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Differences in the cnidomes and toxicities of the oral arms of two commercially harvested rhizostome jellyfish species in Thailand

Published online by Cambridge University Press:  25 August 2020

Yusuke Kondo*
Affiliation:
Takehara Station, Setouchi Field Science Center, Graduate School of Integrated Science for Life, Hiroshima University, 5-8-1 Minato-machi, Takehara, Hiroshima, 725-0024, Japan
Yasuko Suzuki
Affiliation:
Department of Ocean Sciences, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo, 108-8477, Japan
Susumu Ohtsuka
Affiliation:
Takehara Station, Setouchi Field Science Center, Graduate School of Integrated Science for Life, Hiroshima University, 5-8-1 Minato-machi, Takehara, Hiroshima, 725-0024, Japan
Hiroshi Nagai
Affiliation:
Department of Ocean Sciences, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo, 108-8477, Japan
Hayato Tanaka
Affiliation:
Tokyo Sea Life Park, 6-2-3 Rinkai-cho, Edogawa-ku, Tokyo, 134-0086, Japan
Khwanruan Srinui
Affiliation:
Institute of Marine Science, Burapha University, Muang, Chon Buri, 20131, Thailand
Hiroshi Miyake
Affiliation:
School of Marine Bioscience, Kitasato University, 1-15-1, Kitasato, Minami-ku, Sagamihara, Kanagawa, 252-0373, Japan
Jun Nishikawa
Affiliation:
School of Marine Science and Technology, Tokai University, 3-20-1, Orido, Shimizu-ku, Shizuoka, Shizuoka, 424-8610, Japan
*
Author for correspondence: Yusuke Kondo, E-mail: [email protected]

Abstract

In Thailand, two species of rhizostome jellyfish, Rhopilema hispidum and Lobonemoides robustus, are commercially harvested. The cnidomes, nematocyst size and toxicities were compared between these species. Rhopilema hispidum and L. robustus each had four types of nematocysts on their oral arms. For R. hispidum, these nematocyst types included two types of isorhiza and two types of rhopaloid, while in L. robustus, there were three types of isorhiza and one type of rhopaloid. For R. hispidum, tubule lengths of the largest nematocyst type (large round isorhiza; mean ± SD = 313.8 ± 62.2 μm) were significantly longer than those of L. robustus (large ellipsoid rhopaloid; 162.1 ± 38.5 μm). Using the freshwater shrimp, Palaemon paucidens, in a bioassay, we determined that the lethal nematocyst concentrations for R. hispidum and L. robustus were 5705.3 ± 1118.1 and 3408.3 ± 1032.9 unit g−1 wet weight, respectively, and that these concentrations were significantly higher in the former than in the latter.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

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References

Al-Rubiay, KK, Al-Musaoi, HA, Alrubaiy, L and Al-Freje, MG (2009) Skin and systemic manifestations of jellyfish stings in Iraqi fishermen. Libyan Journal of Medicine 4, 9699.CrossRefGoogle ScholarPubMed
Arai, MN (1997) A Functional Biology of Scyphozoa. London: Chapman & Hall.Google Scholar
Ates, R (1988) Medusivorous fishes: a review. Zoologische Mededeelingen 62, 2942.Google Scholar
Avian, M, Del Negro, P and Rottini Sandrini, L (1991) A comparative analysis of nematocysts in Pelagia noctiuca and Rhizostoma pulmo from the North Adriatic Sea. Hydrobiologia 216/217, 615621.CrossRefGoogle Scholar
Avian, M, Spanier, E and Galil, B (1995) Nematocysts of Rhopilema nomadica (Scyphozoa: Rhizostomeae), and immigrant jellyfish in the eastern Mediterranean. Journal of Morphology 224, 221231.CrossRefGoogle Scholar
Behera, PR, Raju, SS, Jishnudev, MA, Ghosh, S and Saravanan, R (2020) Emerging jellyfish fisheries along Central South East coast of India. Ocean and Coastal Management 191, 105183.CrossRefGoogle Scholar
Birsa, LM, Verity, PG and Lee, RF (2010) Evaluation of the effects of various chemicals on discharge of and pain caused by jellyfish nematocysts. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 151, 426430.Google ScholarPubMed
Brotz, L (2016) Jellyfish fisheries: a global assessment. In Pauly, D and Zeller, D (eds), Global Atlas of Marine Fisheries: A Critical Appraisal of Catches and Ecosystem Impacts. Washington, DC: Island Press, pp. 110124.Google Scholar
Brotz, L, Schiariti, A, López-Martínez, J, Álvarez-Tello, J, Peggy Hsieh, YH, Jones, RP, Quiñones, J, Dong, Z, Morandini, AC, Preciado, M, Laaz, E and Mianzanet, H (2017) Jellyfish fisheries in the Americas: origin, state of the art, and perspectives on new fishing grounds. Reviews in Fish Biology and Fisheries 27, 129.CrossRefGoogle Scholar
Burke, WA (2002) Cnidarians and human skin. Dermatologic Therapy 15, 1825.CrossRefGoogle Scholar
Burnett, JW and Calton, GJ (1985) Recurrent eruption following a solitary envenomation by the cnidarian Stomolophous meleagris. Toxicon 23, 10101014.CrossRefGoogle ScholarPubMed
Calder, DR (1972) Nematocysts of the medusa stage of Rhopilema verrilli (Scyphozoa, Rhizostomeae). Transactions of the American Microscopical Society 91, 213216.CrossRefGoogle Scholar
Calder, DR (1983) Nematocysts of stages in the life cycle of Stomolophus meleagris, with keys to scyphistomae and ephyrae of some western Atlantic Scyphozoa. Canadian Journal of Zoology 61, 11851192.CrossRefGoogle Scholar
Chen, J and Ding, G (1981) On the nematocysts of the various stages of development of Rhopilema esculenta Kishinouye (Cnidaria, Scyphozoa). Acta Zoologica Sinica 27, 310316. [In Chinese with English abstract].Google Scholar
Dong, Z, Liu, D and Keesing, JK (2010) Jellyfish blooms in China: dominant species, causes and consequences. Marine Pollution Bulletin 60, 954963.CrossRefGoogle ScholarPubMed
FAO (2018) FishStatJ – software for fishery statistical time series. Available at http://www.fao.org/fishery/statistics/software/fishstatj/en (Accessed 18 October 2018).Google Scholar
Fenner, PJ (1993) 63rd Annual Report 1992–93. Newstead: Surf Life Saving Queensland.Google Scholar
Fenner, PJ (2005) Venomous jellyfish of the world. South Pacific Underwater Medicine Society Journal 35, 131138.Google Scholar
Fenner, PJ, Lippmann, J and Gershwin, LA (2010) Fatal and nonfatal severe jellyfish stings in Thai waters. Journal of Travel Medicine 17, 133138.CrossRefGoogle ScholarPubMed
Fujii, N, Kondo, Y, Okada, S, Ohtsuka, S, Urata, M, Adati, A, Kato, M, Yamaguchi, S, Nakaguchi, K, Muranaka, S, Yoshino, K and Tsutsumi, H (2014) Estimation of biomass of the rhizostome jellyfish Rhopilema esculentum Kishinouye in Ariake Sea in summer and fall of 2012. Bulletin of the Plankton Society of Japan 61, 2331. [In Japanese with English abstract].Google Scholar
Galil, BS, Spanier, E and Ferguson, WW (1990) The Scyphomedusae of the Mediterranean coast of Israel, including two Lessepsian migrants new to the Mediterranean. Zoologische Mededelingen 64, 95105.Google Scholar
Ghosh, TK, Gomes, A and Nag Chaudhuri, AK (1990) Pharmacological actions of tentacle extract of the jellyfish, Acromitus rabanchatu, occurring in the Bay of Bengal. Indian Journal of Experimental Biology 28, 3942.Google ScholarPubMed
Gul, S, Jahangir, S and Schiariti, A (2015) Jellyfish fishery in Pakistan. Plankton and Benthos Research, 10, 220224.CrossRefGoogle Scholar
Halstead, BW (1965) Poisonous and Venomous Marine Animals of the World. London: Darwin Press.Google Scholar
Heeger, T, Möller, H and Mrowietz, U (1992) Protection of human skin against jellyfish (Cyanea capillata) stings. Marine Biology 113, 669678.CrossRefGoogle Scholar
Heins, A, Glatzel, T and Holst, S (2015) Revised descriptions of the nematocysts and the asexual reproduction modes of the scyphozoan jellyfish Cassiopea andromeda (Forskål, 1775). Zoomorphology 134, 351366.CrossRefGoogle Scholar
Hessinger, DA and Lenhoff, HM (1988) The Biology of Nematocysts. San Diego, CA: Academic Press.Google Scholar
Holst, S, Sötje, I, Tiemann, H and Jarms, G (2007) Life cycle of the rhizostome jellyfish Rhizostoma octopus (L.) (Scyphozoa, Rhizostomeae), with studies on cnidocysts and statoliths. Marine Biology 151, 16951710.CrossRefGoogle Scholar
Jarms, G, Tiemann, H and Båmstedt, U (2002) Development and biology of Periphylla periphylla (Scyphozoa: Coronatae) in a Norwegian fjord. Marine Biology 141, 647657.Google Scholar
Kass-Simon, G and Scappaticci, AA Jr (2002) The behavioral and developmental physiology of nematocysts. Canadian Journal of Zoology 80, 17721794.CrossRefGoogle Scholar
Kawahara, M, Uye, S, Burnett, J and Mianzan, H (2006) Stings of edible jellyfish (Rhopilema hispidum, Rhopilema esculentum and Nemopilema nomurai) in Japanese waters. Toxicon 48, 713716.CrossRefGoogle Scholar
Kim, JH, Han, SB and Durey, A (2018) Fatal pulmonary edema in a child after jellyfish stings in Korea. Wilderness and Environmental Medicine 29, 527530.CrossRefGoogle Scholar
Kingsford, MJ, Pitt, KA and Gillanders, BM (2000) Management of jellyfish fisheries, with special reference to the order Rhizostomeae. Oceanograply and Marine Biology: An Annual Review 38, 85156.Google Scholar
Kitatani, R, Yamada, M, Kamio, M and Nagai, H (2015) Length is associated with pain: jellyfish with painful sting have longer nematocyst tubules than harmless jellyfish. PLoS ONE 10, e0135015.CrossRefGoogle ScholarPubMed
Kokelj, F and Plozzer, C (2002) Irritant contact dermatitis from the jellyfish Rhizostoma pulmo. Contact Dermatitis 46, 179180.CrossRefGoogle ScholarPubMed
Kubota, S (1985) Hydrozoan – various lifestyles and species. Iden 39, 5261. [In Japanese].Google Scholar
Kubota, S, Kawamura, M and Ueno, S (2006) First occurrence of a mature medusa of Nemopilema nomurai (Cnidaria, Scyphozoa, Rhizostomae) in Tanabe Bay, Wakayama prefecture, Japan. Nankiseibutsu 48, 5759. [In Japanese and English abstract].Google Scholar
Li, R, Yu, H, Xue, W, Yue, Y, Liu, S, Xing, R and Li, P (2014) Jellyfish venomics and venom gland transcriptomics analysis of Stomolophus meleagris to reveal the toxins associated with sting. Journal of Proteomics 106, 1729.CrossRefGoogle ScholarPubMed
López-Martínez, J and Álvarez-Tello, J (2013) The jellyfish fishery in Mexico. Agricultural Sciences 4, 5761.Google Scholar
Lucas, CH, Gelcich, S and Uye, S (2014) Living with jellyfish: management and adaptation strategies. In Pitt, KA and Lucas, CH (eds), Jellyfish Blooms. Heidelberg: Springer Netherlands, pp. 129150.CrossRefGoogle Scholar
Mariottini, GL and Pane, L (2010) Mediterranean jellyfish venoms: a review on Scyphomedusae. Marine Drugs 8, 11221152.CrossRefGoogle ScholarPubMed
Mariottini, GL, Giacco, E and Pane, L (2008) The mauve stinger Pelagia noctiluca (Forsskål, 1775). Distribution, ecology, toxicity and epidemiology of stings: A review. Marine Drugs 6, 496513.Google ScholarPubMed
Mariscal, RN (1974) Nematocysts. In Muscatine, L and Lenhoff, HM (eds), Coelenterate Biology: Reviews and new Perspectives. New York, NY: Academic Press, pp. 129178.CrossRefGoogle Scholar
Marques, AC and Collins, AG (2004) Cladistic analysis of Medusozoa and cnidarian evolution. Invertebrate Biology 123, 2342.CrossRefGoogle Scholar
Marsh, LM and Slack-Smith, SM (2010) Field Guide to Sea Stingers and Other Venomous and Poisonous Marine Invertebrates of Western Australia. Western Australia: Western Australian Museum.Google Scholar
Morandini, AC, Custódio, MR and Marques, AC (2016) Phylum Porifera and Cnidaria. In Gopalakrishnakone, P, Haddad, V Jr, Kem, WR, Tubaro, A and Kim, E (eds), Marine and Freshwater Toxins. Dordrecht: Springer, pp. 287316.CrossRefGoogle Scholar
Nishida, S and Nishikawa, J (2011) Biodiversity of marine zooplankton in Southeast Asia (Project-3: Plankton Group). In Nishida, S, Fortes, MD and Miyazaki, N (eds), Coastal Marine Science in Southeast Asia —Synthesis Report of the Core University Program of the Japan Society for the Promotion of Science: Coastal Marine Science (2001–2010). Tokyo: Terra Scientific Publishing Company, pp. 5971.Google Scholar
Nishikawa, J, Thu, NT, Ha, TM and Thu, PT (2008) Jellyfish fisheries in northern Vietnam. Plankton and Benthos Research 3, 227234.CrossRefGoogle Scholar
Nishikawa, J, Ohtsuka, S, Mulyadi, N, Mujiono, N, Lindsay, DJ, Miyamoto, H and Nishida, S (2015) A new species of the commercially harvested jellyfish Crambionella (Scyphozoa) from central Java, Indonesia with remarks on the fisheries. Journal of the Marine Biological Association of the United Kingdom 95, 471481.Google Scholar
Nishikawa, J, Srinui, K, Ohtsuka, S, Kondo, Y, Miyake, H, Lindsay, D and Iida, A (2019) Jellyfish fisheries in Thailand. Aquabiology 41, 1318. [In Japanese with English abstract].Google Scholar
Ohtsuka, S, Kondo, Y, Sakai, Y, Shimazu, T, Shimomura, M, Komai, T, Yanagi, K, Fujita, T, Nishikawa, J, Miyake, H, Venmathi-Maran, BA, Go, A, Nagaguchi, K, Yamaguchi, S, Dechsakulwatana, C, Srinui, K, Putchakarn, S, Mulyadi, M, Mujiono, N, Md F, and Yusoff, FM (2010) In-situ observations of symbionts on medusae occurring in Japan, Thailand, Indonesia and Malaysia. Bulletin of the Hiroshima University Museum 2, 918.Google Scholar
Omori, M and Kitamura, M (2004) Taxonomic review of three Japanese species of edible jellyfish (Scyphozoa: Rhizostomeae). Plankton Biology and Ecology 51, 3651.Google Scholar
Omori, M and Nakano, E (2001) Jellyfish fisheries in Southeast Asia. Hydrobiologia 451, 1926.CrossRefGoogle Scholar
Östman, CA (2000) Guideline to nematocyst nomenclature and classification, and some notes on the systematic value of nematocysts. Scientia Marina 64, 3146.CrossRefGoogle Scholar
Othman, I, Fathilah, AR, Mohd Saad, J, Mohd Yusof, M, Mustaffa, MR and Azila, N (1996) Studies of the venomous coelenterate: Rhopilema hispidum. Journal of Natural Toxins 5, 361375.Google Scholar
Palmieri, MG, Barausse, A, Luisetti, T and Turner, K (2014) Jellyfish blooms in the Northern Adriatic Sea: fishermen's perceptions and economic impacts on fisheries. Fisheries Research 155, 5158.CrossRefGoogle Scholar
Peach, MB and Pitt, KA (2005) Morphology of the nematocysts of the medusa of two scyphozoans, Catostylus mosaicus and Phyllorhiza punctata (Rhizostomeae): implications for capture of prey. Invertebrate Biology 124, 98108.CrossRefGoogle Scholar
Purcell, JE (1984) The functions of nematocysts in prey capture by epipelagic siphonophores (Coelenterata, Hydrozoa). Biological Bulletin 166, 310327.CrossRefGoogle Scholar
Purcell, JE and Mills, CE (1988) The correlation between nematocysts types and diets in pelagic hydrozoa. In Hessinger, DA and Lenhoff, HM (eds), The Biology of Nematocysts. San Diego, CA: Academic Press, pp. 463485.CrossRefGoogle Scholar
Purcell, JE, Uye, S and Lo, WT (2007) Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Marine Ecology Progress Series 350, 153174.CrossRefGoogle Scholar
R Core Team (2016). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Computing. Available at: https://www.R-project.org/.Google Scholar
Remigante, A, Costa, R, Morabito, R, Spada, GL, Marino, A and Dossena, S (2018) Impact of scyphozoan venoms on human health and current first aid options for stings. Toxins 10, 133.CrossRefGoogle ScholarPubMed
Richardson, AJ, Bakun, A, Hays, GC and Gibbons, MJ (2009) The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends in Ecology and Evolution 24, 312322.CrossRefGoogle ScholarPubMed
Schuchert, P (1993) Phylogenetic analysis of the Cnidaria. Zeitschrift für Zoologische Systematik und Evolutionsforschung 31, 161173.CrossRefGoogle Scholar
Technau, U, Genikhovich, G and Kraus, JEM (2015) Cnidaria. In Wanninger, A (ed.), Evolutionary Developmental Biology of Invertebrates. 1: Introduction, Non-Bilateria, Acoelomorpha, Xenoturbellida, Chaetognatha. Vienna: Springer, pp. 115163.CrossRefGoogle Scholar
Williamson, JA, Fenner, PJ, Burnett, JW and Rifkin, JF (1996) Venomous and Poisonous Marine Animals: Medical and Biological Handbook. Sydney: University of New South Wales Press.Google Scholar
Yasuda, T, Ueno, S and Adachi, A (2003) Marine UFO medusa. Tokyo: Kouseisya. [In Japanese].Google Scholar