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Impact of sea spider parasitism on host clams: susceptibility and intensity-dependent mortality

Published online by Cambridge University Press:  14 March 2017

Katsumasa Yamada ,
Katsumi Miyazaki ,
Takeshi Tomiyama ,
Gen Kanaya ,
Yoshifumi Miyama ,
Tomoyoshi Yoshinaga ,
Kunihiro Wakui ,
Masanori Tamaoki  and
Mitsuharu Toba
Katsumasa Yamada*
Affiliation:
Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Taira-machi, Nagasaki, 851-2213, Japan
Katsumi Miyazaki
Affiliation:
Department of Environmental Science, Faculty of Science, Niigata University, Niigata 950-2181, Japan
Takeshi Tomiyama
Affiliation:
Graduate School of Biosphere Science, Hiroshima University Higashi-Hiroshima, Higashi-Hiroshima, 739-8528, Japan
Gen Kanaya
Affiliation:
National Institute for Environmental Studies, Onogawa 16-2, Tsukuba 305-8506, Japan
Yoshifumi Miyama
Affiliation:
Tokyo Bay Fisheries Laboratory, Chiba Prefectural Fisheries Research Center, 3091 Okubo, Futtsu, Chiba 293-0042, Japan
Tomoyoshi Yoshinaga
Affiliation:
Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan
Kunihiro Wakui
Affiliation:
Fukushima Prefectural Fisheries office, Iwaki, Fukushima, 970-8026, Japan
Masanori Tamaoki
Affiliation:
National Institute for Environmental Studies, Onogawa 16-2, Tsukuba 305-8506, Japan
Mitsuharu Toba
Affiliation:
Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo 108-0075, Japan
*
Correspondence should be addressed to: K. Yamada, Seikai National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Taira-machi, Nagasaki, 851-2213, Japan. email: k.yamada@affrc.go.jp
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Abstract

Nymphonella tapetis (Pycnogonida, Ascorhynchidae) is an endoparasitic sea spider affecting bivalves. Recently, sea spiders have been found on a massive scale in the commercially important Manila clams (Veneridae, Ruditapes philippinarum) in Japan (Tokyo Bay). Simultaneously, mass mortality has occurred in this area. Local fishers assumed that this mass mortality was caused by the parasitic sea spider, despite the effect of the parasite and parasite intensity on the host being unknown. To evaluate the susceptibility of the Manila clam to sea spider infestation and the impact on mortality levels, we established six treatments at different infection intensities (density of newly hatched larvae of sea spiders) over a 6-month long laboratory experiment. We monitored mortality and three susceptibility indices (clearance rate, sand-burrowing speed and adductor muscle strength) under sufficient food conditions. Parasitization by sea spider affected clearance rate and sand-burrowing speed. The pattern of parasitic intensity effects on survival of Manila clam hosts was shown to be dependent on the levels of parasite numbers, i.e. clams with lower parasitic levels (total of <200 hatching larvae of sea spider given to a host) have a higher survival rate, and high mortality of host clams was shown in excessively higher parasitic densities (400–4000 individuals). Such pattern of parasitic effects on host survival might be one of the causes of mass mortality of Manila clams occurring in the field.

Keywords

Clam fisheryendoparasitehost-parasite interactionmortalityparasite intensitysublethal impact
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 4 , June 2018 , pp. 735 - 742
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Adler, F.R. and Kretzschmar, M. (1992) Aggregation and stability in parasite-host models. Parasitology 104, 199–205.CrossRefGoogle ScholarPubMed
Altizer, S., Dobson, A.P., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006) Seasonality and the dynamics of infectious disease. Ecology Letters 9, 467–484.CrossRefGoogle Scholar
Anderson, R.M. and May, R.M. (1978) Regulation and stability of hostparasite population interactions, I: regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Chow, S., Niwa, K., Okamoto, S., Murauchi, Y., Hirai, R., Hibino, M., Wakui, K., Tomiyama, T., Kobayashi, Y., Toba, M. and Kano, Y. (2012) Genetic diversity in three local populations of the parasitic sea spider Nymphonella tapetis and taxonomic position of the species. Nippon Suisan Gakkaishi 78, 895–902. [In Japanese with English abstract].CrossRefGoogle Scholar
Cox, D.R. (1972) Regression models and life tables. Journal of the Royal Statistical Society B 34, 187–202.Google Scholar
Fredensborg, B.L., Mouritsen, K.N. and Poulin, R. (2005) Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Marine Ecology Progress Series 290, 109–117.CrossRefGoogle Scholar
Hudson, P.J., Dobson, A.P. and Newborn, D. (1998) Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle ScholarPubMed
Kikuchi, T. (1976) Rediscovery of the bivalve-infesting pycnogonid, Nymphonella tapetis Ohshima 1927, in Amakusa. Publications from the Amakusa Marine Biological Laboratory 4, 51–56.Google Scholar
May, R.M. and Anderson, R.M. (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society, B 219, 281–313.Google ScholarPubMed
Miyazaki, K., Kobayashi, Y., Toba, M. and Tsuchiya, H. (2010) Biology of Nymphonella tapetis Ohshima, 1927, a harmful pycnogonid endoparasitic on the commercial bivalve, Ruditapes philippinarum. Proceedings of the Japanese Society of Systematic Zoology 28, 45–54. [In Japanese with English abstract]Google Scholar
Miyazaki, K., Tomiyama, T., Yamada, K. and Tamaoki, M. (2015) 18s analysis on the taxonomic position of an endoparasitic pycnogonid Nymphonella tapetis (Arthropoda, Pycnogonida) in the family Ascorhynchidae. Journal of Crustacean Biology 35, 491–494.CrossRefGoogle Scholar
Møller, A.P. (2000) Survival and reproductive rate of mites in relation to resistance of their barn swallow hosts. Oecologia 124, 351–357.Google ScholarPubMed
Murauchi, Y., Okamoto, S., Hirai, A., Miyazaki, D., Yamamoto, N., Hibino, M., Kawamura, K., Harada, M., Okamura, Y. and Hattori, K. (2014) Seasonal dynamics of the parasitic larvae free-living adults of the sea spider Nymphonella tapetis infecting the Manila clam Ruditapes phillipinarum in the eastern coast of China peninsula, and the effect of water temperature on the infection levels. Aquaculture Science 62, 183–190. [In Japanese with English abstract]Google Scholar
Nakamura, Y. (2004) Suspension feeding and growth of juvenile Manila clam Ruditapes philippinarum reared in the laboratory. Fisheries Science 70, 215–222.CrossRefGoogle Scholar
Ogawa, K. and Matsuzaki, K. (1985) Discovery of bivalve-infesting Pycnogonida, Nymphonella tapetis, in a new host, Hiatella orientalis. Zoological Science 2, 583–589.Google Scholar
Ohshima, H. (1927) Nymphonella tapetis, ng, n. sp., a pycnogon parasitic in a bivalve. Annotationes Zoologicæ Japonenses 11, 257–263.Google Scholar
Ohshima, H. (1933) The adult of the bivalve-infesting pycnogonid, Nymphonella tapetis Ohshima. Annotationes Zoologicæ Japonenses 14, 53–60.Google Scholar
Ohshima, H. (1935) A further note on Nymphonella tapetis: the egg-carrying mature male (Eurycydidae: Pantopoda). Annotationes Zoologicæ Japonenses 15, 95–102.Google Scholar
Sassa, S., Watabe, Y., Yang, S. and Kuwae, T. (2011) Burrowing criteria and burrowing mode adjustment in bivalves to varying geoenvironmental conditions in intertidal flats and beaches. PLoS ONE 6, e25041. http://dx.doi.org/10.1371/journal.pone.0025041.CrossRefGoogle ScholarPubMed
Toba, M., Kobayashi, Y., Kakino, J., Yamakawa, H., Ishii, R. and Okamoto, R. (2016) Stocks and fisheries of asari in Japan. Bulletin of Japan Fisheries Research and Education Agency 42, 9–21.Google Scholar
Toba, M. and Miyama, Y. (1991) Gonadal development and spawning induction in artificially conditioned manila clams Ruditapes philippinarum. Nippon Suisan Gakkaishi 57, 1269–1275. [In Japanese]CrossRefGoogle Scholar
Tomiyama, T., Yamada, K., Wakui, K., Tamaoki, M. and Miyazaki, K. (2016) Impact of sea spider parasitism on host clams: relationship between burial patterns and parasite loads, somatic condition, and survival of host. Hydrobiologia 770, 15–26.CrossRefGoogle Scholar
Tompkins, D.M. and Begon, M.E. (1999) Parasites can regulate wildlife populations. Parasitology Today 15, 311–313.CrossRefGoogle ScholarPubMed
Waki, T. and Yoshinaga, T. (2013) Experimental challenges of juvenile and adult Manila clams with the protozoan Perkinsus olseni at different temperatures. Fisheries Science 79, 779–786.CrossRefGoogle Scholar
Wakita, K., Yamakita, T., Yamada, K., Yagi, N. and Kurokura, H. (2014) An evaluation of Tokyo Bay as a marine space for Porphyra spp. farming: evaluating marine spaces through quantitative examination of water environmental variables across categorized marine spaces, making use of multiple institutional data. The Japanese Society of Fisheries Science 80, 689–701. [In Japanese with English abstract]CrossRefGoogle Scholar
Yamada, K., Miyamoto, Y., Fujii, C., Yamaguchi, K. and Hamaguchi, M. (2014) Vertical zonation and aggregated distribution of the Manila clam on subtidal sandy flats in a coastal brackish lagoon along Sea of Japan. Marine Ecology 35, 408–418.CrossRefGoogle Scholar
Yamada, K., Miyamoto, Y., Nakano, T. and Okamura, K. (2016a) Inter- and intraspecific variation in anoxic survival among three bivalve species in intertidal and subtidal areas along the coast of Japan. Plankton and Benthos Research 11, 49–56.CrossRefGoogle Scholar
Yamada, K., Miyazaki, K., Chow, S., Yamamoto, T., Tomiyama, T., Yoshinaga, T., Miyama, Y., Tamaoki, M. and Toba, M. (2016b) Life history and distribution of Nymphonella tapetis, a sea spider parasitic on the Manila clam, Ruditapes philippinarum in Tokyo Bay, Japan. Bulletin of Japan Fisheries Research and Education Agency 42, 94–95.Google Scholar
Yoshinaga, T. (2012) Works toward development of countermeasures against fish and shellfish parasitic diseases. Nippon Suisan Gakkaishi 78, 384–387. [In Japanese]CrossRefGoogle Scholar
Yoshinaga, T., Kobayashi, Y., Toba, M. and Miyama, Y. (2011) Development of a sensitive method for the detection of young larvae of the parasitic pycnogonid Nymphonella tapetis in Manila clam Ruditapes philippinarum. Fish Pathology 46, 38–41.CrossRefGoogle Scholar
Yoshinaga, T., Watanabe, S., Waki, T., Aoki, S. and Ogawa, K. (2010) Influence of Perkinsus infection on the physiology and behavior of adult Manila clam Ruditapes philippinarumi. Fish Pathology 45, 151–157. [In Japanese with English abstract].CrossRefGoogle Scholar