Interspecific Amplexus Between Rana Dalmatina (Fitzinger in Bonaparte, 1838) and Salamandra Salamandra (Linnaeus, 1758) in “Shumensko Plato” Nature Park, Bulgaria

Herpetology Notes, volume 14: 653-655 (2021) (published online on 10 April 2021)

Interspecific amplexus between Rana dalmatina (Fitzinger in Bonaparte, 1838) and Salamandra salamandra (Linnaeus, 1758) in “Shumensko Plato” Nature Park, Bulgaria

Teodora V. Koynova1,* and Nikolay D. Natchev1,2

There are many observations of unusual amplexus in Fire salamanders are predominantly crepuscular and anurans (e.g., interspecific, holding of artificial objects, nocturnal, but can also be seen during the day, when and with dead specimen - both inter and intra specific, it rains continuously (Stojanov et al., 2011). After etc.) (Waterstrat et al., 2008; Mollov et al., 2010; Sodre completion of its aquatic larval phase, S. salamandra is et al., 2014; Müller, 2016; Shin et al., 2020). The price strictly terrestrial (Manenti et al., 2017). Mating occurs for such behaviour, however, is a waste of resources: on land, and in Bulgaria it happens in September- time, energy and reproductive material, and in turn this December. In the spring or autumn of the following can lead to death from exhaustion, reproductive failures year, the larvae are deposited into suitable aquatic and even affect the population dynamics (Pearl et al., habitats (Stojanov et al., 2011). 2005; Hochkirch et al., 2007; Gröning and Hochkirch, During a field survey within the Natural Park 2008; D’Amore et al., 2009; Álvarez, 2011). “Shumensko Plateau” in North-Eastern Bulgaria In the present study, we report on a case of interspecific (43.2622°N, 26.8695°E; Datum WGS 84; 490 m amplexus between two sympatric species, the Agile elevation), we observed two cases of interspecific frog (Rana dalmatina Fitzinger in Bonaparte, 1838) amplexus between a frog, R. dalmatina, and a and the Fire salamander (Salamandra salamandra salamander, S. salamandra. The events were observed Linnaeus, 1758). Records of sexual interaction between on 9 March 2020, in two different instances, at 13:57 anurans and urodelans are rare (Moldowan et al., 2013; h and 14:04 h respectively. The interspecific pairs Crane and Ferrari, 2015) and there is only one report were located 2 m away from each other. The first of amplexus between R. dalmatina and S. salamandra interspecific amplexus was found in a small pond. A (Simović et al., 2014). male Agile frog was grasping the adult salamander in The Agile frog is a medium-sized frog and like most of the inguinal section of the body (Fig. 1A). The second the temperate anurans, it breeds in stagnant waterbodies interspecific amplexus (Fig. 1B) was found on the like puddles, small lakes and pools (Stojanov et al., shore and was in the axillary body section (the usual 2011). The breeding season starts immediately after amplexus for R. dalmatina). The water temperature was hibernation, which occurs in late February to early 10.3 °C, water pH was 7.17, air temperature was 12.2 March in the Balkan Peninsula (Stojanov et al., 2011; °C. Both pairs were observed for 25 minutes. During Iosob and Prisecaru, 2014). Amplexus in R. dalmatina this time, the frogs held a tight grip. The salamander is axillary and Hettyey et al. (2005) reported that the from the shore kept moving around carrying the frog amplexus can extend from several hours up 3 to 4 days. on its back. The pairs were still in amplexus when we However, in a previous study, we observed an amplexus left the area. On the territory of the park, we detected that lasted 12 days (Koynova et al., 2020). only two pairs of available water bodies, at a distance of about 3 km from each other. During this field survey at these water bodies for that day, we encountered a total 1 Department of Biology, Faculty of Natural Sciences, Shumen of 21 salamanders (including these in amplexus with the 2 University, Universitetska 115, 9700 Shumen, Bulgaria. Agile frogs) only in one of these pairs (area of 10 m and 2 Department of integrative Zoology, Vienna University, 25 m2 respectively). Althanstrasse 14, 1090 Vienna, Austria. Although R. dalmatina and S. salamandra occur * Corresponding author. E-mail: [email protected] in similar habitats within their sympatric range, such © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. amplexus events are apparently rare. A case of such 654 Teodora V. Koynova & Nikolay D. Natchev

dislodging frog amplexus (see Simović et al., 2014) and the fitness of both participants may be impacted. The negative effects seem to be mostly related to energy waste for the frogs and disturbance for the salamanders. The energy reserves of the male Agile frogs from the region are at their minimum during the reproduction period (Koynova et al., 2021). As all of the observed salamanders were most probably females that came to the puddles to deposit their larvae, the efforts to release themselves from amplexus may impact the successful birth of their offspring.

Acknowledgements. This work was supported by the Bulgarian Ministry of Education and Science under the National Program for Research “Young Scientists and Postdoctoral Students” and under Grant No. RD-08-67/25.01.2021.

References

Álvarez, J.A. (2011): Bufo boreas (Western Toad). Davian behavior. Herpetological Review 42: 408–409. Biaggini, M., Campetti, I., Corti, C. (2018): Breeding activity of the agile frog Rana dalmatina in a rural area. Animal Biodiversity and Conservation 41: 405–413. Crane, A., Ferrari, M. (2015): Intense interspecific amplexus Figure 1. Rana dalmatina males grasping Salamandra of wood frogs, Lithobates sylvaticus, on a tiger salamander, salamandra adults into (A) inguinal amplexus, (B) axillary Ambystoma tigrinum. Herpetology Notes 8: 295. amplexus. Photos by Teodora Koynova. D’Amore, A., Kirby, E., Hemingway, V. (2009): Reproductive Interference by an Invasive Species: An Evolutionary Trap? Herpetological Conservation and Biology 4: 325–330. sexual behaviour of Agile frogs was reported for the Gröning, J., Hochkirch, A. (2008): Reproductive interference first time from Serbia in 2013 (Simović et al., 2014). R. between animal species. The Quarterly review of biology 83: 257–282. dalmatina has an extended breeding season which can Hettyey, A., Török, J., Hévizi, G. (2005): Male Mate Choice Lacking last from 30 to over 70 days (Hettyey et al., 2005; Vági in the Agile Frog, Rana dalmatina. Copeia 2: 403–408. and Hettyey, 2016; Biaggini et al., 2018) especially Hochkirch, A., Gröning, J., Bücker, A. (2007): Sympatry with when the water resources are scarce (Koynova et al., the devil: reproductive interference could hamper species 2020). A possible explanation for the abnormal sexual coexistence. Journal of Animal Ecology 76: 633–642. behaviour of the Agile frogs may be related to their Iosob, G.A., Prisecaru, M. (2014): Observations on the life cycle strongly male-biased populations, the coincidence in the and reproductive behavior in Rana Dalmatina F. Studii şi peaks of the breeding activity of the two species, and the Cercetări 23: 50–59. Koynova, T., Doichev, D., Natchev, N. (2020): Impacts of resource limited number of water bodies in the area (Koynova et limitations on the reproduction behaviour in the Agile Frog al., 2020). (Rana dalmatina) on the territory of Natura park “Shumensko The associated costs for the salamanders involved in plato”. ZooNotes 168: 1–4. the intraspecific amplexus may be rather negative, as the Koynova, T., Valkova, S., Simov, N., Langourov, M., Natchev, weight of the frogs can interfere with their movement N. (2021): Data on the stomach content analysis and fat-body ability. This can be problematic especially when the morphology in the Agile frog (Rana dalmatina Fitzinger in salamanders are grasped into inguinal amplexus and Bonaparte, 1838) during the mating season. Ecologia balkanica cannot leave the aquatic environment. In this case, the 13: 27–33. Manenti, R., Conti, A., Pennati, R. (2017): Fire salamander weight of the frog pressed on the caudal section of the (Salamandra salamandra) males’ activity during breeding salamander and restricted its movement. However, in season: effects of microhabitat features and body size. Acta axillary amplexus it seemed that the salamander could Herpetologica 12: 29–36. handle the additional weight and carry the frog on its Moldowan, P.D., Legros, D.L., Tattersall, G.J. (2013): Lithobates back, out of the water. Urodelans are not efficient in sylvaticus (Wood Frog). Davian behavior. Herpetological Interspecific amplexus between Rana dalmatina and Salamandra salamandra 655

Review 44: 296–297. Simović, A., Anderson, N., Anđelković, M., Gvozdenović, S., Mollov, I.A., Popgeorgiev, G.S., Naumov, B.Y., Tzankov, N.D., Đorđević, S. (2014): Unusual amplexuses between anurans and Stoyanov, A.Y. (2010): Cases of abnormal amplexus in anurans caudates. Herpetology Notes 7: 25–29. (Amphibia: Anura) from Bulgaria and Greece. Biharean Sodré, D., Vilhena-Martins, A. A., Vallinoto, M. (2014): Biologist 4: 121–125. Heterospecific amplexus between the frog Leptodactylus Müller, H. (2016): Heterospecific amplexus of a male Tomopterna macrosternum (Anura: Leptodactylidae) and the toad Rhinella delalandii with a dead Sclerophrys cf. capensis (Amphibia: cf. granulosa (Anura: Bufonidae). Herpetology Notes 7: 287– Anura: Bufonidae et Pyxicephalidae). Herpetology Notes 9: 288. 283–284. Stojanov, A., Tzankov, N., Naumov, B. (2011): Die Amphiben und Pearl, C.A., Hayes, M.P., Haycock, R., Engler, J.D., Bowerman, J. Reptilien Bulgariens. Frankfurt am Main, Germany, Chimaira. (2005): Observation of interspecific amplexus between western Vági, B., Hettyey, A. (2016): Intraspecific and interspecific North American ranid frogs and the introduced American competition for mates: Rana temporaria males are effective bullfrog (Rana catesbeiana) and an hypothesis concerning satyrs of Rana dalmatina females. Behavioral Ecology and breeding interference. The American Midlands Naturalist 154: Sociobiology 70: 1477–1484. 126–134. Waterstrat, F.T., McIntyre, A.P., Hayes, M.P., Phillips, K.M., Curry, Shin, Y., Ambu, J., Borzee, A. (2020): Additional observations on T.R. (2008): Ascaphus truei (Coastal tailed frog). Atypical heterospecific amplexus in Asiatic toads (Anura: Bufonidae: amplexus. Herpetological Review 39: 458. Bufo gargarizans) in the Republic of Korea. Herpetology Notes 13: 411–413.

Accepted by Florina Stanescu