SCIENTIFIC CORRESPONDENCE

Non-indigenous sea slug adspersa in the southeast coast of the Arabian Sea, India

Nudibranchs are gastropod molluscs brackish water bodies, lagoons and har- tion and subsequently identified. During belonging to suborder Opisthobranchia. bours of temperate and tropical regions3. one such investigation, T. adspersa was They are easily identified based on their This was first described by Nord- identified on the basis of 17 specimens shell-less bodies and a pair of rhinopho- mann4 in 1844, based on specimens col- collected from the bar mouth of Cochin res (tentacles) on the dorsal side of the lected from the Black Sea, Ukraine. harbour (958N, 7615E) at 5 m depth head. These organisms are stunningly ICAR-Central Marine Fisheries Re- (Figure 1) on 13 September 2013. This colourful, hence are often called ‘butter- search Institute (CMFRI), Kochi has is the first record from Indian waters. flies of the ocean’. About 3000 species been monitoring the benthos in Cochin The collection consisted of juveniles of Nudibranchs are known globally1, and harbour and the adjacent coastal region (2.96 mm) and adults (up to 7.80 mm) 311 species have been reported from from 2010. In the present study, the ben- (Figure 2). Table 1 provides the mor- India2. Tenellia adspersa is a tiny nudi- thos samples were collected using a phometric details. The benthos sample branch, commonly known as lagoon sea sampler (Van Veen Grab) with an area of also contained amphipods, decapod crus- slug or miniature aeolis. It is a eury- 0.28 m2. The samples (surface layer taceans, polychaetes (Nereis spp., Malm- haline aeolid sea slug inhabiting shallow sediments) were sieved using 2 mm and grenia spp.) and Oligochaetes. Table 2 areas from 1 to 34 m depth, and with 500 m sieves. The benthos retained in provides the environmental parameters salinity ranging from 3‰ to 50‰ (ref. the sieves was preserved in 4% buffered recorded during the sampling period. The 3). Its preferred habitats are estuaries, formalin stained with Rose Bengal solu- specimens have been deposited in the Marine Biodiversity Museum of CMFRI (accession no. DB.1.3.1). It has been re- ported that T. adspersa grows up to 8 mm length and attains maturity at 3.6 mm (ref. 3). Its known longevity is less than one year and it reaches sexually maturity in 20 days (ref. 5). It spawns 3–5 times, with each spawning period lasting for 3–5 days, and lays 25–50 eggs per spawn5. Taxonomical studies on the T. ads- persa specimens were carried out follow- ing Alder and Hancock6, and Rogin- skaya3. This species is known to be pale brown-coloured with tiny black spots.

Table 1. Total length and body width of Tenellia adspersa specimens

Total length (mm) Body width (mm)

2.96 1.16 3.41 1.99 3.55 1.35 Figure 1. Map showing the sampling point (station-1) at Cochin estuary, Kerala, India. 4.13 1.85

4.30 2.34 4.37 1.55 4.44 2.18 5.13 2.07 5.37 1.32 5.46 1.96 5.63 2.19 5.90 2.57 6.37 2.74 6.76 2.02 6.90 2.05 7.07 2.39

7.80 2.01 Figure 2. Morphometric characteristics of miniature sea-slug T. adspersa.

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However, in the present study the colour and plants (phytoplankton) are trans- a major international transhipment ter- of the fresh specimens could not be ob- ported along with the ballast water to minal and latest statistics has revealed served, and identification was based on new biogeographical areas, where they that it handled 1430 vessels during the preserved specimens. It is easily distin- become marine pests. Similarly, benthos year 2013–14 and 1476 vessels in 2014– guished by its minute slender body taper- may unintentionally enter the ballast 15 (ref. 15). The intensive international ing behind and two short, cylindrical tank. Cochin backwater is a tropical shipping activity could have triggered rhinopores/tentacles or veils on the sides estuary along the southwest coast of the invasion of T. adspersa. Ship hulls of the head, which serve as chemosen- India, in which the Cochin harbour is contain several fouling organisms, includ- sory organs. The tentacle-like dorsal out- situated. The bar mouth of the Cochin ing hydroids. The adult T. adspersa might growths called papillae/cerata form 2–6 estuary is the main entrance of the have got attached to the hydroids on the groups of 1–3 simple cerata each. Cochin harbour and is permanently con- surface of the ship hull and then trans- T. adspersa is closely associated with nected to the Arabian Sea. Cochin port is ported to Cochin. Another possibility is hydroids and mainly feeds on them. It mostly prefers to feed on hydroids, Garveia franciscana, Cordylophora cas- Table 2. Hydrological characteristics observed at the sampling site pia, Gonothyraea loveni and Ectopleura Observed parameters Surface Bottom 3,7 crocea . Among these, Garveia francis- cana commonly called rope grass hy- Water temperature (C) 29 26.2 droid, has been reported from the Cochin pH 6.78 7.47 backwaters. Leloup8 described Bimeria Salinity (PSU) 4.62 31.9 franciscana (a junior synonym of Garveia Chlorophyll a (mg m–3) 1.364 0.929 franciscana) for the first time from the Chlorophyll b (mg m–3) 0.031 0.000 west coast of India. Subsequently, Chlorophyll c (mg m–3) 0.213 0.000 Mammen9 reported it in large numbers Dissolved oxygen (mg l–1) 5.82 3.28 –1 from Cochin, wherein its colonies gener- SiO3-Si (mg l ) 2.74 0.05 –1 ally grew up to 15 cm (maximum of PO4 -P (mg l ) 0.040 0.045 –1 30 cm) and the distance between the NO3-N (mg l ) 0.002 0.000 –1 branches was 3–10 mm. The rope grass NO2-N (mg l ) 0.003 0.007 –1 hydroid had been surviving in fresh, Total NH3-N (mg l ) 0.013 0.252 brackish and marine water habitats and GPP (mg C L–1 h–1) 0.038 – tolerated salinities varying from 1‰ to NPP (mg C L–1 h–1) 0.059 – 35‰ (ref. 10). It is one of the important 11 GPP, Gross Primary Productivity; NPP, Net Primary Productivity. prey items for T. adspersa ; one T. ads- persa can devour 100 individuals of 3 Garveia species per day . Garveia fran- Table 3. First records of Tenellia adspersa reported in different countries ciscana provides shelter and habitats to many crustaceans like amphipods, Tenellia adspersa/synonym Year Country name Reference shrimps, crabs and juvenile fishes12, and edwardsii 1846 Ukraine 4 is probably helpful in sustaining good Tergipes lacinulatus 1849 Germany 18 fishery. The major impacts of invasive pallida 1881 Finland 19 species are the alteration of nutrient cy- Embletonia pallida 1907 Russia 20 cling, food webs, community structure Embletonia pallida 1907 Sweden 20 and shifting of native species13,14. Inva- Embletonia pallida 1910 England 21 sive alien species are the major threats to Embletonia pallida 1926 France 22 biodiversity. Tenellia pallida 1944 Denmark 23 To the best of our knowledge, there Embletonia mediterranea 1953 Brazil 24 are no earlier records of this species from Tenellia ventilabrum 1953 Atlantic Ocean 25 the Indian Ocean rim countries. The Embletonia pallida 1955 Mediterranean 26 natural geographical range of the species Embletonia pallida 1960 Brazil 27 is from northeastern Atlantic Ocean to Tenellia pallida 1963 Japan 28 the Caspian Sea3,7. More recently, it has Tenellia adpsersa 1970 Russia 3 been introduced into New Zealand (Ta- Tenellia adspersa 1972 East coast of USA 29 ble 3). It has also been introduced to the Tenellia adspersa 1979 West coast of USA 30 several Pacific Ocean countries through Tenellia pallida 1979 South Carolina, USA 31 ballast water of ships3. Ballast water is Tenellia adspersa 1990 Russia 32 stored in ballast tanks located at the bot- Tenellia adspersa 1996 Australia 33 tom chamber of empty cargo ships to Tenellia adspersa 2001 New Zealand 34 maintain buoyancy. When these ships en- Tenellia adspersa 2005 The Netherlands 35 ter the next port of call to load cargo, the Tenellia adspersa 2006 Hong Kong 36 ballast water is discharged. Microscopic Tenellia adspersa 2013 Norway 37 marine (zooplankton, nekton)

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26. Marcus, E. R., Kiel. Meeresforsch., 1955, 11, 2. 27. Marcus, E. R., Bull. Mar. Sci. Gulf Caribb., 1960, 10, 2. 28. Baba, K. and Hamatani, I., Publ. Seto Mar. Biol. Lab., 1963, 11, 337–338. 29. Marcus, E., Chesapeake Sci., 1972, 13, 300–317. 30. Carlton, J. T., History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific Coast of North America, Ph D disserta- tion, University of California, Davis, USA, 1979, p. 904. 31. Eyster, L. S., Mar. Biol., 1979, 51, 133– 140.

32. Antsulevich, A. E. and Starobogatov, Y. Figure 3. Juvenile and adult specimens of T. adspersa. I., Zool. Zh., 1990, 69, 138–140. 33. Hewitt, C. L. and Martin, R. B., CRIMP Technical Report No. 4, CSIRO Marine the transport of egg masses of T. ads- 10. Crowell, S. and Darnell, R. M., Ecology, Research, Hobart, Australia, 1996. 1955, 36, 516–518. persa discharged through ballast water, 34. McClary, D., Project Report (ZBS 11. Abbe, G. R., In Ecological Studies in which might have developed into adults. 2000/03), Kingett Mitchell & Associates the Middle Reach of Chesapeake Bay – This is corroborated by the occurrence of Ltd, Ministry of Fisheries Research, New Calvert Cliffs (eds Heck, K. L.), juveniles as well as adult stages (Figure Zealand, 2001, p. 29; www.biosecu- Springer-Verlag, Berlin, 1987, pp. 82– 3). During the monsoon months (June– rity.govt.nz/files/pests/salt-freshwater/ 91. kma-hull-clea-ning-guidelines.pdf September), the Cochin estuary salinity 12. Cory, R. L., Chesapeake Sci., 1967, 8, 16 35. Wolff, W. J., Zool. Verh., 2005, 79, 1– gradients are very low , which might 71–89. 116. have favoured T. adspersa development 13. Molnar, J. L., Gamboa, R. L., Revenga, 36. WWFHK, An extension to the existing and survival. India is one of the signato- C. and Spalding, M. D., Front. Ecol. En- boardwalk and new mudflat bird-watching ries to the Convention on Biological Di- viron., 2008, 6, 485–492. hide at Mai Po Nature Reserve for educa- 17 14. Thomsen, M. S., Wernberg, T., Olden, J. versity (CBD) . Article 8(h) of the CBD tion and conservation purposes. WWF D., Byers, J. E., Bruno, J. F., Silliman, B. states that, ‘Each contracting Party shall, Hong Kong Project Report, 2006, p. 81. R. and Schiel, D. R., NeoBiota, 2014, 22, as far as possible and as appropriate, 37. Evertsen, J. and Bakken, T., Fauna 1–22. prevent the introduction of, control or Norv., 2013, 32, 45–52. 15. CPT, Cochin Port Trust statistics, 2015; eradicate those alien species which http://cochinport.gov.in/writereaddata/ threaten ecosystems, habitats or species’. pdf/1432800794-10%20years%20details. ACKNOWLEDGEMENTS. We thank David Therefore, continuous monitoring of har- pdf W. Behrens (California Academy of Sciences, bours/ports is essential to prevent the in- 16. Qasim, S. Z., In Indian Estuaries, Allied USA) for confirming the identification of the vasion of non-indigenous species. Publishers Pvt Ltd, Mumbai, 2003, pp. species. We also thank the Director, CMFRI, 305–382. ISBN: 81-7764-369-X. Kochi for providing the necessary facilities 1. Willan, R. C. and Coleman, N., Nudi- 17. CBD, Global Biodiversity Outlook 2, Se- and crew members of F.V. Silver Pompano branchs of Australasia, Australasian cretariat of the Convention on Biological for their support. Marine Photographic Index, Caringbah, Diversity, Montreal, 2006, pp. 81 + vii; Sydney, 1984, p. 56. https://www.cbd.int/doc/gbo/gbo2/cbd- 2. Bhave, V. and Apte, D., In Ecology and gbo2-en.pdf Received 17 November 2016; revised ac- Conservation of Tropical Marine Faunal 18. Schultze, M. S., Arch. Naturgesch., cepted 19 April 2017 Communities, Springer-Verlag, Berlin, 1849, 15, 268–279. 2013, vol. 5, pp. 63–79. 19. Palmén, J. A., Medd. Soc. Fauna Flora 3. Roginskaya, I. S., Malacol. Rev., 1970, Fenn., 1881, 7, 129–131. A. M. DHANYA 3, 167–174. 20. Odhner, N. H., K. Sven. Vetenskapskad. R. JEYABASKARAN* 4. Nordmann, A. De, Ann. Sci. Nat., 3me Handl., 1907, 41, 1–118. D. PREMA Ser., 1846, 5, 109. 21. Eliot, C., A Monograph of the British S. CHINNADURAI 5. Chester, C. M., J. Exp. Mar. Biol. Ecol., Nudibranchiate Molluscs, 8 (Supplemen- K. S. ABHILASH 1996, 198, 113–130. tary), Ray Society, London, 1910, p. K. K. SAJIKUMAR 198. 6. Alder, J. and Hancock, A., Trans. Zool. V. KRIPA 22. Naville, A., Rev. Suisse Zool., 1926, 33, Soc., London, 1864, 5, 113–147. 7. Thompson, T. E. and Brown, G. H., Bio- 251–286. ICAR-Central Marine Fisheries logy of Opisthobranch Molluscs, 1984, 2, 23. Rasmussen, E., Vidensk. Meddrdan- 229, Ray Society, no. 156. sknaturh. Foren., 1944, 107, 207–233. Research Institute, 8. Leloup, E., Records of Indian Museum, 24. Vannucci, M. and Hosoe, K., Bull. Inst. P.O. Box. 1603, Ernakulam North P.O, 1932, 34, 131–170. Oceanogr., 1953, 4, 103–120. Kochi 682 018, India 9. Mammen, T. A., J. Mar. Biol. Assoc. 25. Pruvot-Fol., Trav. Inst. Sci. Cherifien, *For correspondence. India, 1963, 5, 27–61. Zool., 1953, 5, 1–105. e-mail: [email protected]

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