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Effects of a crustacean parasite and hyperparasite on the Japanese spiny oyster Saccostrea kegaki

Abstract

Parasitism is one of the most common interspecific interactions, but little information exists on the detailed relationships among hosts, parasites, and hyperparasites (secondary parasites) in marine ecosystems. Pea crabs parasitize a wide variety of marine animals, and the crabs themselves are often parasitized by other animals. The present study investigated the relationships among the oyster Saccostrea kegaki, its parasite, the pea crab Pinnotheres boninensis, and a hyperparasite, the isopod Onychocepon resupinum. Field sampling was conducted during the oyster’s reproductive season (June–September 2014 and 2015) to evaluate effects of the pea crab on the body weight, maturation, and sex of the oyster in western Japan (Banshozaki, Shirahama Town, Wakayama Pref.; 33.41°N, 135.20°E). The relationship between the pea crab and the isopod and indirect effects of the isopod on the oyster were also investigated. The pea crab reduced the oyster’s body weight and affected its reproduction: the proportion of mature individuals was lower in infested oysters (39.1%) than in non-infested ones (86.2%). The isopod affected the crab’s sexual characteristics: infested female crabs had poorly developed ovaries, and infested males showed degrees of feminization and increased body size. The prevalence of the isopod was much higher in male (47.1%) than female (6.4%) crabs inside the oyster shells, suggesting that the parasitized male crabs became larger and were forced to remain inside the shells. Therefore, the isopod appears to have an indirect negative impact on the oyster by changing the male crab’s traits.

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References

  • Abrams PA, Menge BA, Mittelbach GG, Spiller DA, Yodzis P (1996) The role of indirect effects in food webs. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics. Chapman & Hall, New York, pp 371–395

    Chapter  Google Scholar 

  • Amemiya I (1931) Aquatic animal: Oyster reproduction. Iwanami Shoten Publishers, Tokyo (in Japanese)

    Google Scholar 

  • Asama H, Yamaoka K (2009) Life history of the pea crab, Pinnotheres sinensis, in terms of infestation in the bivalve mollusc, Septifer virgatus. Mar Biodivers Rec 2:e77. doi:10.1017/S1755267209000621

    Article  Google Scholar 

  • Atkins D (1926) The moulting stages of the pea-crab (Pinnotheres pisum). J Mar Biol Assoc UK 14:475–493. doi:10.1017/S0025315400007955

    Article  Google Scholar 

  • Awati PR, Rai HS (1931) Ostrea cucullata (the Bombay oyster). Methodist Publishing House, Lucknow

    Google Scholar 

  • Chaparro OR, Thompson RJ, Pereda SV (2002) Feeding mechanisms in the gastropod Crepidula fecunda. Mar Ecol Prog Ser 234:171–181

    Article  Google Scholar 

  • Christensen AM, McDermott JJ (1958) Life-history and biology of the oyster crab, Pinnotheres ostreum Say. Biol Bull 114:146–179. doi:10.2307/1538845

    Article  Google Scholar 

  • Coe WR (1943) Sexual differentiation in mollusks. I. Pelecypods. Q Rev Biol 18:154–164. doi:10.1086/394673

    Article  Google Scholar 

  • Freeman M (2005) Marine hyperparasites. In: Rohde K (ed) Marine parasitology. CSIRO Publishing, Collingwood, pp 293–298

    Google Scholar 

  • Griffen BD (2009) Effects of a newly invasive parasite on the burrowing mud shrimp, a widespread ecosystem engineer. Mar Ecol Prog Ser 391:73–83

    Article  Google Scholar 

  • Haven D (1959) Effects of pea crabs, Pinnotheres ostreum, on oysters, Crassostrea virginica. Proc Nat Shellfish Assoc 49:77–86

    Google Scholar 

  • Janssen HH, Brandt A (1994) Heterocepon marginatum Shiino, 1936, (Crustacea: Isopoda: Epicaridea: Bopyridae), a new hyperparasite from the Philippines, and a short review of the biology of the bopyridae. Philipp Sci 31:5–31

    Google Scholar 

  • Konishi K (1977) On three species of the pinnotherid crabs from Hokkaido, Japan. J Fac Sci Hokkaido Univ (VI) 20:605–610

    Google Scholar 

  • Lafferty KD, Kuris AM (2012) Ecological consequences of manipulative parasites. In: Hughes DP, Brodeur J, Thomas F (eds) Host manipulation by parasites. Oxford University Press, Oxford, pp 158–168

    Chapter  Google Scholar 

  • Lauckner G (1983) Diseases of Mollusca: Bivalvia. In: Kinne O (ed) Diseases of marine animals, vol II. Biologische Anstalt Helgoland, Hamburg, pp 477–961

    Google Scholar 

  • Longshaw M, Feist SW, Bateman KS (2012) Parasites and pathogens of the endosymbiotic pea crab (Pinnotheres pisum) from blue mussels (Mytilus edulis) in England. J Invertebr Pathol 109:235–242. doi:10.1016/j.jip.2011.11.011

    Article  Google Scholar 

  • McDermott JJ (2009) Hypersymbioses in the pinnotherid crabs (Decapoda: Brachyura: Pinnotheridae): a review. J Nat Hist 43:785–805. doi:10.1080/00222930802702480

    Article  Google Scholar 

  • Morita S (1952) The effects of epicaridization on the external characters of a Pinnotherid crab (Pinnotheres cardii Buerger). Dobutsugaku Zasshi 61:22–26 (in Japanese with English abstract)

    Google Scholar 

  • Morita S (1953) On the life-cycle of a bopyrid, Heterocepon marginatum Shiino. Sci Bull Fac Lib Arts Educ Nagasaki Univ 3:14–20 (in Japanese with English abstract)

    Google Scholar 

  • Narvarte MA, Saiz MN (2004) Effects of the pinnotherid crab Tumidotheres maculatus on the Tehuelche scallop Aequipecten tehuelchus in the San Matıas Gulf, Argentina. Fish Res 67:207–214. doi:10.1016/j.fishres.2003.09.041

    Article  Google Scholar 

  • O’Beirn FX, Walker RL (1999) Pea crab, Pinnotheres ostreum Say, 1817, in the eastern oyster, Crassostrea virginica (Gmelin, 1791): prevalence and apparent adverse effects on oyster gonad development. Veliger 42:17–20

    Google Scholar 

  • Ocampo EH, Nuñez JD, Cledón M, Baeza JA (2014) Parasitic castration in slipper limpets infested by the symbiotic crab Calyptraeotheres garthi. Mar Biol 161:2107–2120. doi:10.1007/s00227-014-2490-y

    Article  Google Scholar 

  • Owens L (1993) Prevalence of Cabirops orbionei (Epicaridea; Cryptoniscidae) in northern Australia: a biocontrol agent for bopyrids. Mar Freshw Res 44:381–387. doi:10.1071/MF9930381

    Article  Google Scholar 

  • Page RDM (1985) Review of the New Zealand Bopyridae (Crustacea: Isopoda: Epicaridea). N Z J Zool 12:185–212. doi:10.1080/03014223.1985.10428279

    Article  Google Scholar 

  • Rohde K (1993) Ecology of marine parasites: an introduction to marine parasitology, 2nd edn. CAB International, Wallingford

    Google Scholar 

  • Saito N (2002) A list of crustacean hosts of the epicaridean isopods (Crustacea: Peracarida) in the Japanese waters. Taxa Proc Jpn Soc Syst Zool 13:18–31 (in Japanese with English abstract)

    Google Scholar 

  • Sandoz M, Hopkins SH (1947) Early life history of the oyster crab, Pinnotheres ostreum (Say). Biol Bull 93:250–258. doi:10.2307/1537973

    CAS  Article  Google Scholar 

  • Schmitt WL, McCain JC, Davidson ES (1973) Decapoda I, Brachyura I, family Pinnotheridae. In: Gruner HE, Holthuis LB (eds) Crustaceorum catalogus. Dr. W. Junk BV, Den Haag, pp 1–160

    Google Scholar 

  • Seto Marine Biological Laboratory (2015) Water temperature at the Aquarium: 2014. Annual Reports Seto Marine Biological Laboratory, Kyoto University 28:13

  • Shields JD, Gómez-Gutiérrez J (1996) Oculophryxus bicaulis, a new genus and species of dajid isopod parasitic on the euphausiid Stylocheiron affine Hansen. Int J Parasitol 26:261–268. doi:10.1016/0020-7519(95)00126-3

    CAS  Article  Google Scholar 

  • Shields JD, Boyko CB, Williams JD (2015) Chapter 71–12 Parasites and pathogens of Brachyura. In: Castro P, Davie PJF, Guinot D, Schram FR, von Vaupel Klein JC (eds) The Crustacea. Treatise on zoology/traite de zoologie, vol 9B, Brill, Leiden, pp 639–774

  • Shiino SM (1936) Bopyrids from Tanabe Bay, III. Mem Coll Sci Kyoto Imp Univ (B) 11:157–174

    Google Scholar 

  • Soong K (1997) Some life history observations on the pea crab, Pinnotheres tsingtaoensis, symbiotic with the bivalve mollusk, Sanguinolaria acuta. Crustaceana 70:855–866. doi:10.1163/156854097X00474

    Article  Google Scholar 

  • Stauber LA (1945) Pinnotheres ostreum, parasitic on the American oyster, Ostrea (Gryphaea) virginica. Biol Bull 88:269–291. doi:10.2307/1538315

    Article  Google Scholar 

  • Stimpson W (1858) Prodromus descriptionis animalium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republica Federata missa, Cadwaladaro Ringgold et Johanne Rodgers Ducibus, observavit et descripsit W. Stimpson, Pars V. Crustacea Ocypodoidea. Proc Acad Nat Sci Phila 10:93–110

    Google Scholar 

  • Suzuki H (1967) An intersex found in a male of the pea crab, Pinnotheres sinensis. Shen Res Crustac Tokyo 3:52–60 (in Japanese with English abstract)

    Google Scholar 

  • Suzuki H (1972) Freshwater and commensal crustacean decapods from the Bonin Islands. Sci Rep Yokohama Natl Univ Sect II Biol Geol Sci 19:1–26

    CAS  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Torigoe K, Inaba A (1981) On the scientific name of Japanese spiny oyster “Kegaki”. Venus 40:126–134

    Google Scholar 

  • Trottier O, Walker D, Jeffs AG (2012) Impact of the parasitic pea crab Pinnotheres novaezelandiae on aquacultured New Zealand green-lipped mussels, Perna canaliculus. Aquaculture 344:23–28. doi:10.1016/j.aquaculture.2012.02.031

    Article  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Matassa CM (2006) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252. doi:10.1111/j.1461-0248.2006.00981.x

    Article  Google Scholar 

  • Williams JD, Boyko CB (2012) The global diversity of parasitic isopods associated with crustacean hosts (Isopoda: Bopyroidea and Cryptoniscoidea). PLoS One 7:e35350. doi:10.1371/journal.pone.0035350

    CAS  Article  Google Scholar 

  • Yamada C, Itani G, Asama H (2009) Utilization of the non-indigenous green mussel, Perna viridis, by the native pinnotherid crab Arcotheres sinensis in Uranouchi Inlet, Kochi, Japan. Crustac Res 38:70–76

    Article  Google Scholar 

  • Yasuoka N, Yusa Y (2016) Effects of size and gregariousness on individual sex in a natural population of the Pacific oyster Crassostrea gigas. J Molluscan Stud 82:485–491. doi:10.1093/mollus/eyw020

    Article  Google Scholar 

  • Yasuoka N, Yusa Y (2017) Direct evidence of bi-directional sex change in natural populations of the oysters Saccostrea kegaki and S. mordax. Plankton Benthos Res 12:1–4

    Article  Google Scholar 

  • Yoo M, Kajihara T (1985) The effect of the pea carb [sic] Pinnotheres pholadis on the reproductive capacity of the blue mussel Mytilus edulis galloprovincialis. Bull Korean Fish Soc 18:581–585

    Google Scholar 

Download references

Acknowledgements

We thank Dr. Keiji Wada, Dr. Hiroaki Sato, and Dr. Gyo Itani for their valuable advice and support for this study. We also thank the anonymous reviewer for highly constructive comments, and the members of our laboratory and Seto Marine Biological Laboratory of Kyoto University for discussion and assistance.

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Correspondence to Noriko Yasuoka.

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Yasuoka, N., Yusa, Y. Effects of a crustacean parasite and hyperparasite on the Japanese spiny oyster Saccostrea kegaki . Mar Biol 164, 217 (2017). https://doi.org/10.1007/s00227-017-3250-6

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