A new colour morph of Calliophis bibroni (Squamata: Elapidae) and evidence for Müllerian mimicry in Tropical Indian coralsnakes

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1 Herpetology Notes, volume 10: (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 Raveendran 1, V. Deepak 2, Eric N. Smith 3 and Utpal Smart 3, * 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 Animal colouration provides many functions; the most important among them is probably predator avoidance and deterrence. Camouflage, or crypsis, blends animals into their environment while deimatism surprises and confuses predators with the display of startling colour patterns. Taxonomically and geographical widespread, aposematism or warning colouration is the display of noxious defense by the means of cautionary colours, to deter predatory attacks. Batesian mimicry occurs when a non-venomous or palatable species mimics the colour and pattern of a dangerous or unpalatable species (Poulton, 1890), whereas Müllerian mimicry is when a venomous, toxic or distasteful species, mimics other organisms with similar disagreeable traits. 1 Centre for Venom Informatics, University of Kerala, Thiruvananthapuram, Kerala, India 2 Centre for Ecological Sciences, Indian Institute of Science, Bengaluru, India 3 Amphibian and Reptile Diversity Research Center and Department of Biology, University of Texas at Arlington, Arlington, Texas, USA * Corresponding author usmart@uta.edu Müllerian co-mimics benefit from sharing the same signal since this reduces the number of individuals that have to be sacrificed per prey species to educate local predators of a given aposematic colouration (Müller, 1879). Furthermore, possibly to balance prey-predator dynamics, some mimics may replicate the colours or patterns of dangerous models which lack bright, conspicuous colours and are cryptic instead (Wüster et al., 2004, McElroy, 2016). The majority of work on Batesian and Müllerian mimicry complexes has been carried out on arthropods such as the toxic Heliconius butterflies (e.g., Baxter et al., 2008, Nadeau et al., 2014, Kronforst and Papa, 2015). While it is true that mimicry is far more taxonomically widespread in invertebrates (Pough, 1988), amongst 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, disruptive colouration and aposematism (Kikuchi et al., 2014). In effect, close to 35% of non-venomous snake species worldwide are thought to be mimics of venomous viperids (vipers and asps) and/or elapids (cobras, kraits, coralsnakes and sea snakes) (Savage and Slowinski 1992, Greene and McDiarmid, 1981). Information on mimetic resemblances in vipers thus

2 210 far has lacked experimental rigor, most likely because vipers lack distinctive patterns that would enable a quantitative approach (Pough 1988). Amongst elapids, the New World coralsnakes (Micrurus and Micruroides) have been amongst the earliest subjects for inquiries on mimicry given their beautiful aposematic colours, usually consisting of red, yellow and black bands (e.g. Cope, 1860). Ever since highlighted by Wallace (1867) as exceptional systems, numerous experimental as well as qualitative studies have dealt with aposematism and mimicry in these coralsnakes (Gehlbach 1972, Smith 1975, 1977, 1980, Greene and McDiarmid 2005, 1981, Brodie 1993, Rabosky et al. 2016). Though fervently contested (e.g. Gadow, 1911; Brattstrom, 1955), in general both empirical and experimental evidence suggests that chromatic patterns of New World coralsnakes are aposematic and that they indeed serve as mimicry models for several harmless or semi-venomous colubrid snakes; prominent examples include some kingsnakes (Lampropeltis) and various false coralsnakes Pliocerus and Erythrolamprus; (Dunn, 1954; Campbell and Lamar, 1989; Brodie and Janzen, 1995). In addition to this, New World coralsnakes are also known to have several plausible instances of Müllerian mimicry within themselves (Greene and McDiarmid, 1981, 2005). Reports of mimicry in Asian elapids, on the other hand, have been largely speculative. Several instances include Batesian mimicry between colubrid mimics and coralsnake models, such as subtropical Asian coralsnakes of the genus Sinomicrurus and their putative snake mimics in the genus Oligodon or Kukri snakes, and long glanded tropical coralsnakes and their possible reed snake mimics in Calamaria (Greene and McDiarmid, 2005). Additionally, the occurrence of metallic dark blue or black bodies with bright red heads and tails on both the Malayan Blue coralsnake Calliophis bivirgata (Boie, 1827), and the sympatric Red-headed Krait Bungarus flaviceps (Reinhardt, 1843) has been cited as an example of Müllerian mimicry in Asian elapids (Slowinski, 1994; Greene and McDiarmid, 2005). Here we report the first observational evidence of a complex chromatic defensive strategy in a tropical Old World elapid, Bibron s coralsnake Calliophis bibroni (Jan, 1858), found in and along the Western Ghats of India. This species is unique in that it undergoes an ontogenetic colour alteration that may correspond to a shift in Müllerian mimicry while simultaneously representing a transition from aposematism to crypsis: juvenile snakes with a aposematic flesh coloured dorsum and black bands possibly mimic the venomous MacClelland s coralsnake Sinomicrurus macclellandii Dileep Kumar Raveendran et al. (Reinhardt, 1844) until they attain an SVL of >400 mm. As adults they transition to one of two phenotypes 1) a dorsal colouration that is a cryptic glossy bistre with bands of the same colour running down the flanks (plain morph), or 2) a dorsal colouration of an iridescent bole brown without any dark bands on the flanks, resembling the venomous Castoe s coralsnake C. castoe (Smith, Ogale, Deepak and Giri, 2012). The ventral pattern retains a vivid flesh coloured red hue throughout this transition in both cases. The complex set of chromatic defensive strategies described in this paper have not yet been reported in any other elapid, not even among the New World pattern-diverse snakes of the genus Micrurus. Methods Species and study area. Calliophis is a genus of Asian coralsnakes comprising ten species, distributed throughout India and Southeast Asia (Castoe et al., 2007; Smith et al., 2008, 2012). Four out of the five species of Calliophis in India have their distributions largely across the Western Ghats, a mountain range that runs almost parallel to the western coast of the Indian peninsula (Smith, 1943; Whitaker et al., 2004). One of these, Bibron s coralsnake or C. bibroni is distributed along a wide altitudinal range ( m) in the evergreen forests in and around the Western Ghats (Deepak et al., 2010). Overall, there is limited information on the distribution, natural history and ecology of this endangered species (Deepak et al., 2010; Srinivasulu, Srinivasulu and Molur 2014). To our knowledge the first photos published of live specimens were by Sharma (1988, as C. macclellandi). Gowri Shankar and Ganesh (2009) reported on two female individuals representing the northernmost localities known for the species and presented notes on ecology and salient features of external morphology of the species. C. bibroni was later re-described by Deepak et al., (2010) who also provided records from south-west peninsular India and presented additional information on the natural history, taxonomy, morphological variation and ontogenetic shift in colour pattern. The authors brought to light the very unique condition, in which sub-adult (<400 mm snout vent length) C. bibroni tend to be aposematic and disruptive overall but as adults these become cryptic above while remaining aposematic and disruptive below. This ontogenetic shift in colour pattern had not been reported in any other species of Old or New World coralsnake. Castoe s coralsnake Calliophis castoe, described by Smith et al., (2012), is found in tropical semi-evergreen

3 A new colour morph of Calliophis bibroni 211 forest and tropical wet evergreen forest on the western coast of India. The altitudinal range for C. castoe is from near sea level (ca m) in Goa and Karnataka to about 715 m in southern Maharashtra (Smith et al., 2012). An individual, initially identified as Calliophis castoe, was collected by the first author, DKR, on October the 12 th at 0840 hours from Valapattanam, Kannur District, Kerala, India. Upon further investigation it was brought to the attention of the authors that, despite an almost exact resemblance in colour pattern to an adult C castoe, the scale counts of the head and caudal area corresponded strongly to meristic patterns typical to C. bibroni. We therefore used molecular data from the collected specimen and compared sequence divergence between it and several individuals of C. bibroni, and one individual of C. castoe, in order to establish its true identity. Molecular data. The molecular work for this study was carried out in three different laboratories in India (viz. the Centre for Venom Informatics, Evolving Phylolab and the Aggarwal Lab). We isolated genomic DNA from six individuals (one Calliophis castoe, four C. bibroni and the individual in question) from liver and/ or muscle tissue (preserved in 90% ethanol) using the Qiagen DNeasy Kit (Qiagen, Valencia, CA, USA). The following section describes the protocol followed by the Centre for Venom Informatics; for protocols followed by the Evolving Phylo-Lab and the Aggarwal lab see Smith (2012) and (Dutta et al., 2004) respectively. We amplified the mitochondrial gene Cytb via PCR using the primers GLUDGE and ATRCB3 and according to thermocycler protocol used by Castoe et al., (2007). We used Dream Taq Green PCR Master Mix, 2X (Thermo Scientific, Massachusetts, USA) for all amplifications reactions. We performed thermal cycling on a Veriti 96-Well Thermal cycler (Applied Biosystems, Singapore). Post amplification, we resolved the PCR products on 1.5% agarose gel and eluted using GeneJET Gel extraction Kit (Thermo Scientific, Massachusetts, USA). We sequenced the amplified inner PCR products on an ABI3730xL DNA analyzer (Applied Biosystems, California, USA), using the ABI PRISM BigDye Terminator Cycle sequencing Kit (Perkin-Elmer Corp., USA), following the manufacturer s instructions. We cleaned the raw sequences and assembled consensus sequences for the gene fragments using the program Sequencher 4.8 (Gene Codes, Ann Arbor, Michigan, USA). We built the alignment of the resultant consensus sequences using MEGA v5.2.1 (Tamura et al., 2011). We edited sequences by eye for accuracy and also translated them to amino acid sequences, to verify the absence of stop codons. We detected no internal stop codons and we deposited the new sequences in GenBank (Table 1). We calculated uncorrected pairwise p-distances in MEGA v5.2.1 (Tamura et al., 2011). Coloration and meristic data. We took measurements of external morphology from digital images using the software ImageJ (Rasband, 2004). We took photographs with high-resolution digital cameras (> 8 megapixels), placing the subject at right angles with respect to the lens of the camera. We measured snout-vent length (SVL), tail length, and total length (TL) to the nearest mm using ImageJ or a measuring ruler or tape. We followed standard colubroid terminology for scales (e.g. Smith and Campbell, 1994); for counting ventrals we followed the method of Dowling (1951). We excluded the terminal scute (tip) from the number of subcaudals. We counted the numbers of dorsal scale rows at one head length behind the head, at midbody and at one head length before the vent. We determined sex by observing presence or absence of hemipenes, through dissection Table 1. List of Calliophis specimens used in the molecular analysis, with collection locality, sample number, and GenBank accession number. Species Sample # Locality Latitude Longitude GenBank Accession # C. bibroni M816 Bethary, Waynad, Kerala 11 41' " N 76 7' 55.2" E KX C. bibroni M817 Palode, Trivandrum, Kerala 8 31' 26.76" N 76 56' " E KX C. sp. M819 Valapattanam, Kannur, Kerala 11 54' 0" N 75 22' 12" E KX C. bibroni M731 Topslip, Coimbatore, Tamil Nadu 10 27' " N 76 50' " E KX C. bibroni M733 Topslip, Coimbatore, Tamil Nadu 10 16' " N 76 30' " E KX C. castoe M706 Ambe Ghat, South Goa, Goa 15 3' 50.4" N 74 9' " E KX573696

4 212 of the base of the tail. The colour descriptions of the referred specimen in life are based on electronic images. We deposited these images at the Digital Collection of the UTA Amphibian and Reptile Diversity Research Center (UTADC , ). Results Molecular data. The Calliophis species from Kannur, is genetically undifferentiated from the C. bibroni individuals from Kerala with a maximum p- distance of 0.6% and a minimum p-distance of 0 % (Table 2). The C. castoe specimen is 22.0% different from the Calliophis species from Kannur, which it shares near identical dorsal colouration with. Meristic data and colouration. The specimen from Kannur is an adult female with SVL -measuring 587 mm (656 mm total length). Despite of superficial resemblance, the individual differs from Calliophis castoe (characters in parenthesis) in the following characteristics: no preocular (one preocular); one postocular (two postoculars); ventrals ( ); subcaudals - 39 (45-53); single anal plate (divided anal plate) (Figure. 1). All of the meristic data mentioned fall close to or within the morphological variation reported in C. bibroni (Deepak et al., 2010). The Kannur specimen has no temporal extensions of the head cap (temporal extension of head cap present); nuchal/parietal band yellow (orange); midvertebral sepia stripe occupying vertebral and paravertebral rows (no stripe); ventral surface of tail as well as posterior body black/sepia, midventral colour orange (orange with no black/sepia markings); single anal plate almost completely sepia/black, except for orange posterior border (single anal plate, white with only slightly orange lateral edges) (Figure.2 C-F). Discussion Dileep Kumar Raveendran et al. The chromatic resemblance between the new colour morph of Calliophis bibroni and C. castoe is remarkable and since the two species most likely have overlapping ranges (Figure. 3), it is not hard to postulate that they are Müllerian co-mimics. Our proposal of sub-adult C. bibroni being co-mimics of Sinomicrurus macclellandii is primarily based on the fact that the latter is the only other venomous South Asian snake to display a red dorsum with black bars (Whitaker et al., 2004; Deepak et al., 2010). It is to be noted, that the range of the two species does not overlap and they are separated by over 1000 km, with C. bibroni being restricted to the west coast of south India, while S. macclellandi is only found in the forests of north and northeastern India (Whitaker et al., 2004). However, it has already been recognized that mimicry need not be restricted to sympatric species (Pfennig and Mullen, 2010; Pfennig et al., 2015); several New World coralsnake mimics have ranges that exceed that of their models (Endler, 1981). The two assumptions then, implicit to our reasoning are: 1) banded patterns (as seen in Sinomicrurus macclellandi) function as aposematic signals (Brodie, 1993; Mochida et al., 2015) ; 2) avifauna are significant predators of Old World coralsnakes, as is the case of their New World counterparts (Pough, 1988). If these assumptions hold true then it entirely plausible that a wide-ranging or migratory avian predator would generalize its avoidance of an unprofitable prey with a characteristic bright banded pattern (Greene and McDiarmid, 1981). Indeed, several wide-ranging Indian raptors are known to be forest dwellers, specializing on snakes and other reptiles: the Crested Serpent Eagle Spilornis cheela (Latham, 1790) and the Changeable Hawk Eagle Spizaetus cirrhatus (Gmelin, 1788) both reside in tropical evergreen forests across India, and are known to actively prey on snakes; other widespread Table 2. Uncorrected pairwise genetic distances (p-distances) of Cytb sequences from the specimens used in this study. M816 C. bibroni Wynad, Kerala M817 C. bibroni Trivandrum, Kerala M819 C. sp. Kannur, Kerala M731 C. bibroni Tamil Nadu M733 C. bibroni Tamil Nadu M816 C. bibroni Wynad, Kerala M817 C. bibroni Trivandrum, Kerala M819 C. sp. Kannur, Kerala M731 C. bibroni Tamil Nadu M733 C. bibroni Tamil Nadu M706 C. castoe Goa

5 A new colour morph of Calliophis bibroni 213 Figure 1. Color patterns in Bibron s coralsnake, Calliophis bibroni, and comparison to suspected Müllerian co-mimics. Dorsum (A) and venter (B) of adult male C. bibroni, adult with cryptic dorsal colour and aposematic venter. Dorsum (C) and tail ventral surface of adult C. bibroni (D) resembling C. castoe (F). Dorsum of juvenile C. bibroni (E), resembling S. macclellandi (G). Individuals of C. bibroni presented in A-B, C-D, and E correspond to M816, M819 and M817, respectively. Photos A E by Dileep Kumar, F by Hemant Ogale, and G by Ishan Agarwal.

6 214 Dileep Kumar Raveendran et al. Figure 2. Lateral and dorsal head views of selected coralsnakes of the Western Ghats showing convergent head colour patterns and scalation, adult Calliophis bibroni with cryptic dorsal colour (A and B), adult C. bibroni with Mullerian mimicry with C. castoe (C and D), and adult C. castoe (E and F). raptors such as the Common Buzzard Buteo buteo (Linnaeus, 1758), the Oriental Honey Buzzard Pernis ptilorhycus (Temminck, 1821) and the Booted Eagle Hieraaetus pennatus (Gmelin, 1788) also frequent forests and regularly feed on reptiles (Naoroji and Schmitt 2007). DV has found a dead Calliophis bibroni with perforations made by birds on two occasions (Deepak, 2015). There is also a confirmed report of a Brown Fish Owl Bubo zeylonensis (Gmelin, 1788) feeding on a Striped coralsnake C. nigrescens from Karnataka, India ( Given that Calliophis bibroni are known to attain a total length of 880 mm while Sinomicrurus macclellandi in India barely get over 800 mm long (Whitaker et al., 2004; Deepak et al., 2010), it is possible that the former would benefit by changing their mimicry strategy if they are too large to effectively mimic S. macclellandi as adults. Old World coralsnakes are known to flip over and expose their bright bellies when threatened.

7 A new colour morph of Calliophis bibroni 215 Figure 3. Map showing the localities of Calliophis castoe and C. bibroni in India, including those used in this study (modified from Deepak et al., 2010). Retaining an aposematic venter could actually provide the snake a last resort opportunity to fend off any predator that was not fooled by crypsis and was naïve enough to proceed attacking after having located the snake. Conceding that we have no experimental backing to our claims of mimicry between the allopatric C. bibroni and S. macclellandi, there is no means for us to theoretically dismiss alternatives that could serve as drivers of convergent evolution in colouration. Flickerfusion (Pough, 1976), background matching, or simply the innate fear of aposematic phenotypes (Smith, 1975, 1977), are all hypothesized to drive the independent evolution of parallel external appearances in snakes. Nevertheless, the complex combination of aposematism and mimicry in Calliophis bibroni reported here is unique in many respects. Below we discuss what sets it apart from chromatic strategies seen in other relevant snake mimicry systems of the New World. - Even though less drastic than that of Calliophis bibroni (Deepak et al., 2010), an ontogenetic transition from aposematism to crypsis has also been reported in New World coralsnakes; for example, in Costa Rica, Allen s coralsnake Micrurus alleni (Schmidt, 1936) is known to undergo an ontogenetic shift wherein its vivid pattern of red, yellow and black rings change into uniform black. Remarkably, the sympatric Milksnake Lampropeltis triangulum (Lacépède, 1789) known to be a Batesian mimic of the M. alleni, displays a similar ontogenetic shift (Savage and Vial- Kearney, 1974; Greene and McDiarmid, 2005). There is no comparable instance of ontogenetic transition involving Müllerian co-mimics in New World elapids. - Some New World snakes are also known to combine features of two or more models, as seen with the Variegated False coralsnake Pliocerus elapoides (Cope, 1860) in southern Mexico and northern Guatemala, which combines the colour sequence

8 216 of two sympatric coralsnake species (Pough, 1988). However, this dual mimicry is displayed simultaneously and is not sequentially associated with ontogeny as seen with C. bibroni. - While apostasy (frequency-dependent selection of rare morphs[clark, 1969]) is expected to maintain polymorphism in Batesian mimics, Müllerian comimics typically tend to be monomorphic (Endler and Greenwood, 1988; Joron and Mallet, 1998; Mallet and Joron, 1999). Calliophis bibroni is unique in that it not only displays polymorphism (i.e. the plain morph and the C. castoe morph) while being a Müllerian comimic, but that the two colour morphs are sympatric (Figure. 3). And even though conspicuous exceptions to this rule are frequently seen in several species of butterflies (Mallet and Joron, 1999), polymorphism in Müllerian mimics within New World coralsnakes is yet to be reported. In summary, the new colour morph of Calliophis bibroni described here provides a unique glimpse into the complex eco-evolutionary interactions occurring between an enigmatic group of tropical venomous snakes and their environment, which have not been reported before in any coralsnakes. The hypotheses we discuss above are testable with rigorous field experiments, involving clay or plasticine models. We hope that the evidence provided herein will motivate ecologists to initiate pioneering experimental studies, drawing inspiration from the elegant work on Neotropical snake fauna, exploring mimicry, crypsis and aposematism in Old World coralsnakes. Acknowledgments. We would like to thank Dr. Praveen K. Karanth and his lab (Center for Ecological Sciences, Indian Institute of Science, Bengaluru) and Dr. Ramesh K Aggarwal and his lab (Center for Cellular and Molecular Biology, Hyderabad) for sequencing the Calliophis castoe and C. bibroni individuals respectively. 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