Herpetology Notes, volume 14: 77-81 (2021) (published online on 09 January 2021)

First record of leucism in the order : kodaguensis Wilkinson et al., 2007 from the southern Western Ghats, India

Govindappa Venu1,*, Gandlahalli N. Balakrishna1, Robert K. Browne2, Narayanappa G. Raju3, Kulkarni Varadh1, Sompalem Ramakrishna1, and Govindaiah Venkatachalaiah1

Caecilians are an order of eel-like that Ichthyophis kodaguensisis is a striped Western Ghats comprises 214 extant species. They are a small radiation species that was described by Wilkinson et al. (2007) compared to the 7236 species of and toads, and based on six specimens collected at the Venkidds Valley the 757 species of (Frost, 2020). They are Estate (elevation 1143 m), located about 20 km south restricted in distribution to the tropics and sub-tropics, of Mercara, Coorg District, southern Karnataka State, and most are fossorial in moist and humus-rich soil as India, and on a seventh specimen from an uncertain adults. Because of their hidden life they are unfamiliar location. Bhatta et al. (2011) reported two additional to most herpetologists, and their biology is perhaps the specimens of I. kodaguensis from the Western Ghats least known among all amphibians and reptiles (Taylor, region, from Basarekatte, Koppa Taluk, Chikkamagalur 1968; Nussbaum and Wilkinson, 1989; Gower and District, Karnataka State. That report extended the Wilkinson, 2005). range of I. kodaguensis by approximately 125 km to the The Western Ghats of India are part of a global north from the type locality. biodiversity hotspot (Myers et al., 2000). Over the During the late monsoon season in 2004–05, we past decade the targeted sampling of by collected two adult caecilians at the Hegde Coffee herpetologists has resulted in the discovery of many Plantation (12.4730°N, 75.7808°E) that resembled new species and has revealed other significant aspects I. kodaguensis. These were vouchered and of biodiversity and autecology in the Western deposited in the collection of the Department of Ghats (Bhatta et al., 2007, 2011; Wilkinson et al., 2007; Zoology, Bangalore University, Bengaluru, Karnataka, Kotharambath et al., 2012; Sreekumar and Dinesh, India (specimen numbers BUB 1141 and BUB 1179). 2020). The genus Ichthyophis Fitzinger, 1826 includes Hegde Plantation is a 5-ha mixed orchard producing fifty currently recognized species, the greatest number in coffee, areca, bananas, oranges, and cardamom, and any caecilian genus (Frost, 2020). Post-metamorphosis, it lies about 0.5 km north of the I. kodaguensis type Ichthyophis species categorise into two morphs: those locality. Specimen BUB 1141 (Fig. 1A, B) is an adult with a yellow or cream lateral stripe, commonly known male, which was collected from rotting vegetation in as “striped,” and those without a stripe, known as agricultural trenches. Trenching is a general agricultural “unstriped” (Taylor, 1968). practice in the coffee estates of the Western Ghats. The trenches are small depression dug between adjacent coffee plants and used as artificial repositories for weeds and other cultivation refuse that when rotted are used as compost. These trenches are left undisturbed 1 Department of Zoology, Centre for Applied Genetics, Jnana for 4–5 months before the compost is used, and they Bharathi Campus, Bangalore University, Bengaluru, Karnataka, provide good habitats for endogeic herpetofauna, such 560056, India. 2 Sustainability America, La Isla Road, Sarteneja, Corozal as caecilians and shieldtail snakes (family Uropeltidae), District, Belize. who may use them as shelter and to forage for the 3 Department of Biotechnology, Karnataka State Open University, abundant earthworms (Venu and Venkatachalaiah, pers. Mukthagangothri, Mysuru, Karnataka, 570006, India. obs.). Specimen BUB 1179 (Fig. 1C, D) is an adult * Corresponding author. E-mail: [email protected] female, collected from the surroundings of an artificial © 2020 by Notes. Open Access by CC BY-NC-ND 4.0. pond, situated in the lowland area of the estate. Ponds 78 Govindappa Venu et al.

Figure 1. Ichthyophis kodaguensis from Hegde Coffee Plantation, Coorg District, Karnataka State, India. (A) Dorsolateral view of a male (BUB 1141) with a striped body colouration considered normal for the species. (B) The male specimen in ventral view. (C) Leucistic female (BUB 1179) collected from the area surrounding a pond in dorsal view. Note the black eyes. (D) Ventral view of the female. in these estates serve as water storage bodies during the were prepared using the protocol of Venkatachalaiah monsoon seasons and the stored water is pumped out and Venu (2002). Localization of heterochromatin during the drier seasons of the year (Fig. 2). was carried out on meiotic chromosomes following The specimens were transported in plastic bags the protocols of Sumner (1972) and Venu (2014). All to Bangalore University. Following euthanisia in a experiments were conducted in accordance with the 0.5% MS-222 solution, total length of each specimen ethical committee guidelines of the Department of was measured with a string and a ruler, and other Zoology, Bangalore University. measurements were made to the nearest 0.1 mm on Morphometric and meristic data obtained for the formalin-fixed specimens using dial calipers. Numbers two specimens were in agreement with the diagnostic of teeth in both upper and lower jaws were counted using features detailed for I. kodaguensis by Wilkinson et a dissecting microscope. Morphometric and meristic al. (2007). Mitotic and meiotic chromosomal analyses data collected for both BUB 1141 and BUB 1179, with of both specimens revealed a diploid number of 2n = values listed in that order, are as follows: total length 42 chromosomes with fundamental number (FN) 60 289 mm, 324 mm; total number of annuli 302, 321; (Fig. 3A) and n = 21 bivalents (Fig. 3B). Presence of ratio of tentacle-nostril and tentacle-eye distance 1.39, a submetacentric Chromosome Pair 3 in the meiotic 1.56; number of premaxillary + maxillary teeth 39, complement (Fig. 3B) and a prominent heterochromatic 42; number of vomeropalatine teeth 51, 44; number band at the telomeric end on the long arm of of dentary teeth 34, 43; number of inner mandibular Chromosome Pair 1 (Fig. 3C, D) provide a cytogenetic teeth 28, 31. Mitotic chromosomes from liver and identity of both specimens as I. kodaguensis (Venu, meiotic chromosomal stages from testes and ovary 2013). First Record of Leucism in Ichthyophis kodaguensis 79

Figure 2. (A) Map of Karnataka State showing the locality (Hegde Coffee Plantation) of I. kodaguensis (red star). The inset is a map of India, showing Karnataka in red. (B) Habitat of the leucistic female I. kodaguensis. (C) Heaps of dug-out soil surrounding the pond. This is the microhabitat that yielded the first leucistic caecilian.

The colouration of the male resembled that of the with sporadic incidences including (1) variation in Sri commonly seen I. kodaguensis phenotype (Wilkinson Lankan Ichthyophis that had faint or possibly absent et al., 2007). However, the colouration of the female stripes in some I. glutinosus (Linnaeus, 1758), or a more was highly distinct from the male and all other reported or less bicoloured appearance in I. orthoplicatus Taylor, I. kodaguensis in demonstrating leucism, or a partial 1965 (Nussbaum and Gans, 1980); (2) an albino male loss of colouration. The female presented with absence indistinctum (Reinhardt and Lütken, of pigmentation on all body surfaces. The lateral 1862), collected on the edge of the Paraná River near yellow stripe was dull and discontinuous compared Barranqueras City, Chaco Province, Argentina (Cacivio to specimens displaying the colouration usual in this and Cespedez, 1998); (3) notable external differences in species. Intermittent patches of pale chestnut brown colouration with a relatively large genetic differentiation and lilac-grey brown were evident on the dorsum and within I. tricolor Annandale, 1909, collected from a the ventral surface, respectively (Fig. 1C, D). The eyes most northerly population in the Western Ghats (Gower were black (Fig. 1C), indicating that the specimen is not et al., 2002); (4) albinism in a male an albino. mhadeiensis Bhatta et al., 2007, an indotyphlid caecilian Occurrence of intraspecific colour variation is collected in Karnataka, India (Bhatta et al., 2007); (5) widespread among animals (Orteu and Jiggins, 2020). two distinct patterns of ventral colouration in The most common chromatic aberrations, including tentaculata Linnaeus, 1758 from Brazilian Amazonia albinism and leucism, have been documented globally (Maciel and Hoogmoed, 2011); (6) across different classes of vertebrates (e.g., Figon and guarantanus Maciel et al., 2009 that are either entirely Casas, 2018). There are few reports on substantial pale lavender or dark lavender, gradually paler towards intraspecific colour variation or anomalies in caecilians, the head (Maciel and Hoogmoed, 2011); (7) specimens 80 Govindappa Venu et al.

Figure 3. Chromosomal analyses of normal and leucistic Ichthyophis kodaguensis. (A) Somatic metaphase spread prepared from liver cells of the leucistic female (BUB 1179). The arrows denote submetacentric Chromosome Pair 3, the marker chromosomes for I. kodaguensis. (B) Diplotene complement obtained from the testes of the normal individual (BUB 1141). (C) C-banded diplotene and (D) C-banded meiotic metaphase complements from the leucistic female. The arrows correspond to the prominent heterochromatic bands localized in the telomeric regions on the long arms of Chromosome Pair 1. Scale bars = 10 μm. of ron Wilkinson & Gower, 2010 with heavy brown flecking (Nussbaum and Prefender, 1998; yellow spots that are either sparse or closely spaced Stoelting et al., 2014); (11) variation in the colour on the dark brown dorsum (Maciel and Hoogmoed, (pinkish to brownish) of Idiocranium russeli Parker, 2011); (8) brownish or grayish Potomotyphlus kaupii 1936, an indotyphlid and the smallest known caecilian (Berthold, 1859) (Maciel and Hoogmoed, 2011); (9) species from Cameroon (Gower et al., 2015); (12) individuals of a single population of Ichthyophis garoensis Pillai and Ravichandran, 1999 taylori Nussbaum and Hoogmoed, 1979 that are pink with presence or absence of the yellow naris-tentacular or purple or pale lavender, with the rest having a venter aperture line (Kamei and Biju, 2016); and (13) and lateral surfaces slightly lighter than dorsum along chromatic head and body variation in three individuals the entire body (Maciel and Hoogmoed, 2011); (10) of Caecilia volcani Taylor, 1969 from Costa Rica thomense (Bocage, 1873) with no to (Kubicki and Arias, 2017). First Record of Leucism in Ichthyophis kodaguensis 81

To the best of our knowledge, our findings are the first Kamei, R.G., Biju S.D. (2016): On the taxonomic status of record of leucism not only for the genus Ichthyophis Ichthyophis husaini Pillai & Ravichandran, 1999 (Amphibia: but also for the order Gymnophiona. The female did Gymnophiona: ). Zootaxa 4079: 140–150. Kotharambath, R., Wilkinson, M., Oommen, O.V., George, S., not vary cytogenetically compared to either the male Nussbaum, R.A., Gower, D.J. (2012): On the systematics, or to other analysed specimens of I. kodaguensis distribution and conservation status of Ichthyophis (Venu, 2013). The female is the only example of colour longicephalus Pillai, 1986 (Amphibia: Gymnophiona: abnormality found in I. kodaguensis to date, and due to Ichthyophiidae). Journal of Natural History 46: 2935–2959. the limited number of only eleven known specimens we Kubicki, B., Arias, E. 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Accepted by Hinrich Kaiser