New records of pseudocerotid polyclads from Andaman and Nicobar Islands, India

Marine Biodiversity Records, page 1 of 5. # Marine Biological Association of the United Kingdom, 2011 doi:10.1017/s1755267211000819; Vol. 4; e73; 2011 Published online New records of pseudocerotid polyclads from Andaman and Nicobar Islands, India c.r. sreeraj and c. raghunathan Zoological Survey of India, Andaman and Nicobar Regional Centre, National Coral Reef Research Institute, Port Blair 744 102, Andaman and Nicobar Islands Six species of polyclads Pseudobiceros damawan, Pseudobiceros flavocanthus, Pseudoceros bifurcus, Pseudoceros concinnus, Pseudoceros gamblei and Pseudoceros goslineri are newly reported from Andaman and Nicobar Islands of India. Not only do all recorded species constitute first records for the Andaman coast of India, but except for Pseudoceros gamblei, all species are new to Indian waters. Keywords: Polycladida, flatworm, Andaman, Nicobar, Pseudoceros, Pseudobiceros Submitted 7 July 2011; accepted 27 July 2011 INTRODUCTION Marine flatworms are of moderate size, averaging from 2 3 mm in length, with a greatly flattened and more or less oval shape. The phylum Platyhelminthes embraces three classes of worms. Two of these are entirely parasitic; such as Trematoda and Cestoda. The third class, the Turbellaria, is free living and is considered to be the ancestors of the two parasitic classes (Barnes, 1980). The phylogenetic system of the Platyhelminthes proposed by Ehlers (1985) rejects the existence of a monophylum Turbellaria based on the principles and methods of phylogenetic systematics and proposed a clade Rhabditophora for the free living polyclads. Even then the class Turbellaria is used widely for taxonomic purposes of polyclads by most of the workers. Previous to 1984, it was believed that the majority of conspicuous and flamboyantly coloured pseudocerotid flatworms belonged to the genus Pseudoceros Lang, 1884. However, Faubel (1984) clearly separated the genus Pseudobiceros from Pseudoceros on the basis of its double male copulatory system. Pseudobiceros includes the biggest and often most colourful of the polyclad flatworms. These are the only polyclads which actively swim with exaggerated undulations of their ruffled margin (Newman & Cannon, 1997). Laidlaw (1902) reported 13 polyclads of which ten are described up to species level from the Laccadive Islands, which is the first report on marine flatworms from India. Until then, no records have been available for these animals from Indian waters. In fact, little is known about the diversity and biology of free-living flatworms from this region. Although the Polycladida are prominent members of many reef communities, no comprehensive surveys exist for the Andaman waters of India. The majority of species were found under boulders and corals in the reef crest and also in the intertidal region. The relatively large size, ostentatious colour and fluid motion of the ruffled undulating margin of Pseudobiceros makes them the more conspicuous and easily observed of the genera, so they easily get noticed in the intertidal region as well as in the reef. Animals were found generally active during the daytime. MATERIALS AND METHODS The Andaman and Nicobar group of islands consists of 572 islands, islets and rocky outcrops and have an aggregate coastline of 1962 km. The continental shelf area is very limited with an estimated area of 16,000 km 2 and the sea is very deep within a few kilometres from the shore. Survey sites were chosen based on the habitat features and ease of accessibility (Figure 1). The reef areas were surveyed using SCUBA diving. Photographs were taken using a Sony Cybershot TSC900 camera with housing. Specimens were photographed in situ and were hand-collected for further taxonomic studies. In vitro photographs were also taken and the animals were preserved. The morphological features and measurements of the specimen were examined using the stereo-zoom microscope (Leica, DFC 500). The taxonomic identification was based on Newman & Cannon (2003, 2005). No histological confirmation was made since within Pseudocerotidae species have been recognized solely on the basis of their colour patterns (Newman & Cannon, 1994, 1998). Reliability of the use of these colour patterns for species diagnosis has been confirmed with molecular data (Goggin & Newman, 1996; Litvaitis & Newman, 2001). All examined materials are deposited in the National Zoological Collections of the Zoological Survey of India, Andaman and Nicobar Regional Centre. SYSTEMATICS Corresponding author: C.R. Sreeraj Email: crsreeraj@gmail.com Phylum PLATYHELMINTHES Gegenbaur, 1859 Clade RHABDITOPHORA Ehlers, 1986 1

2 c.r. sreeraj and c. raghunathan Fig. 1. Map showing the areas surveyed. Order POLYCLADIDA Lang, 1884 Sub-order COTYLEA Lang, 1884 Super-family PSEUDOCEROTOIDEA Faubel, 1984 Family PSEUDOCEROTIDAE Lang, 1884 Body oval or oblong, surface smooth or papillate, with prominent tentacles derived from margin, sucker central. Pharynx ruffled, anterior clearly ruffled in Pseudoceros and Pseudobiceros and not tubular as in many other families, gut anastomosing. Male copulatory complex (single or double) just behind pharynx, penis usually armed with stylet; female complex single, uterus may be greatly branched. Genus Pseudobiceros Faubel, 1984 Flamboyantly or cryptically coloured. Body soft and delicate, raised medially, elongate oval, tapering posteriorly, margin with numerous deep ruffles. Pseudotentacles well developed. Cerebral eye spot small, horse-shoe shaped. Pharynx is generally relatively smaller, narrower and elongate-oval with 10 to 20 shallow simple pharyngeal folds which do not divide. The symmetrical male pores are found posterior to the end of pharynx, and they are clearly separate. The female pore is clearly found between the male pores (after Newman & Cannon, 1994). Pseudobiceros damawan Newman & Cannon, 1994 One example sexually mature, size: 45 mm, date: 10 September 2010, coll. C.R. Sreeraj, registered no.: ZSI/ ANRC5207. Australia, Indonesia, Micronesia, Marshall Islands, Papua New Guinea and South Africa. Harminder Bay (10832.990 N92832.708 E), depth: intertidal, Little Andaman; Andaman and Nicobar Islands; India. Body with thin black margin and wider orange margin crossed with white bars and tiny black spots (Figure 2A). Ventral side white with an orange margin and a black rim. Marginal band orange interrupted with white spots; narrow black rim. Cerebral eyespot small with 50 eyes. Pseudotentacles square and ruffled. It is of interest to mention that P. damawan was observed to swim upside down in the field. Pseudobiceros flavocanthus Newman & Cannon, 1994 One example sexually mature, size: 75 mm, date: 14 September 2010, coll. C. Raghunathan, registered no.: ZSI/ ANRC5204. One example sexually mature, size: 68 mm, date: 12 September 2010, coll. C. Raghunathan, registered no.: ZSI/ANRC5205. Papua New Guinea.

new records of polyclads from india 3 Fig. 2. (A) Pseudobiceros damawan; (B) Pseucobiceros flavocanthus; (C) Pseudoceros bifurcus; (D) Pseudoceros concinnus; (E) Pseudoceros gamblei; (F) Pseudoceros goslineri. Scale bar: 1 cm. Joginder Nagar (06856.384 N93854.608 E), depth: intertidal, Campbell Bay, Great Nicobar Island; B. Quarry (06859.697 N 93856.760 E), Campbell Bay, Great Nicobar Islands, depth: intertidal; Andaman and Nicobar Islands; India. Background thick black with two equal width marginal bands. Inner band bluish-white; outer band narrow, bright yellow (Figure 2B). Body margins are ruffled. Ventrally grey with same coloured marginal bands. Cerebral eyespot with 30 eyes. Pseudotentacles small, square and slightly ruffled. This species is reported to be rare by Newman & Cannon (2005), but is relatively uncommon in the intertidal regions of South Andaman and Great Nicobar. Genus Pseudoceros Lang, 1884 Combination of smooth dorsal surface, tentacles as folds of the anterior margin, and ruffled pharynx. Pharynx is round and oval with about seven complex pharyngeal lobes, each dividing and extending laterally. The single male pore is found between or just posterior to the last pair of pharyngeal folds and the female pore is clearly separated from the male pore (after Newman & Cannon, 1994). Pseudoceros bifurcus Prudhoe, 1989 Two juvenile examples, size: 8 10 mm, date: 22 August 2010, coll. C.R. Sreeraj, four examples, one juvenile and three sexually mature, size: 8 10 mm, date: 11 September 2010, coll. C.R. Sreeraj. Australia, Indonesia, Japan, Madagascar, Papua New Guinea, Philippines and Thailand. Chidiyatappu (11829 23.21 N92842 31.84 E), South Andaman, depth: 2 m; Patharnallah (10832.935 N 92832.673 E), Little Andaman, depth: 7 m; Andaman and Nicobar Islands; India. Animal blue in colour with a distinctive median stripe down the length of the body that is dark reddish-purple bordered with a white centre ending in a red tip at the front end. Lacks distinct marginal bands (Figure 2C). About 28 eyes in the cerebral eyespot and have few pre-cerebral eyespots. It has a pair of erect pseudotentacles. This species was often observed feeding on colonial ascidians of the genus Eudistoma.

4 c.r. sreeraj and c. raghunathan Pseudoceros concinnus (Collingwood, 1867) One example sexually mature, size: 44 mm, date: 22 August 2010, coll. C.R. Sreeraj, registered no.: ZSI/ANRC5206. One example sexually mature, size: 65 mm, date: 12 September 2010, coll. C. Raghunathan, registered no.: ZSI/ANRC5208. Indonesia, Papua New Guinea and Philippines. Chidiyatappu (11829 23.21 N 92842 31.84 E), South Andaman, depth: 2 m; B. Quarry (06859.697 N93856.760 E), Campbell Bay, Great Nicobar Island, depth: intertidal, Andaman and Nicobar Islands; India. Background cream to fleshy coloured, with an edging of blue all around, composed of small and larger spots running into one another. A similar blue streak runs along the median line from a little posterior to the head to some distance from the posterior (Figure 2D). All the animals recorded had a white mottling pattern over the body; Newman & Cannon (1994) included this species under the category with spots, dots and mottling but did not mention any mottling pattern in this species. The animal recorded was found resting on a yellow-coloured boring sponge. Pseudoceros gamblei Laidlaw, 1902 One example sexually mature, size: 40 mm, date: 16 November 2010, coll. S. Kumaralingam, registered no.: ZSI/ ANRC5203. India (Arabian Sea) and Australia. Kalipur (13813 26.9 N 93802 42.0 E), Diglipur, North Andaman, depth: intertidal, Andaman and Nicobar Islands; India (Bay of Bengal). Background milky-white in colour with bright blue rim (Figure 2E). No spots and blotches on the body. Cerebral eyespot with 30 35 eyes and there is a row of pre-cerebral eyes along the margin of the tentacles. This species was originally described from Minicoi, Laccadive Islands, India. In the original Laidlaw (1902) mentions the colour as milky-white or transparent fleshy colour with purple or dark-blue colour. The animal reported by Litvaitis from Australia (http://www.discoverlife.org/mp/20q?search= Pseudoceros+gamblei) is flesh coloured where as the milkywhite coloured animal is reported for the first time after its original. Pseudoceros goslineri Newman & Cannon, 1994 One example sexually mature, size: 36 mm, date: 13 November 2010, coll. S. Kumaralingam, registered no.: ZSI/ ANRC5202. Australia, Chagos, Indonesia, Maldives, Marshall Islands, Micronesia, Papua New Guinea, Red Sea, Somalia and Tanzania. Plastic Island (13825 32.7 N93804 02.1 E), Diglipur, North Andaman, depth: 6 m, Andaman and Nicobar Islands; India. Background cream mottled with darker-brown (medially), pink and brick-red dots; concentrated brick-red dots medially appearing as irregular elongate blotches. Margin composed of blue and pink irregular dots and spots (Figure 2F). Marginal spots are numerous anteriorly across the pseudotentacles. Ventrally light violet. Cerebral eyespot with 30 eyes. Pseudotentacles simple folds. This species is relatively uncommon in these islands. CONCLUSIONS Pseudocerotids are thought to feed on sessile invertebrates, so the in situ study on the behaviour, feeding and habitat adds further information about them. During this work feeding observations were rare. Due to a focused and long term sampling effort, some of the highest diversity of polyclads (more than 600 species) has been recorded from the Great Barrier Reef and the Indo-Pacific (Newman & Cannon, 2003). In contrast, polyclad diversity in Indian waters has received no attention in the past with the exception of Laidlaw (1902). Recently nine new pseudocerotid polyclads were recorded from Indian waters increasing the total number to 19 species (Sreeraj et al., personal communication). All species except Pseudoceros gamblei reported in this work are new to Indian waters, increasing the total number of species from India to 24. ACKNOWLEDGEMENTS The authors thank the Ministry of Environment and Forests, Government of India for providing the necessary facilities for carrying out the work. Our gratitude is also expressed to The Director, Zoological Survey of India for the support provided. REFERENCES Barnes R.D. (1980) Invertebrate zoology. Philadelphia: Holt-Saunders International Editions, 1089 pp. Collingwood C. (1876) On thirty-one species of marine planarians, collected partly by the late Dr. Kelaart, F.L.S. at Trincomalee and partly

new records of polyclads from india 5 by Dr. Collingwood, F.L.S. in the eastern seas. Transactions of the Linnean Society, London. II. Zoology 1, 83 98. Ehlers U. (1985) Das phylogenetische System der Plathelminthes. Stuttgart: Gustav Fisher Verlag. Faubel A. (1984) The Polycladida, Turbellaria. Proposal and establishment of a new system. Part II. The Cotylea. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 80, 189 259. Goggin G.L. and Newman L.J. (1996) Species discrimination in pseudocerotid flatworms (Platyhelminthes, Polycladida) using ribosomal DNA. Journal of Helminthology 70, 123 126. Laidlaw F.F. (1902) The marine Turbellaria, with an account of the anatomy of some species. Fauna and Geology of the Maldive and Laccadive Archipelagoes 1, 282 312. Litvaitis M.K. and Newman L.J. (2001) A molecular framework for the phylogeny of Pseudocerotidae (Playhelminthes, Polycladida). Hydrobiologia 444, 177 182. Newman L.J. and Cannon L.R.G. (1994) Pseudoceros and Pseudobiceros (Polycladida, Pseudocerotidae) from Eastern Australia and Papua New Guinea. Memoirs of the Queensland Museum 37, 205 266. Newman L.J. and Cannon L.R.G. (1997) Nine new Pseudobiceros (Platyhelminthes, Polycladida, Pseudocerotidae) from the Indo- Pacific. Raffles Bulletin of Zoology 45, 341 368. Newman L.J. and Cannon L.R.G. (1998) New Pseudoceros (Platyhelminthes, Polycladida, Pseudocerotidae) from the Indo- Pacific. Raffles Bulletin of Zoology 46, 293 323. Newman L.J. and Cannon L.R.G. (2003) Marine flatworms: the world of polyclad flatworms. Melbourne, Victoria: CSIRO Publishing, 112 pp. and Newman L.J. and Cannon L.R.G. (2005) Fabulous flatworms: a guide to marine polyclads. Version 1. Canberra and Melbourne, Australia: ABRS and CSIRO Publishing, CD-ROM. Correspondence should be addressed to: C.R. Sreeraj Zoological Survey of India Andaman and Nicobar Regional Centre National Coral Reef Research Institute Port Blair 744 102 Andaman and Nicobar Islands email: crsreeraj@gmail.com