Colour Aberrations in Bufotes Balearicus (Anura: Bufonidae) and Hyla Perrini (Anura: Hylidae) from Italy

Herpetology Notes, volume 13: 57-60 (2020) (published online on 30 January 2020) “Translucent” colour aberrations in Bufotes balearicus (Anura: Bufonidae) and Hyla perrini (Anura: Hylidae) from Italy Giacomo Bruni1,*, Angelo Di Mitri2, Laura Grecchi3, and Matteo Riccardo Di Nicola4 Chromatic anomalies in amphibians may often be On the other hand, dark variants with black eyes and difficult to classify. One of the most enigmatic cases pale blackish skin may appear when iridophores are concern the occurrence of translucent skin, often lacking (Richards and Nace, 1983). combined with black coloured eyes (Henle and Dubois, Several observations of anurans showing these 2017). Transparent skin is the natural condition for colouration anomalies are reported in literature (reviewed some anuran species, such as the as Glass Frogs of in Henle and Dubois, 2017), and there are similar cases the Neotropics (Family Centrolenidae), and there are of individuals which have been identified as melanoid several frogs which normally possess black eyes where (Richards et al., 1969), axanthic (Jablonski et al., 2014), the pupil is difficult to distinguish (Glaw and Vences, or hypomelanistic (Turner, 2017). Herein we report 1997; Henle and Dubois, 2017). In other anurans, the three distinct cases of chromatic aberrations involving presence of these characters in only a few individuals translucent skin and black eyes in two European anuran is the result of rare colour mutations (Glaw and Vences, species from Italy. 1997; Sumida et al., 2016). The first observation in chronological order concerns Amphibian colouration is determined via different kinds a young Balearic green toad (Bufotes balearicus of chromatophores: xanthophores and erythrophores [Boettger, 1880]), which was rescued on the road by contain pterinosomes and carotenoid vesicles (yellow to G. B. in the outskirts of Sesto Fiorentino (Province of red colours), iridophores contain light-reflecting platelets Florence, Tuscany) on 7 June 2011 (Fig. 1A). The toad (silvery to golden or blue colours) and melanophores showed black eye colouration without any sign of the contain melanosomes (brown to black colours) (Obika typical iridescent green iris. The skin was translucent and Bagnara, 1964; Bagnara and Hadley, 1973). Black- with highly visible blood vessels. Irregular marks eyed individuals appear so because of the absence of were brownish or greyish instead of bright green. iridophores, while the transparency of the skin might These features suggest the absence of iridophores and be caused by the lack or deficiency of more than xanthophores. However, the presence of reddish warts one type of dermal chromatophore (Jablonski et al., and pinkish parotoid glands indicate the presence of 2014; Sumida et al., 2016; Henle and Dubois, 2017). erythrophores. Therefore, several grades of transparency can be The second record deals with the same species: four observed in amphibians. For instance, when the skin is juveniles of the year were found together under an entirely translucent there is basically absence of all the artificial shelter, by G. B., in a rice-fields area near aforementioned chromatophores (Sumida et al., 2016). Pavia (Lombardy) on 28 July 2017 (Fig.1B).This site is about 222 km as the crow flies from Sesto Fiorentino. One of them possessed black eyes and blackish skin (Fig. 1C-D). Only the ventral side appeared relatively transparent, allowing to discern limb bones and inner organs (Fig. 1C). The spot pattern was poorly marked 1 Viale Togliatti, 50019 Sesto Fiorentino, Florence, Italy. and most visible on the limbs. The other three toads 2 Via Cascina Palazzo, 27020 Nicorvo, Pavia, Italy. 3 Via San Giovannino, 27100 Pavia, Italy. were all normal in eye and skin colouration, except for 4 Via Bobbio, 20144 Milan, Italy. some irregular dark patches on dorsum, head and limbs * Corresponding author. E-mail: [email protected] (Fig. 1B), which resembled the blackish colouration of 58 Giacomo Bruni et al. Figure 1. Balearic green toads Bufotes balearicus. (A) Young individual observed in Sesto Fiorentino; (B) four juveniles found together near Pavia; (C) ventral view of the dark juvenile found near Pavia; (D) lateral view of the same dark individual. Photos by Giacomo Bruni. the other one. We speculate that the observed anomalies were also clearly visible (Fig 2A, 2C). A white ovoid are due to the total or localised absence of iridophores mark was present on the throat (Fig. 2B), which was and a potential overproduction of melanin. consistent with the normal colouration of the species. The last case is particularly remarkable, concerning Given the similarities with the translucent frog obtained an almost completely transparent tree frog (Fig. 2). An by Sumida et al. (2016), we hypothesize that this skin adult female of Po’s tree frog (Hyla perrini Dufresnes coloration is the result of the absence of iridophores and et al., 2018) was found by A. D. M., L. G. and M. R. melanophores, combined with a consistent presence of D. N. in the commune of Nicorvo (Province of Pavia, xanthophores in the dorsal skin and few xanthophores Lombardy) on 15 October 2019 in a farmhouse’s garden in the ventral parts. Nevertheless, melanophores and surrounded by rice fields, about 40 km as the crow flies iridophores were retained in the eyes and likely in the from the previous locality, which is part of the same river patch on the throat. basin (Po River). Eyes appeared partially black with Even though we cannot make assumptions about the asymmetrical silvery-golden patches, where iridophores genetic mechanisms which underlie these chromatic were present (Fig. 2A, 2D). Dorsal skin appeared aberrations (some information is provided by Richards transparent with a pinkish-brownish colouration (Fig. and Nace [1983], Sumida et al. [2016], and Henle and 2A), the ventral side was highly translucent allowing the Dubois [2017]), inbreeding depression due to isolation observation of the ova (Fig 2A, 2C) and blood vessels was stated as one of the potential causes for the higher “Translucent” colour aberrations in Bufotes balearicus and Hyla perrini 59 Figure 2. Po’s tree frog Hyla perrini. (A) dorso-lateral view; (B) ventral view; (C) lateral view; (D) detail of the eye. Photos by Matteo Riccardo Di Nicola. frequency of black-eyed Moor frogs (Rana arvalis) References in an urban populations compared to ones inhabiting Bagnara, J.T., Hadley, M.E. (1973): Chromatophores and color rural habitats (Vershinin, 2004). Our observations were change: the comparative physiology of animal pigmentation. indeed made in areas where agricultural activities and PrenticeHall, Inc., Englewood Cliffs, NJ. urbanization may promote habitat fragmentation and Glaw, F., Vences, M. (1997): Anuran eye colouration: definitions, isolation of amphibian breeding groups. However, variation, taxonomic implications and possible functions. blackish patches in juvenile European green toads Herpetologia Bonnensis. SEH Proceedings, Bonn: 125–138. Henle, K., Dubois, A. (2017): Studies on Anomalies in Natural (Bufotes viridis) from Germany were possibly Populations of Amphibians. Mertensiella, 25: 185–242. connected to radioactive pollution (Henle et al., 2017). Henle, K., Dubois, A., Rimpp, K., Vershinin, V. (2017): Mass Further investigation on these anomalies frequencies is anomalies in green toads (Bufotes viridis) at a quarry in Roßwag, needed to assess whether they may indicate inbreeding Germany: inbred hybrids, radioactivity, or an unresolved case. processes in amphibian populations, and if pollutants Mertensiella, 25: 185–242. can promote their occurrence. Jablonski, D., Alena, A., Vlcek, P., Jandzik, D. (2014): Axanthism in amphibians: A review and the first record in the widespread toad of the Bufotes viridis complex (Anura: Bufonidae). Belgian Acknowledgements. We are grateful to StevenJ. R. Allain Journal of Zoology 144: 93–101. and Benedetta Gambioli for their English revision, to Daniele Obika, M., Bagnara, J.T. (1964): Pteridines as pigments in Pellitteri-Rosa for his suggestions and to Andrea Gazzola for the amphibians. Science 143: 485–487. pre-peer review of the manuscript. Richards, C.M., Nace, G.W. (1983): Dark pigment variants in 60 Giacomo Bruni et al. anurans: classification, new descriptions, color changes and inheritance. Copeia: 979–990. Richards, C.M., Tartof, D.T., Nace, G.W. (1969): A melanoid variant in Rana pipiens. Copeia: 850–852. Sumida, M., Islam, M.M., Igawa, T., Kurabayashi, A., Furukawa, Y., Sano, N., Fujii, T., Yoshizaki, N. (2016): The first see-through frog created by breeding: description, inheritance patterns, and dermal chromatophore structure. Scientific reports 6: 24431. Turner, G.S. (2017). A hypomelanistic Roth’s tree frog Litoria rothii from North Queensland. Queensland Naturalist 55: 22. Vershinin, V. L. (2004). Frequency of iris depigmentation in urban populations of Rana arvalis frogs. Russian journal of ecology 35: 58–62. Accepted by Christoph Liedtke.

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