Unken reflex POIM - SMIS 116964 - “Managementul Integrat al Podișului Nord Dobrogean” (MiPoNoDo), and partly by grant PN-III-1.2- might be stimulated by low-temperature conditions in PCCDI-2017-0721 (INTERASPA). FS is partly supported by the Rana temporaria Linnaeus, 1758. Similarly, the project ANTREPRENORDOC, in the framework of Human Mochida (2010) found a negative correlation Resources Development Operational Programme 2014-2020, between temperature and the tendency to adopt an financed from the European Social Fund under the contract immobile posture as a defensive behaviour in Cynops number 36355/23.05.2019 HRD OP /380/6/13 – SMIS Code: pyrrhogaster (Boie, 1826), while Toledo et al. (2011) 123847. The research in the area was carried out under permit suggested that anurans are more prone to escape by 191/APND/23.10.2018. running when exposed to higher temperatures. In a controlled experiment, Polčák and Gvoždík (2014) References examined both temperature and sex effects on defensive Arntzen, J.W., Bugter, R., Cogălniceanu, D., Wallis, G.P. (1997): responses in Ichthyosaura alpestris (Laurenti, 1768) The distribution and conservation status of the Danube crested and concluded that at high body temperature newts newt, Triturus dobrogicus. Amphibia-Reptilia 18: 133–142. would rather flee, while immobility and other defence Arntzen, J.W., Kuzmin, S., Jehle, R., Denoël, M., Anthony, B., 512 Alexandra E. Telea et al.

Grillitsch, H. (1984): Zum Feindabwehr-Verhalten des Kammolches, Triturus cristatus (Laurenti, 1768) (Caudata: ). Salamandra 20(1): 61–63. Haberl, W., Wilkinson, J.W. (1997): A note on the unkenreflex and similar defensive postures in Rana temporaria (Anura, Amphibia). The Herpetological Bulletin 61: 16–20. Herrero, D., Zimić, A. (2015): Unken reflex inMesotriton alpestris. Boletín de la Asociación Herpetológica Española 26(1): 4–7. Jablonski, D. (2014): Natural history notes. Triturus ivanbureschi. Defensive behavior. Herpetological Review 45(2): 302–303. Lanza, B. (1966): Reazione di tipo Unkenreflex in un Urodelo (Salamandrina terdigitata). Zeitschrift für Tierpsychologie 23: 855–857. Löhner, L. (1919): Über einen eigentümlichen Reflex der Feuerunken nebst Bemerkungen über die „tierische Hypnose”. Pflüger’s Archiv für die gesamte Physiologie des Menschen und der Tiere 174: 324–351. Marco, A., Leguia, J. (2001): “Unken reflex” en el tritón iberico, Triturus boscai: postura defensiva innata en hábitats terrestres. Revista Española de Herpetología 15: 5–11. Mochida, K. (2009): A parallel geographical mosaic of morphological and behavioral aposematic traits of the newt, Cynops pyrrhogaster (Urodela: Salamandridae). Biological Figure 2. Low-intensity Unken reflex in aTriturus dobrogicus Journal of the Linnean Society 97: 613–622. subadult, with the body coiled snout close to vent, a forearm Mochida, K. (2010): Temperature-dependent aposematic behavior covering the head, eyes closed, and with the coiled tail and in the newt Cynops pyrrhogaster. Zoological Science 27(7): hindlimbs partially raised on one side to expose the ventral 555–558. colouration, shown in (A) a view from above and (B) in lateral Nishikawa, K. (2014): Natural history notes. Paramesotriton view. Photos by Florina Stănescu. longliensis. Defensive behavior. Herpetological Review 45(3): 475–476. Polčák, D., Gvoždík, L. (2014): Should I stay or should I go? The Miaud, C., et al. (2009): Triturus dobrogicus. The IUCN Red influence of temperature and sex on predator-induced responses List of Threatened Species 2009: e.T22216A9366668. in newts. Behaviour 89: 79–84. Bajger, J. (1980): Diversity of defensive responses in populations Tarkhnishvili, D.N., Gokhelashvili, R.K. (1999): Advances of fire toads (Bombina bombina and Bombina variegata). in Research in the Former Soviet Union: The Herpetologica 36(2): 133–137. Amphibians of the . Sofia, Bulgaria, Pensoft Publishers. Bare, E.A., Guadiana, C.J. (2019): Natural history notes. Tanaka, T., Means, B.D. (2017): Natural history notes. Notophthalmus meridionalis. Anti-predatory behavior. Notophthalmus viridescens (). Predation. Herpetological Review 50(2): 335. Herpetological Review 48(1): 155–157. Brodie, E.D., Jr. (1977): antipredator postures. Copeia Toledo, L.F., Sazima, I., Haddad, C. (2011): Behavioral defences of 1977: 523–535. anurans: an overview. Ethology Ecology and Evolution 23: 1–25. Brodie, E.D., Jr. (1983): Antipredator adaptations of salamanders: Vitt, L.J., Caldwell, J.P. (2014): Herpetology: an Introductory evolution and convergence among terrestrial species. In: Biology of Amphibians and Reptiles. Fourth Edition. San Adaptations to Terrestrial Environments, p. 109–133. Margaris, Diego, California, USA, Academic Press. N.S., Arianoutsou-Faraggitaki, M., Reiter, R.J., Eds., Boston, Yakin, B.Y., Çiçek, K., Afsar, M., Tok, C.V. (2019): Observation on Massachusetts, USA, Springer. defensive behavior of two salamandrids: Ommatotriton vittatus Brodie, E.D., Jr., Howard, R.R. (1972): Behavioral in the (Gray, 1835) and Triturus ivanbureschi Arntzen and Wielstra, defensive displays of the urodele amphibians Notophthalmus 2013. South Western Journal of Horticulture, Biology and viridescens and Pseudotriton ruber. Bioscience 22(11): 666–667. Environment 10(1): 45–49. Brodie, E.D., Jr., Johnson, J.A., Dodd, C.K., Jr. (1974): Immobility as a defensive behavior in salamanders. Herpetologica 30(1): 79–85. Denton, J. (1990): Defensive reflexes in newts of the Triturus. The Herpetological Bulletin 32: 30. Dodd, C.K., Jr., Brodie, E.D., Jr. (1976): Defensive mechanisms of neotropical salamanders with an experimental analysis Accepted by Wouter Beukema of immobility and the effect of temperature on immobility. Herpetologica 32(3): 269–290.