North-Western Journal of Zoology Vol. 5, No. 1, 2009, pp.218-223 P-ISSN: 1584-9074, E-ISSN: 1843-5629 Article No.: 051206

A melanistic adder ( berus) neonate born from a cryptic female: Are black vipers born heavier?

Alexandru STRUGARIU* & Ştefan R. ZAMFIRESCU

“Alexandru Ioan Cuza” University, Faculty of Biology, Carol I Blvd. No. 20 A, 700506, Iaşi, Romania. * Corresponding author’s e-mail address: [email protected]

Abstract. The ecological advantages and disadvantages of melanism in , especially in the adder ( (L. 1758)), have been intensively studied over the years. General consideration would agree that, in most cases, adders which go on to become melanistic, are born cryptic, with a typical zigzag pattern, and darken with age, becoming black in the second or third year of life. In the present note we report the second known case in which a cryptic female adder gave birth to a melanistic neonate. Based on the fact that the observed body mass (7 g) of the melanistic neonate lies beyond the upper 95% confidence zone of the expected body mass (5.74g ± 0.977) calculated using the linear regression model from the cryptic neonates for a snout-vent length of 175 mm, and on the supporting literature, we propose a new hypothesis (which should be tested in future studies) according to which, melanistic adders may benefit of a significant higher fitness since birth.

Key words: reptiles, colour polymorphism, reproduction, new hypothesis, body size, fitness advantage

The coloration of is considered 2003). Although generally rare in reptiles, to be an adaptation to different biotic and melanism has been reported to be locally abiotic environmental factors. In general, frequent in some species in certain geogra- the colouration of an plays an im- phical areas or under certain environmental portant role in predator avoidance (through conditions (e.g. Monney et al. 1995, Bittner crypsis, mimicry or aposematism) (e.g. et al. 2002, Tanaka 2007). The adder (Vipera Sweet 1985), inter- and intraspecific commu- berus (Linnaeus 1758)) is one of the nication and sexual selection (e.g. Roulin & European species in which colour Bize 2006). In ectothermic animals, colora- polymorphism has been most studied. The tion could also be important in thermo- species is probably the most widespread regulation (e.g. Trullas et al. 2007). venomous in the world, being present Colour polymorphism (the presence of from the British Isles in the West to the two or more phenotypic morphs in the Sachalin Island in the East and from same population) and the mechanisms northern Sweden in the North to the Balkan which maintain it, have been the subject of Peninsula in the South (Saint Girons 1980, numerous studies and several hypotheses Nilson & Andrén 1997). The typical, cryptic have been suggested (e.g. Munday et al. morph of the adder is characterized by a

©NwjZ, Oradea, Romania, 2009 North-West J Zool, 5, 2009 www.herp-or.uv.ro/nwjz Oradea, Romania Are black vipers (V. berus) born heavier? 219 dark, contrasting zigzag stripe which is faint darker vertebral line could be dis- present longitudinally on the dorsal side of tinguished outdoors under direct sunlight. the animals (e.g. Fuhn & Vancea 1961). The female and all the neonates were re- While albino or leucistic specimens are very leased, 14 days after parturition, at the place rarely observed (Krecsak 2008), melanistic where the female was initially captured. individuals have been very frequently Prior to this, all neonates were measured reported. Higher proportions of melanistic with digital callipers and weighed with a specimens in adder populations are usually digital scale to the nearest mm and 0.1 g, associated with mountain areas, high respectively. latitudes, coastal northern areas and islands, The genetic background of melanism in thus with colder environments (Thiesmeier the adder is still unknown and the general & Voelkl 2002). However, melanistic consideration is that melanistic adders be- specimens also represent the vast majority come so in their second or third year of life of the eastern populations of Vipera berus (Forsman 1995). However, on very rare nikolskii, which are present at lower occasions, melanistic neonates with mela- altitudes and latitudes (Milto & Zinenko nistic mothers have been recorded (e.g. 2005, Zinenko 2006). Biella 1977, Forsman 1995) and, only once, In 2007-2008 we conducted field studies, melanistic neonates with a cryptic (zigzag) focused on several aspects of the natural mother have been previously observed history and ecology of adders inhabiting the (Schiemenz 1978). Schiemenz (1978) re- lowland deciduous forests from the Central ported a cryptic female adder which gave Moldavian Plateau (Eastern Romania). In birth to 10 cryptic and three melanistic the summer of 2008 our studies also focused neonates. Thus, at least to our knowledge, on the reproductive biology of the species, our record is the second one of a cryptic for which four gravid females (one female adder giving birth to a melanistic melanistic and three cryptic) were taken neonate. The fact that V. berus is one of the into captivity and kept individually in most studied snake species in the world and indoor terrariums until parturition. The first that numerous studies have focused on its viper to reach parturition was the smallest reproductive characteristics (e.g. Luiselli of the cryptic specimens (Snout-Vent Length 1992, Madsen & Shine 1992, Capula & = 550 mm; Pre-partum body mass = 146.6 g; Luiselli 1994, Monney et al. 1995) without Post-partum body mass = 85.5 g) and she mentioning the phenomenon we are des- gave birth to five neonates, all alive, on the cribing in the present note, is an argument 20th of August 2008. A relevant aspect of for the rarity of this occurrence. As a result, this event was the fact that one of the neo- we consider that it is important to mention nates was melanistic. As almost all mela- another observation: on the 8th of June 2008, nistic adders studied in eastern Romania a juvenile male adder was caught near to (Strugariu & Zamfirescu in prep.), this spe- the habitat in which the adult female dis- cimen was fairly black, with the exception cussed above was captured. This specimen of some small white spots on the labial and was also melanistic despite its small size the longitudinal row of dorsal scales which (SVL = 230 mm) (Fig. 2). Thus, we suppose are in contact with the ventral plates and for that it is most probable that this specimen the yellowish coloured tail (Fig. 1). A very was only about 9-10 months of age (con-

North-West J Zool, 5, 2009 220 Strugariu, A. & Zamfirescu, Ş.R. sidering it would have been born in August this could suggest that melanistic neonates –September 2007) and it was also born me- occur more frequently in the respective lanistic. Even if we cannot know if its mo- population. ther was melanistic or cryptic in coloration,

Figure 1. The melanistic neonate adder (Vipera berus) born from a cryptic (zigzag) female. Photo taken at the release date. (Photo: A. Strugariu)

Figure 2. The juvenile (9-10 months approximated age) melanistic adder caught in june 2008. (Photo: A. Strugariu)

North-West J Zool, 5, 2009 Are black vipers (V. berus) born heavier? 221

The proportion of melanistic specimens neonate (175 mm), the value would be 5.742 in the litter of “our” cryptic female did not g (95% confidence interval: 4.77-6.72 g). The differ significantly to that derived from observed BM value (7 g) for the same SVL Schiemenz’s (1978) data (χ2 test: Yates lies beyond the upper limit of the 95 % corrected χ2 = 0.3805; df = 1; p = 0.5373). The confidence zone for an isolated observation. mean body mass (BM) of all the neonates Thus, the body mass of the melanistic from our female was 5.687 g (SD = 0.842) neonate does not fit the cryptic neonate and the snout-vent length (SVL) was 173.4 model (Fig. 3). mm (SD = 8.234). If we use the linear Some authors have reported that mela-

regression function (F(1,26) = 113.363; p < nistic males are longer or, at least heavier 0.0001) derived from the available cryptic than cryptic individuals and therefore have neonate data (n = 27 neonates from 4 litters; a better mating success (e.g. Andrén & SVL as independent variable and BM as Nilson 1981, Luiselli 1992, Monney et al. dependent variable) to calculate the ex- 1995). The larger size and/or weight of me- pected BM for the SVL of the melanistic lanistic adders has been explained by the

9

8

7

6

5 BM (g) BM

4

y = 0.08x - 8.2504 r² = 0.8193 3

2

1 130 140 150 160 170 180 190 200 SVL (mm)

Confidence zone of the individual estimate (95%) Confidence zone of the regression line (95%) predicted g for 175 mm if cryptic observed g for 175 mm (melanic) Cryptic Model

Figure 3. The difference between the observed and the expected weight of the melanistic neonate. The latter is based on the relationship between the snout-vent length (SVL – mm) and the body mass (BM - g) of the cryptic neonate neonates.

North-West J Zool, 5, 2009 222 Strugariu, A. & Zamfirescu, Ş.R.

fact that, being superior in thermoregula- References tion (Gibson & Falls 1979), melanistic spe- Andrén, C., Nilson, G. (1981): Reproductive success and cimens are able to be active and to forage risk of predation in normal and melanistic colour for a longer part of the day and of the year, morphs of the adder, Vipera berus. Biological Journal and, therefore grow faster and larger of the Linnaen Society 15: 235-246. Biella, H.J. (1977): Studien zur Verbreitung und Okologie (Andrén & Nilson 1981, Madsen & Stille der Kreuzotter (Vipera b. berus) in der Oberlausitz. 1988). Although scarce, the data presented Abhandlungen und Berichte des Naturkunde by us in the present note seem to confirm Museums Gorlitz 51: 1-9. Bittner, T.D., King, R.B., Kerfin, J.M. (2002): Effects of the fact that melanistic adders are heavier body size and melanism on the thermal biology of than cryptic ones at a given length. Also, in garter (Thamnophis sirtalis). Copeia 2: 477-482. the light of our findings, we propose a new Capula, M., Luiselli, L. (1994): Reproductive strategies in hypothesis according to which melanistic alpine adders, Vipera berus – The black females bear more often. Acta Oecologica – International Journal adders (or at least the ones which are born of Ecology 15 (2): 207-214. melanistic) benefit from an important Forsman, A. (1995): Opposing fitness consequences of advantage with regard to fitness since the colour pattern in male and female snakes. Journal of Evolutionary Biology 8: 53-70. moment of their birth. This could be com- Fuhn, I.E., Vancea, Ş. (1961): The Fauna of the People’s plemented later in their lives by the faster Republic of Romania, vol. XIV, Fascicola II: Reptilia. growth rates which are associated with Ed. Academiei R.P.R., Bucharest. [in Romanian]. thermoregulatory superiority. Nevertheless, Gibson, A.R., Falls, J.B. (1979): Thermal biology of the common garter snake, Thamnophis sirtalis L. II The the potential advantages associated with effects of melanism. Oecologia 43: 99-109. melanism in newborn adders appear to Krecsak, L. (2008): Albinism and leucism among have low adaptive value, given the domi- European Viperinae: a review. Russian Journal of Herpetology 15 (2): 97-102. nance of cryptic morphs in adder popula- Luiselli, L. (1992): Reproductive success in melanistic tions. Therefore, the validity of our hypo- adders: a new hypothesis and some considerations thesis as well as the possible mechanisms on Andren and Nilson’s (1981) suggestions. Oikos which would enforce it must be tested in 64 (3): 601-604. Madsen, T., Shine, R. (1992): Determinants of future studies. reproductive success in female adders, Vipera berus. Oecologia 92: 40-47. Madsen, T., Stille, B. (1988): The effect of size dependent mortality on colour morphs in male adders, Vipera berus. Oikos 52: 73-78. Milto, K.D., Zinenko, O.I. (2005): Distribution and morphological variability of Vipera berus in Eastern Acknowledgements. We are grateful to Drs. T. Madsen, . Pp. 56-73. In: Ananjeva, N. & Tsinenko, O. G. Nilson, M. A. L. Zuffi and an anonymous reviewer for (eds): Herpetologia Petropolitana - Proceedings of their constructive critical comments and suggestions on the 12th Ordinary General Meeting of the Societas this manuscript. We also thank C. Puşcaşu for her help Europaea Herpetologica, Saint-Petersburg, Russia. in properly keeping the adders in captivity and data Monney, J.-C., Luiselli, L., Capula, M. (1995): Correlates collecting and I. Gherghel, M.V. Huţuleac-Volosciuc and of melanism in a population of adders (Vipera berus) A. Mizeruş who assisted one of the authors (A.S.) in the from the Swiss Alps and comparisons with other field. The research was carried out under permission alpine populations. Amphibia-Reptilia 16: 323-330. from the Romanian Academy of Sciences (C.M.N.) and Munday, P.L., Eyre, P.J., Jones, G.P. (2003): Ecological A.S. was financially supported by two awards from the mechanisms for coexistence of colour poly- National University Research Council of Romania morphism in a coral-reef fish: an experimental

evaluation. Oecologia 137 (4): 519-526.

North-West J Zool, 5, 2009 Are black vipers (V. berus) born heavier? 223

Nilson, G., Andrén, C. (1997): Vipera berus. Pp. 388-389. advantages? Biological Journal of the Linnean In: Gasc, J.P., Cabela, A., Crnobrnja-Isailovic, J., Society 92 (2): 309-332. Domen, D., Grossenbacher, K., Hauffner, P., Thiesmeier, B., Voelkl, W. (2002): Distribution and Lescure, J., Martens, H., Martinez Risca, J.P., ecology of melanistic adders – a review. Zeitschrift Maurin, H., Oliveira, M.E., Sofianidou, T.S., Veith, fur Feldherpetologie 9 (2): 127-142. M. & Zuiderwijk, A. (eds): Atlas of Amphibians and Trullas, S.C., van Wyk, J.H., Spotilla, J.R. (2007): Thermal reptiles in Europe. Collection Patrimoines Naturels, melanism in ecotherms. Journal of Thermal Biology 29, Societas Europaea Herpetologica, Museum 32 (5): 235-245. National d’Histoire Naturelle & Service du Zinenko, O.I. (2006): Habitats of Vipera berus nikolskii in Petrimone Naturel, Paris. Ukraine. Pp. 205-209. In: Vences, M., Kohler, J., Roulin, A., Bize, P. (2006): Sexual selection in genetic Ziegler, T., Boehme, W. (eds.): Herpetologia colour-polymorphism species: a review of Bonnensis II - Proceedings of the 13th Congress of experimental studies and perspectives. Journal of the Societas Europaea Herpetologica, Bonn, Ethology 25 (2): 99-105. Germany. Saint-Girons, H. (1980): Biogeographie et evolution des vipers europeennes. Compte Rendu Sommaire des Seances. Societe de Biogeographie 496: 156-172. Schiemenz, H. (1978): Zur Okologie und Bionomie der Submitted: 05 November 2008 Kreuzotter (Vipera b. berus L.). Zoologische / Accepted: 27 March 2009 Abhandlungen / Staatliches Museum für Tierkunde in Dresden 35: 203-217. Sweet, S.S. (1985): Geographic variation, convergent Published Online: 30 March 2009 crypsis and mimicry in gopher snakes (Pituophis melanoleucus) and western rattlesnakes (Crotalus viridis). Journal of Herpetology 19: 44-67. Tanaka, K. (2007): Thermal biology of a colour- dimoprhic snake, Elaphe quadrivirgata, in a montane forest: do melanistic snakes enjoy thermal

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