R. Saravanan 1, N. Ramamoorthy 2, I. Syed Sadiq 3, K. Shanmuganathan 4 & G. Gopakumar 5
1,2,3,4,5 Marine Biodiversity Division, Mandapam Regional Centre of Central Marine Fisheries Research Institute (CMFRI), Mandapam Fisheries, Tamil Nadu 623520, India
1 stingray_mr@yahoo.com (corresponding author), 2 ramamoorthymdm@gmail.com, 3 shamimasadiq@gmail.com, 5 drggopakumar@gmail.com
doi: http://dx.doi.org/10.11609/JoTT.o3878.7726-8 | ZooBank: urn:lsid:zoobank.org:pub:63DC1D2B-8C30-46C7-9C76-255D6D4A47F4
Editor: M. Nithyanandan, Environmental Department, La Ala Al Kuwait Real Estate. Co. K.S.C., Kuwait. Date of publication: 26 August 2015 (online & print)
Manuscript details: Ms # o3878 | Received 11 December 2013 | Final received 09 July 2015 | Finally accepted 11 August 2015
Citation: Saravanan, R., N. Ramamoorthy, I.S. Sadiq, K. Shanmuganathan & G. Gopakumar (2015). A note on the obligate symbiotic association between crab Zebrida adamsii White, 1847 (Decapoda: Pilumnidae) and Flower Urchin Toxopneustes pileolus (Lamarck, 1816) (Camarodonta: Toxopneustidae) from the Gulf of Mannar, India. Journal of Threatened Taxa 7(10): 7726–7728; http://dx.doi.org/10.11609/JoTT.o3878.7726-8
Copyright: © Saravanan et al. 2015. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use of this article in any medium, reproduction and distribution by providing adequate credit to the authors and the source of publication.
Funding: ICAR-Central Marine Fisheries Research Institute (CMFRI).
Competing interests: The authors declare no competing interests.
Acknowledgements: The authors sincerely thank Dr. A. Gopalakrishnan, Director, CMFRI for his encouragement and support.

The Toxopneustes pileolus (Image 1) is one of the most venomous sea urchins. Venom comes from the disc-shaped pedicellariae, which is pale-pink with a white rim, but not from the white tip spines. Contact of the pedicellarae with the human body can lead to numbness and even respiratory difficulties. This species of sea urchin comes under the family Taxopneustidae which includes 11 other genera and 38 species. The general distribution of the flower urchin is Indo-Pacific in a depth range of 0–90 m (Suzuki & Takeda 1974). The genus Toxopneustes has four species viz., T. elegans Döderlein, 1885, T. maculatus (Lamarck, 1816), T. pileolus (Lamarck, 1816), T. roseus (A. Agassiz, 1863). James (1982, 1983, 1986, 1988, 1989, 2010) and Venkataraman et al. (2013) reported the occurrence of T. pileolus from the Andamans and the Gulf of Mannar, but did not mention the association of Zebrida adamsii with this species. On examination of these sea urchins the parthenopid crab Zebrida adamsii association was noted. Generally echinoderms and many species of crustaceans live in symbiotic association with each other. Many sea urchin species, some of which harbor endo or ecto-symbiotic crustaceans, form aggregations consisting of tens of individual (Telford 1978; Bell 1984). In these dense aggregations, ectosymbiotic crustaceans may easily move from one sea urchin to the next under the cover of their spines.
Members of five genera of eumedonid crabs (Echinoecus, Eumedonus, Gonatonotus, Zebridonus and Zebrida) are known obligate symbionts on sea urchins (Ng & Chia 1999). Organisms with an obligate symbiotic lifestyle are restricted in their distribution and abundance by the availability of suitable hosts. The symbiotic genus Zebrida was thought to be monotypic for a long time, but recently, two additional species, namely Zebrida brevicarinata Ng & Chia, 1999 and Zebrida longispina Haswell, 1880; were recognized bringing the total number to three (Ng & Chia 1999).
Materials and Methods
About 15 specimens of Toxopneustes pileolus with a test diameter ranging from 35–98 mm were brought alive from bottom set gillnet landing at Vedalai fishing village along the Gulf of Mannar during the regular survey trip in December 2013. A thorough visual examination was carried out to count the number of symbionts. All the sea urchins were kept in a 2-tonne FRP tank with sand bedding planted with seagrass species Cymodocea serrulata to simulate the natural environment. These were fed with seagrass species Cymodocea serrulata and Coralline algae Halimeda gracilis during the one month period of investigation, to know the nature of the association between the sea urchin and crab. To assess the host specificity of the crab association with T. pileolus, five individuals of Salmacis bicolor with a test diameter range of 18.92±5.6 was released in the same tank. The identification of the sea urchin was done according to Smith & Kroh (2011), after denuding the test. For the identification of the zebrid crabs their eyestalk, rostrum, lateral carapace teeth and ambulatory legs were studied to differentiate the present species from the three known species under the genus Zebrida.
Results and Discussion
The genus Toxopneustes contains one of the most venomous sea urchin species, if touched by the bare hand it can inflict a severe sting through its globiferous pedicellariae. The venom causes severe pain and muscular paralysis that may last around six hours. Death from poison is unknown, but the pain can reportedly lead to accidental drowning of swimmers and skin divers (McCormack 2007). The spines are relatively short and non venomous. It is an algae feeding species which prefers to feed on coralline green and rohodolith algae. Upon examination of these urchins, there were nearly five sea urchins hosting the parthenopid crab Zebrida adamsii and a maximum of four crabs (Image 2) were found on a sea urchin with 88mm test diameter. There were 10 males and four females observed among the collected sea urchins. Yanagisawa & Hamaishi (1986) reported that a solitary crab Zebrida adamsii lives on a host from the earliest stage of its benthic life. During the breeding season males frequently move between hosts to search for mates. In the present investigation no ovigerous females were found.
The association of Z. adamsii with T. pileolus is reported for the first time from the Gulf of Mannar and has been found to be parasitic. Naked inter-ambulacral zones (Image 3) were observed which could have been damaged by the crabs. Suzuki & Takeda (1974) found the evidence that urchin tissue was being ingested by Z. adamsii and argued that the relationship between crab and urchin is essentially a parasitic one. During the study period, although five individuals of Salmacis bicolor were released in the same tank and in contact with the crab possessing T. pileolus, Z. adamsii never ventured out of T. pileolus. Daniel & Krishnan (1979), however, reported the association of Z. adamsii with Salmacis virgulata. It was found that the Z. adamsii was feeding on the tube-feet in the inter-ambulacral zone (Image 3), but inspite of this, the sea urchins were found to survive. Thiel et al. (2003) studied the different crustacean ectosymbionts on sea urchins and compiled the nature of their symbiotic relationship (Table 1). In sea urchins, tube-feet are mainly responsible for gas exchange, but whether the damage done to tube feet is within the tolerable range of the sea urchin or beyond; could not be concluded from the present observation. This observation indicates preference of Z. adamsii to certain species and certain size ranges (Table 2).

References
Bell, J.L. (1984). Changing residence: dynamics of the symbiotic relationship between Dissodactylus mellitae Rathbun (Pinnotheridae) and Mellita quinquiesperforata (Leske) (Echinodermata). Journal of Experimental Marine Biology and Ecology 82(2–3): 101–115; http://dx.doi.org/10.1016/0022-0981(84)90097-2
Daniel, A. & S. Krishnan (1979). A parthenopid crab, Zebrida adamsii White, 1847 inhabiting interspaces of spines of the Sea Urchin, Salmacis virgulata L. Agassiz, 1846. Bulletin of Zoological Survey of India 1(2): 171–175.
James, D.B. (1982). Ecology of intertidal echinoderms of the Indian Seas. Journal of Marine Biological Association of India 24(1&2): 124–129.
James, D.B. (1983). Sea cucumber and sea urchin resources. CMFRI Bulletin 34: 85–93.
James, D.B. (1986). Zoogeography of shallow-water echinoderms of Indian Seas, pp. 569–591. In: James, P.S.B.R. (ed.). Recent Advances in Marine Biology. Today and Tomorrow Printers and Publishers, New Delhi.
James, D.B. (1988) Echinoderm fauna of the proposed national marine park in the Gulf of Mannar. In: Proceedings symposium endangered marine animals and marine parks. pp 403–406
James, D.B. (1989). Echinoderms of Lakshadweep and their zoogeography. CMFRI Bulletin Marine living resources of the union territory of Lakshadweep An Indicative Survey With Suggestions For Development, 43, 97–144pp.
James, D.B. (2010). Marine poisonous echinoderms. Fishing Chimes, 30(1): 39–41.
McCormack, G. (2007). Cook Islands Biodiversity Database, Version 2007.2. Cook Islands Natural Heritage Trust, Rarotonga. Online at http://cookislands.bishopmuseum.org.
Ng, P.K.L. & D.G.B. Chia (1999). “Revision of the genus Zebrida White, 1847 (Crustacea: Decapoda: Brachyura: Eumedonidae)”. Bulletin of Marine Science 65(2): 481–495.
Smith, A.B. & A. Kroh (2011). The Echinoid Directory. World Wide Web electronic publication. http://www.nhm.ac.uk/research-curation/projects/echinoid-directory. Accessed on 9 December 2013
Suzuki, K. & M. Takeda (1974). On a parthenopid crab, Zebrida adamsii on the Sea Urchins from Suruga Bay, with a special reference to their parasitic relations. Bulletin of Natural Science Museum of Tokyo 17(4): 287–296.
Telford, M. (1978). Distribution of two species of Dissodactylus (Brachuyra: Pinnotheridae) among their echinoid host population in Barbados. Bulletin of Marine Science 32: 585–594.
Thiel, M., A. Zander & J.A. Baesa (2003). Movements of the symbiotic crab Liopetrolisthesmitra between its host Sea Urchin Tetrapygusniger. Bulletin of Marine Science 72(1): 89–101.
Venkatraman, C., K. Venkataraman, R. Rajkumar, S. Shrinivaasu, P. Padmanaban, K. Paramasivam & C. Sivaperuman (2013). Diversity and distribution of Echinoderms in Palk Bay and Gulf of Mannar Biosphere Reserve, southern India, pp. 197–212. In: Venkataraman, K., C. Sivaperuman & C. Raghunathan (eds.). Ecology and Conservation of Tropical Marine Faunal Communities. Springer-Verlag Berlin Heidelberg.
Yanagisawa, Y. & A. Hamaishi (1986). Mate acquisition by a solitary crab Zebrida adamsii, a symbiont of the sea urchin. Journal of Ethology 4(2): 153–162.
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