Skip to main content

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

  • Katsumasa Yamada (a1), Katsumi Miyazaki (a2), Takeshi Tomiyama (a3), Gen Kanaya (a4), Yoshifumi Miyama (a5), Tomoyoshi Yoshinaga (a6), Kunihiro Wakui (a7), Masanori Tamaoki (a4) and Mitsuharu Toba (a8)...

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.

Corresponding author
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:
Hide All
Adler, F.R. and Kretzschmar, M. (1992) Aggregation and stability in parasite-host models. Parasitology 104, 199205.
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, 467484.
Anderson, R.M. and May, R.M. (1978) Regulation and stability of hostparasite population interactions, I: regulatory processes. Journal of Animal Ecology 47, 219247.
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, 895902. [In Japanese with English abstract].
Cox, D.R. (1972) Regression models and life tables. Journal of the Royal Statistical Society B 34, 187202.
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, 109117.
Hudson, P.J., Dobson, A.P. and Newborn, D. (1998) Prevention of population cycles by parasite removal. Science 282, 22562258.
Kikuchi, T. (1976) Rediscovery of the bivalve-infesting pycnogonid, Nymphonella tapetis Ohshima 1927, in Amakusa. Publications from the Amakusa Marine Biological Laboratory 4, 5156.
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, 281313.
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, 4554. [In Japanese with English abstract]
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, 491494.
Møller, A.P. (2000) Survival and reproductive rate of mites in relation to resistance of their barn swallow hosts. Oecologia 124, 351357.
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, 183190. [In Japanese with English abstract]
Nakamura, Y. (2004) Suspension feeding and growth of juvenile Manila clam Ruditapes philippinarum reared in the laboratory. Fisheries Science 70, 215222.
Ogawa, K. and Matsuzaki, K. (1985) Discovery of bivalve-infesting Pycnogonida, Nymphonella tapetis, in a new host, Hiatella orientalis . Zoological Science 2, 583589.
Ohshima, H. (1927) Nymphonella tapetis, ng, n. sp., a pycnogon parasitic in a bivalve. Annotationes Zoologicæ Japonenses 11, 257263.
Ohshima, H. (1933) The adult of the bivalve-infesting pycnogonid, Nymphonella tapetis Ohshima. Annotationes Zoologicæ Japonenses 14, 5360.
Ohshima, H. (1935) A further note on Nymphonella tapetis: the egg-carrying mature male (Eurycydidae: Pantopoda). Annotationes Zoologicæ Japonenses 15, 95102.
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.
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, 921.
Toba, M. and Miyama, Y. (1991) Gonadal development and spawning induction in artificially conditioned manila clams Ruditapes philippinarum . Nippon Suisan Gakkaishi 57, 12691275. [In Japanese]
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, 1526.
Tompkins, D.M. and Begon, M.E. (1999) Parasites can regulate wildlife populations. Parasitology Today 15, 311313.
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, 779786.
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, 689701. [In Japanese with English abstract]
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, 408418.
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, 4956.
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, 9495.
Yoshinaga, T. (2012) Works toward development of countermeasures against fish and shellfish parasitic diseases. Nippon Suisan Gakkaishi 78, 384387. [In Japanese]
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, 3841.
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, 151157. [In Japanese with English abstract].
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the Marine Biological Association of the United Kingdom
  • ISSN: 0025-3154
  • EISSN: 1469-7769
  • URL: /core/journals/journal-of-the-marine-biological-association-of-the-united-kingdom
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 7
Total number of PDF views: 36 *
Loading metrics...

Abstract views

Total abstract views: 461 *
Loading metrics...

* Views captured on Cambridge Core between 14th March 2017 - 19th April 2018. This data will be updated every 24 hours.