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A New Colour Morph of Calliophis Bibroni (Squamata: Elapidae) and Evidence for Müllerian Mimicry in Tropical Indian Coralsnakes

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A New Colour Morph of Calliophis Bibroni (Squamata: Elapidae) and Evidence for Müllerian Mimicry in Tropical Indian Coralsnakes Herpetology Notes, volume 10: 209-217 (2017) (published online on 25 April 2017) A new colour morph of Calliophis bibroni (Squamata: Elapidae) and evidence for Müllerian mimicry in Tropical Indian coralsnakes Dileep Kumar Raveendran1, V. Deepak2, Eric N. Smith3 and Utpal Smart3,* Abstract. Meristic and molecular data provide evidence for an exceptional multi-chromatic defensive strategy in an Indian coralsnake, Calliophis bibroni from the state of Kerala. We propose a mimicry hypothesis involving a combination of an ontogenetic colour shift at maturity, from initial Müllerian mimicry with a subtropical Indian coralsnake Sinomicrurus macclellandii, to one of two very different adult dorsal colours: 1) an aposematic pattern resembling that of the sympatric tropical Indian coralsnake Calliophis castoe or 2) a cryptic dark brown colouration. To this end, we succinctly juxtapose the rich body of work on mimicry in New World elapids to that of their Old World counterparts in an attempt to address the exciting yet unexplored prospect of investigating mimicry, crypsis and aposematism in Old World coralsnakes. Key Words. Aposematism, crypsis, Indian coralsnakes, genetic distance, meristics, mimicry Introduction Müllerian co-mimics benefit from sharing the same signal since this reduces the number of individuals that Animal colouration provides many functions; the most have to be sacrificed per prey species to educate local important among them is probably predator avoidance predators of a given aposematic colouration (Müller, and deterrence. Camouflage, or crypsis, blends animals 1879). Furthermore, possibly to balance prey-predator into their environment while deimatism surprises and dynamics, some mimics may replicate the colours confuses predators with the display of startling colour or patterns of dangerous models which lack bright, patterns. Taxonomically and geographical widespread, conspicuous colours and are cryptic instead (Wüster et aposematism or warning colouration is the display of al., 2004, McElroy, 2016). noxious defense by the means of cautionary colours, The majority of work on Batesian and Müllerian to deter predatory attacks. Batesian mimicry occurs mimicry complexes has been carried out on arthropods when a non-venomous or palatable species mimics such as the toxic Heliconius butterflies (e.g., Baxter et the colour and pattern of a dangerous or unpalatable al., 2008, Nadeau et al., 2014, Kronforst and Papa, 2015). species (Poulton, 1890), whereas Müllerian mimicry While it is true that mimicry is far more taxonomically is when a venomous, toxic or distasteful species, widespread in invertebrates (Pough, 1988), amongst mimics other organisms with similar disagreeable traits. vertebrates (alongside Poison frogs of the family Dendrobatidae [Yeager et al. 2012]) venomous snakes have great potential to serve as model organism since many species are known to show striking crypsis, 1 Centre for Venom Informatics, University of Kerala, disruptive colouration and aposematism (Kikuchi et Thiruvananthapuram, Kerala, India al., 2014). In effect, close to 35% of non-venomous 2 Centre for Ecological Sciences, Indian Institute of Science, snake species worldwide are thought to be mimics of Bengaluru, India venomous viperids (vipers and asps) and/or elapids 3 Amphibian and Reptile Diversity Research Center and Department of Biology, University of Texas at Arlington, (cobras, kraits, coralsnakes and sea snakes) (Savage Arlington, Texas, USA and Slowinski 1992, Greene and McDiarmid, 1981). * Corresponding author e-mail: [email protected] Information on mimetic resemblances in vipers thus 210 Dileep Kumar Raveendran et al. far has lacked experimental rigor, most likely because (Reinhardt, 1844) until they attain an SVL of >400 mm. vipers lack distinctive patterns that would enable a As adults they transition to one of two phenotypes 1) quantitative approach (Pough 1988). Amongst elapids, a dorsal colouration that is a cryptic glossy bistre with the New World coralsnakes (Micrurus and Micruroides) bands of the same colour running down the flanks (plain have been amongst the earliest subjects for inquiries morph), or 2) a dorsal colouration of an iridescent bole on mimicry given their beautiful aposematic colours, brown without any dark bands on the flanks, resembling usually consisting of red, yellow and black bands (e.g. the venomous Castoe’s coralsnake C. castoe (Smith, Cope, 1860). Ever since highlighted by Wallace (1867) Ogale, Deepak and Giri, 2012). The ventral pattern as exceptional systems, numerous experimental as well retains a vivid flesh coloured red hue throughout this as qualitative studies have dealt with aposematism and transition in both cases. The complex set of chromatic mimicry in these coralsnakes (Gehlbach 1972, Smith defensive strategies described in this paper have not 1975, 1977, 1980, Greene and McDiarmid 2005, 1981, yet been reported in any other elapid, not even among Brodie 1993, Rabosky et al. 2016). Though fervently the New World pattern-diverse snakes of the genus contested (e.g. Gadow, 1911; Brattstrom, 1955), in Micrurus. general both empirical and experimental evidence suggests that chromatic patterns of New World Methods coralsnakes are aposematic and that they indeed serve as mimicry models for several harmless or semi-venomous Species and study area.— Calliophis is a genus of colubrid snakes; prominent examples include some Asian coralsnakes comprising ten species, distributed kingsnakes (Lampropeltis) and various false coralsnakes throughout India and Southeast Asia (Castoe et al., 2007; Pliocerus and Erythrolamprus; (Dunn, 1954; Campbell Smith et al., 2008, 2012). Four out of the five species of and Lamar, 1989; Brodie and Janzen, 1995). In addition Calliophis in India have their distributions largely across to this, New World coralsnakes are also known to have the Western Ghats, a mountain range that runs almost several plausible instances of Müllerian mimicry within parallel to the western coast of the Indian peninsula themselves (Greene and McDiarmid, 1981, 2005). (Smith, 1943; Whitaker et al., 2004). One of these, Reports of mimicry in Asian elapids, on the other Bibron’s coralsnake or C. bibroni is distributed along hand, have been largely speculative. Several instances a wide altitudinal range (0–1220 m) in the evergreen include Batesian mimicry between colubrid mimics and forests in and around the Western Ghats (Deepak et coralsnake models, such as subtropical Asian coralsnakes al., 2010). Overall, there is limited information on of the genus Sinomicrurus and their putative snake the distribution, natural history and ecology of this mimics in the genus Oligodon or Kukri snakes, and long endangered species (Deepak et al., 2010; Srinivasulu, glanded tropical coralsnakes and their possible reed Srinivasulu and Molur 2014). To our knowledge the snake mimics in Calamaria (Greene and McDiarmid, first photos published of live specimens were by Sharma 2005). Additionally, the occurrence of metallic dark (1988, as C. macclellandi). Gowri Shankar and Ganesh blue or black bodies with bright red heads and tails on (2009) reported on two female individuals representing both the Malayan Blue coralsnake Calliophis bivirgata the northernmost localities known for the species and (Boie, 1827), and the sympatric Red-headed Krait presented notes on ecology and salient features of Bungarus flaviceps (Reinhardt, 1843) has been cited external morphology of the species. C. bibroni was later as an example of Müllerian mimicry in Asian elapids re-described by Deepak et al., (2010) who also provided (Slowinski, 1994; Greene and McDiarmid, 2005). records from south-west peninsular India and presented Here we report the first observational evidence of a additional information on the natural history, taxonomy, complex chromatic defensive strategy in a tropical Old morphological variation and ontogenetic shift in colour World elapid, Bibron’s coralsnake Calliophis bibroni pattern. The authors brought to light the very unique (Jan, 1858), found in and along the Western Ghats of condition, in which sub-adult (<400 mm snout vent India. This species is unique in that it undergoes an length) C. bibroni tend to be aposematic and disruptive ontogenetic colour alteration that may correspond to overall but as adults these become cryptic above while a shift in Müllerian mimicry while simultaneously remaining aposematic and disruptive below. This representing a transition from aposematism to crypsis: ontogenetic shift in colour pattern had not been reported juvenile snakes with a aposematic flesh coloured in any other species of Old or New World coralsnake. dorsum and black bands possibly mimic the venomous Castoe’s coralsnake Calliophis castoe, described by MacClelland’s coralsnake Sinomicrurus macclellandii Smith et al., (2012), is found in tropical semi-evergreen A new colour morph of Calliophis bibroni 211 forest and tropical wet evergreen forest on the western 96-Well Thermal cycler (Applied Biosystems, coast of India. The altitudinal range for C. castoe is Singapore). Post amplification, we resolved the PCR from near sea level (ca. 10–15 m) in Goa and Karnataka products on 1.5% agarose gel and eluted using GeneJET to about 715 m in southern Maharashtra (Smith et al., Gel extraction Kit (Thermo Scientific, Massachusetts, 2012). USA). We sequenced the amplified inner PCR products An individual, initially identified as Calliophis castoe, on an ABI3730xL DNA analyzer (Applied Biosystems, was collected by the first author,
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