First Case of Intense Melanism in Bothrops Jararaca

Herpetology Notes, volume 14: 629-637 (2021) (published online on 07 April 2021)

First case of intense melanism in Bothrops jararaca (Wied, 1824) with comments on melanic tendencies in cooler regions within the Brazilian Atlantic Forest (Serpentes: Viperidae)

Breno Hamdan1,*, Valéria Ferreira1, Bianca Duque1, Sávio Freire Bruno2, and Thaís B. Guedes3,4

Introduction also be important to intra and interspecific interactions and to reproductive communication (e.g., Cooper and The colour of squamate reptiles is determined by Greenberg, 1992). Experimental research has shown the presence of pigment cells (chromatophores) in the that melanic ectotherms can heat themselves up quicker dermal layer of the skin. These chromatophores’ basic than non-melanic individuals (Gibson and Falls, 1979; units consist of xanthophores (yellow and orange), Jong et al., 1996), raising the hypothesis that selection erythrophores (red), iridophores (brightness), and some for melanism in cooler climates may be favoured due to basal melanophores that contain melanin, that absorbs the enhanced thermoregulatory abilities of ectothermic light and result in darker shades of colour (Bechtel, animals, in which dark pigments absorb solar energy at a 1978; Kuriyama et al., 2006). Mutations and interactions among the pigment cells may result in polymorphism greater rate compared to lighter individuals (Bonato and and a number of chromatic disorders such as albinism Steinfartz, 2005; Clusella-Trullas et al., 2008a; Jambrich and leucism that can affect population survival in nature and Jandzik, 2012). Similarly, Castella et al. (2013) (Forsman et al., 2008; Nicola and Meier, 2013). found that colour polymorphism plays an important Among chromatic disorders, melanism is a role in the ecology and evolution of asp vipers Vipera polymorphism when there is an excessive production aspis and it is maintained through differential selective of the dark-coloured pigment melanin in the skin or pressures. However, such benefits of dark colouration skin appendages (Chavin, 1969; True, 2003). In snakes, may be counterbalanced by reduced crypsis to predators the expression of melanism varies both in terms of the and enhance a higher predation rate (e.g., Gibson and affected body part and frequency among populations Falls, 1979). Controversially, the study of Bittner and (e.g., Nicola and Meier, 2013). King (2003), investigating the role of dark colouration In squamate reptiles, colouration may provide in garter snakes, did not support the prediction that protection against predators through background melanistic individuals are precise thermoregulators matching or aposematism, influence thermoregulation, and random genetic drift may influence colour pattern and protect critical structures from radiation, but it can frequencies. The Jararaca Lancehead Bothrops jararaca (Wied, 1824) is a medium-sized viperid snake, reaching up to 1600 mm in total length and occurs in Brazil, Paraguay 1 Instituto Vital Brazil, Laboratório de Coleções Biológicas e and Argentina, distributed through forest environments Biodiversidade. Rua Maestro José Botelho, 64, Vital Brazil, and anthropic areas (Sazima, 1992; Campbell and Lamar, Niterói, Rio de Janeiro 24230-410, Brazil. 2004; Guedes et al., 2018; Nogueira et al., 2019). The 2 Universidade Federal Fluminense, Faculdade de Veterinária. species belongs to the Bothrops jararaca clade, which Rua Vital Brazil Filho, 64, Santa Rosa, Niterói, Rio de is restricted to the Chacoan subregion (sensu Morrone, Janeiro 24230-340, Brazil. 2014) and its diversification was reconstructed to 3 Centro de Estudos Superiores de Caxias, Universidade Estadual do Maranhão, Caxias, Maranhão 65064-380, Brazil. this same subregion during the Pliocene/Pleistocene 4 Gothenburg Global Biodiversity Center, University of transition c. 2.37 Ma (95% divtime: 0.3–7.66 Ma) Gothenburg, Department of Biological and Environmental (Hamdan et al., 2019). Juveniles of B. jararaca can Sciences, Box 461, SE-405 30 Göteborg, Sweden. frequently be arboreal and feed on anurans, whereas * Corresponding author. Email: [email protected] adults are terrestrial and feed on rodents (Sazima, © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. 1992; Sazima and Haddad, 1992). This species presents 630 Breno Hamdan �� al. different colour patterns and various tones of brown et al., 1991). (see Lema and Renner, 2010). The most common The average minimum temperatures range between dorsal pattern consists of a series of inverted V-shaped 9.5 to 11° C during the winter in the coldest areas and blotches, bordered by lighter colours (Campbell and 17 to 18.5° C in the warmest ones, whereas the average Lamar, 2004). maximum temperatures range between 26 to 27.5° C A number of studies reporting chromatic anomalies during the summer in the coldest areas and 32 to 33.5° in the colour pattern to Bothrops are available (e.g., C in the warmest ones (Silva and Dereczynski, 2014). Machado, 1945; Amaral, 1977; Ruiz-Sueiro et al., 2010; Material examined. We carefully examined one Ortiz et al., 2017; Tokuda and Costa, 2019; Mendonça et specimen of Bothrops jararaca (IVB 3328) with intense al., 2020) but melanism to B. jararaca has not hitherto melanism from an Atlantic Forest site; the specimen is been reported. Nevertheless, the melanic condition has housed at the Scientific Collection of Instituto Vital been documented in a small number of Viperidae snakes Brazil (Appendix I). We took measurements of snout- such as those of the genus Crotalus and Vipera (Silva, vent length (SVL) and tail length (TL) using a flexible 1999; Nicola and Meier, 2013). ruler. Scale counts followed Dowling (1951) and Peters During collection’s curatorial process at the Instituto (1964). Vital Brazil Scientific Collection we found and Additionally, we examined adult specimens of B. hereafter described the first case of intense melanism jararaca with snout-vent lengths greater than 750 in the Lancehead B. jararaca based on a specimen from mm (see Sazima, 1992; Janeiro-Cinquini, 2004) from the Atlantic Forest, in the municipality of Juiz de Fora, 11 sites (see Appendix I for examined specimens and south-eastern Brazil. The municipality elevation ranges collections) across the Brazilian Atlantic Forest of Rio from 467 to 1104 m with an average annual temperature de Janeiro (Fig. 1). We included only adult specimens of 19.4º C (Pifano et al., 2007). The hottest month is in our sample to exclude the ontogenetic variation bias February, average 23.6 ºC, and the coldest months already known for the species (Sazima 1992). The 11 are July and August, with an average of 15.8º C and sampled sites include the warmer and cooler sites (Table minimum temperature of 7.3° C (Pifano et al., 2007). 1) that allow us to address the secondary aim of our This finding led us to examine a sample of a population study. We analysed 279 specimens by visual inspection of B. jararaca across cooler and warmer sites, to explore and considered melanic tendencies those phenotypes an alleged relationship between higher concentrations with black pigmentation covering most parts of the body of melanin and cooler climate. (e.g., Bonnet et al., 2008). The dorsal colour was faded

Material and Methods Study area. Rio de Janeiro state, Brazil, was chosen Table 1. Temperature data from all localities sampled along as a study area to explore the relationship between the Atlantic Forest in the state of Rio de Janeiro. Annual = colouration and climate due to the species good annual temperature average; Min = minimum temperature average; Max = maximum temperature average. representativeness in scientific collections and the wide array of temperatures. Fully contained within the Atlantic Forest Biome, the state of Rio de Janeiro Localities (n) Annual (°C) Min (°C) Max (°C) represents one of the greatest areas of diversity within Niterói (88) 23.6 19.8 29 this biome in Brazil, where the vegetation physiognomy Maricá (3) 22.7 20.5 29.1 conforms to a wide spectrum of reliefs of mountain Saquarema (1) 23.4 20.7 28.6 ranges and coastal plains (Veloso et al., 1991). Various Arraial do Cabo (3) 23.3 21.2 28.1 geomorphological units are contained within this state, Rio de Janeiro (29) 23.9 20.6 28.8 which result in a diversity of vegetation and landscape Armação de Búzios (1) 23.4 20,9 27.7 types and consequently, an extraordinary variety of Macaé (9) 23.5 19,9 28.4 habitats and species, many of which are endemic Teresópolis (29) 18.9 14.2 24.5 (Veloso et al., 1991). The following vegetation types are recognised: the lowland Atlantic Rainforest (< 50 Nova Friburgo (26) 19.1 15 22.7 m elevation), submontane forest (50–500 m elevation), Petrópolis (32) 19.5 15.6 25 montane forest (500–1500 m elevation) and high São José do Vale do 20.3 16.2 25.9 montane or cloud forest (> 1500 m elevation (Veloso Rio Preto (58)

First case of intense melanism in Bothrops jararaca, Brazilian Atlantic Forest 631

Figure 1. Map evidencing the municipality of Juiz de Fora, Minas Gerais State (red star) where the specimen with intense melanism was collected. The figure also highlights the sites within Rio de Janeiro state from where we examined specimens of B. jararaca to explore an alleged relationship between melanin and cooler climate.

in some preserved specimens, whereas the ventral colour coding specimens with melanic tendencies as 1 and remained unfaded. Thus, the data analysis of melanic whitish ones as 0. Comparisons between groups were tendencies was based on the ventral colour only (Fig. 2). performed Pearson’s Chi-squared test with Yates’ We then categorised the specimens into individuals with continuity correction for categorical variables. Statistical a whitish ventral colour, and individuals with a mostly significance was assessed at a two-sided p value < 0.05. dark ventral colour, hereafter called ‘specimens with All analyses were conducted using R version 3.5.3 (R melanic tendencies’. Core Team, 2019). Analyses. The geographic coordinates were obtained from IBGE (2010) and published gazetteers (NGA, Results 2019). Records lacking precise locality data were Bothrops jararaca specimen with intense melanism. georeferenced using municipality centroids. To each The specimen (IVB 3328; Fig. 3 E-F) presenting specimen, we extracted detailed abiotic data on intense melanism is from the municipality of Juiz de temperature with a resolution of 30 arc seconds from the Fora (21.6888ºS, 43.3444º W), state of Minas Gerais, in WorldClim – Global Climate Data (www.worldclim. south-eastern Brazil. It is an adult male, 1190 mm SVL, org) version 2.1, to the period between 1970–2000 125 mm + n of tail length, 202 ventral scales, 51 + n (Fick and Hijmans, 2017). The map of the study area subcaudal scales, lacunolabial present, 10 supralabials was drawn on QGIS 3.10 (QGIS Core Team, 2020). on right side, 8 on the left, 11 infralabials, 9–10 inter We tested the relationship between melanism, average supraocular rows. This specimen presents a very dark temperature, average minimum temperature and average overall colouration on the dorsum and belly, with the maximum temperature by running a logistic regression classical pattern covered by black, therefore no other (GLM with logit response, Quinn and Keough, 2002) patterning is visible. Dorsal and lateral sides of the head 632 Breno Hamdan ��l.

Figure 2. Detailed view of the ventral portion of a sample of Bothrops jararaca preserved specimens showing: (A, C, E) individuals with melanic tendencies (respectively, IVB 2123, IVB 3500, IVB 4071); (B, D, F) individuals with regular colouration (respectively, IVB 3692, IVB 3732, IVB 3465). Scale bars indicate 10 mm. Photos by Gustavo Cunha.

are lighter than the rest of the body, and the gular region found both specimens with regular colouration and with is notably whitish as far as the first ventral scale (Fig. melanic tendencies. The result of the logistic regression 3). analysis corroborates the best relationship (p <0.0001, Melanic tendencies in Bothrops jararaca. We further Fig. 4) being between average minimum temperature examined 279 adult specimens of B. jararaca, from the and a tendency of melanism in the ventral region of warmer sites (n = 134), and from the cooler sites (n = Bothrops jararaca. 145) located within the Atlantic Forest of Rio de Janeiro Overall, 69% of the sampled individuals (n = 193) (Fig. 2). During the morphological examination, we presented whitish bellies, whereas 31% (n = 86) First case of intense melanism in Bothrops jararaca, Brazilian Atlantic Forest 633

Figure 3. A sample of the dorsal and ventral colour patterns found in B. jararaca contrasting with the specimen with intense melanism. (A–B) Regular colour pattern (IVB 3353); (C–D) anomalous colouration with fused dorsolateral blotches (IVB 1805); (E–F) the melanistic specimen from Juiz de Fora-MG (IVB 3328); (G–H) rare photo of a living individual with melanic tendency from Teresópolis, Rio de Janeiro. Scale bars indicate 10 mm. Photos by Gustavo Cunha (A, B, C, D, E, F) and Rodrigo C. Gonzalez (G, H). 634 Breno Hamdan ��l.

the melanistic specimen, we have also explored and reported a relationship between lower temperatures and melanic tendencies in the ventral region of B. jararaca across the Brazilian Atlantic Forest using a larger sample size. Accessing the appearance and maintenance of melanism in natural populations is still a challenge. Melanic individuals of ectothermic organisms are thought to have a thermoregulatory advantage over their regular-coloured counterparts, in some cases leading to an increase in body size and overall fitness since they would heat up faster than light individuals (Clusella-Trullas et al., 2008b). It has been hypothesised that darker colouration of the skin often compromises Figure 4. Plot of Logistic Regression Model (logit function) the cryptic effects if associated with other patterns with 95% confidence intervals depicting the relationships (e.g., zigzags) and exposes individuals to predation; between ventral colour (0= whitish and 1= blackish; y-axis), however, the mortality risk can be offset, for example, and the site average minimum temperature (x-axis in degrees by a thermoregulatory advantage during basking (e.g., Celsius). Colour intensity of data points indicates the number Gibson and Falls, 1979). Melanin-based colouration of observations (n=279). is highly pleiotropic and influences several other phenotypic traits, such as immune and stress responses in vertebrates might affecting other traits under selection. presented it as mostly dark. However, the frequency (Ducrest et al., 2008). Such an adaptive context has been of these colouring patterns varied according to the proposed to explain the appearance and the maintenance temperature data of the study area. In warmer sites of the of melanism within snake populations (e.g., Madsen and Atlantic Forest of Rio de Janeiro, 85% (n = 114) of the Stille, 1988; Bittner et al., 2002). However, genetic drift examined specimens presented whitish bellies, whereas is also a potential explanation for melanism persistence 15% (n = 20) presented mostly dark bellies. Whitish in snakes (Bittner and King, 2003). bellies are also the majority in the cooler sites of Atlantic To our knowledge, this study provides the first reported Forest in Rio de Janeiro, but the sample structure is melanism case in B. jararaca. It presents preliminary statistically different (Chi-squared = 29.148, df = 1, results indicating a higher frequency of specimens with p <0.0001). In the cooler sites, 54.5% (n = 79) of the melanic tendencies at the cooler sites in the Brazilian examined specimens presented a whitish ventral region, Atlantic Forest of Rio de Janeiro. It is crucial to access whereas 45.5% presented the same region as mostly whether this proportion of melanism in the population dark (n = 66). Besides the white-bellied individuals, the is growing, stable, declining, or merely is randomly frequency of dark-bellied ones is increased. distributed. It is important to deepen understanding of the Neotropical biota’s evolutionary history and Discussion melanism traits in nature using B. jararaca as a study We have reported the first case of an intense system. We highlight that temperature and body colour melanistic specimen (IVB 3328) of B. jararaca from the may be related and explain snake speciation in South municipality Juiz de Fora, state of Minas Gerais, Brazil. America (e.g., Hamdan et al., 2017). We recommend Literature reports a number of polymorphic colouration further morphological and genetic studies to test if to this species, in the shape and colour of dorsolateral there is an evolutionary significance between melanism blotches, or background (e.g., Amaral, 1932; Lema and tendency and population structure in B. jararaca. Renner, 2010, Machado, 1945; Amaral, 1977; Barbosa- Therefore, any conclusion but the observation that the Brum et al., 2019, Fig. 2 of this this study), xanthism Brazilian Atlantic Forest’s cooler sites harbour more (e.g., Ruis-Sueiro et al., 2010), but melanism has not individuals presenting melanic tendencies require been properly reported. The municipality of Juiz de Fora further investigation with larger sample sizes. average annual temperature is 19.4º C with minimum temperature of 7.3° C (Pifano et al., 2007). Apart from First case of intense melanism in Bothrops jararaca, Brazilian Atlantic Forest 635

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Appendix I. Specimens Examined. Bothrops jararaca - BRAZIL: Rio de Janeiro: Arraial do Cabo (22º57”57’ S; 42º1”40’ W): IVB 1897, 2648, 2766; Armação dos Búzios (22º44”49’ S; 41º52”55’ W): IVB 606; Macaé (22º22”15’ S; 41º47”13’ W): IVB 867, 908, 910, 949, 1382, 1383, 2147, 2584, 2890; Maricá (22º55”8” S; 42º49”8’ W): IVB 2328, 3648, 4051; Niterói (22º52”58’ S; 43º6”14’ W): IVB: 265, 403, 418, 750, 914, 1213, 1214, 1218, 1252, 1350, 1356, 1357, 1358, 1379, 1381, 1515, 1550, 1555, 1559, 1587, 1655, 1656, 2035, 2059, 2068, 2125, 2165, 2179, 2200, 2204, 2273, 2277, 2288, 2299, 2321, 2322, 2351, 2408, 2435, 2595, 2755, 2758, 2798, 2830, 2835, 2873, 2895, 2812, 2928, 3217, 3230, 3294, 3370, 3376, 3383, 3465, 3505, 3544, 3554, 3592, 3632, 3639, 3683, 3708, 3711, 3720, 3721, 3725, 3737, 3738, 3744, 3760, 3796, 3837, 3849, 3893, 3903, 3908, 3912, 3936, 3975, 3977, 3998, 4022, 4029, 4052, 4171, 427; Nova Friburgo (22º16”55’ S; 42º31”51’ W): IVB 422, 425, 428, 707, 767, 800, 804, 828, 876, 879, 951, 1077, 1103, 1168, 1204, 1224, 1623, 1707, 1833, 2767, 3770, 2901, 2203, 2095, 3556, 3558; Petrópolis (22º30”18’ S; 43º10”44’ W): IVB 703, 1572, 2452, 2537, 2702, 2857, 2903, 3395, 3396, 3397, 3398, 3411, 3439, 3475, 3492, 3494, 3496, 3500, 3517, 3518, 3537, 3543, 3799, 3821, 3902, 3917, 4057, 3677, 4040, 4056, 4172, 4161; Rio de Janeiro (22º54”10’ S; 43º12”28’ W): IVB 2704, 3307, 3642, 3710, 1294, 2022, 2455, 458, 739, 1791, 1671, 2451, 2494, 658, 1768, 1835, 3710, 3642, 3307, 658, 726, 739, 810, 1688, 2500, 1370, 2022, 1575, 714; São José do Vale do Rio Preto (22º9”3’ S; 42º55”26’ W): IVB 1389, 1394, 1508, 1524, 1528, 1535, 1725, 1808, 1838, 1913, 1923, 1978, 2073, 2123, 2174, 2245, 2261, 2342, 2354, 2371, 2372, 2376, 2377, 2442, 2470, 2471, 2472, 2473, 2474, 2475, 2476, 2478, 2479, 2480, 2481, 2482, 2483, 2484, 2485, 2486, 2487, 2488, 2489, 2502, 244, 2505, 2526, 2536, 2820, 2821, 2822, 2823, 2844, 2897, 2902; Saquarema (22º55”12’ S; 42º30”36’ W): IVB 1709; Teresópolis (22º24”43’ S; 42º57”57’ W): IVB 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 1215, 1672, 1950, 1951, 2146, 2239, 2240, 2241, 3165, 3203, 3204, 3825, 3936, 3958, 4068, 4071, 3411, 3702, 3522. Minas Gerais: Juiz de Fora (21º45”50’ S; 43º21”0’ W): IVB 3328.

Accepted by Rodrigo Gonzalez