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Prevalence and patterns of infection by the epicaridean parasite, Gyge ovalis and the emergence of intersex in the estuarine mud shrimp, Upogebia major

Published online by Cambridge University Press:  07 November 2013

Jonathan P. Ubaldo ,
Takahiro Nanri ,
Yoshitake Takada  and
Masayuki Saigusa
Jonathan P. Ubaldo*
Affiliation:
Department of Biology, Faculty of Science, Okayama University, Tsushima 3-1-1, Okayama-Kitaku 700-8530, Japan
Takahiro Nanri
Affiliation:
Department of Biology, Faculty of Science, Okayama University, Tsushima 3-1-1, Okayama-Kitaku 700-8530, Japan
Yoshitake Takada
Affiliation:
Japan Sea National Fisheries Research Institute, Suido-cho 1-5939-22, Niigata 951-8121, Japan
Masayuki Saigusa
Affiliation:
Biodiversity Research Group, Green Planet, Tsushima-Naka 3-1-1, Okayama-Kitaku 700-8530, Japan
*
Correspondence should be addressed to: J.P. Ubaldo, Department of Biology, Faculty of Science, Okayama University, Tsushima 3-1-1, Okayama-Kitaku 700-8530, Japan email: [email protected]
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Abstract

A population of the mud shrimp, Upogebia major, inhabiting Kasaoka Inlet had a higher frequency of intersex males compared to other populations in the Seto Inland Sea, Japan. This population also featured a high prevalence of the branchial epicaridean parasite, Gyge ovalis, and inhabited a tidal flat characterized by increasingly softer sediments going into the lower tidal areas. We examined the rates at which infection co-occurred with intersex features and checked whether infection patterns varied with intersex occurrence according to host size and tidal level position. Fewer specimens were both intersex and infected than those having only one of either condition; infection was not a significant predictor of intersex. However, infection in young hosts that recovered from the parasite could be associated with the intersex morphologies and account for the majority of cases that were intersex but parasite-free. Deletions of the cuticular ridge (CRD) between the first and second abdominal segment and tidal level position were correlated with intersex. Lower tidal zone mud shrimp were, respectively, three and four times more likely to be intersex and exhibit CRD than those in the upper tidal zone. Potentially inclusive factors that may influence these trends are higher rates of early infection and increased exposure to sediment-bound pollutants in mud shrimp inhabiting the lower tidal areas.

Keywords

intersexUpogebia majormud shrimpfirst pleopodabnormal appendagesexual dimorphismGyge ovalishost–parasite interactionepicaridean parasite
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 3 , May 2014 , pp. 557 - 566
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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References

REFERENCES

An, J., Williams, J.D. and Yu, H. (2009) The Bopyridae (Crustacea: Isopoda) parasitic on thalassinideans (Crustacea: Decapoda) from China. Proceedings of the Biological Society of Washington 122, 225–246.Google Scholar
Anderson, G. (1990) Postinfection mortality of Palaemonetes spp. (Decapoda: Palaemonidae) following experimental exposure to the bopyrid isopod Probopyrus pandalicola (Packard) (Isopoda: Epicaridea). Journal of Crustacean Biology 10, 284–292.Google Scholar
Ayaki, T., Kawauchino, Y., Nishimura, C., Ishibashi, H. and Arizono, K. (2005) Sexual disruption in the freshwater crab (Geothelphusa dehaani). Integrative and Comparative Biology 45, 39–42.Google Scholar
Beck, J.T. (1980) Life history relationships between the bopyrid isopod, Probopyrus pandalicola, and one of its freshwater shrimp hosts, Palaemonetes paludosus. American Midland Naturalist 104, 135–154.Google Scholar
Bowen, S.T. and Hanson, J. (1962) Gynandromorph of brine shrimp, Artemia salina. Genetics 47, 227–230.Google Scholar
Boyko, C.B. and Williams, J.D. (2009) Crustacean parasites as phylogenetic indicators in decapod evolution. In Martin, J.W., Crandall, K.A. and Felder, D.L. (eds) Decapod crustacean phylogenetics. Crustacean Issues 18. Boca Raton, FL: CRC Press, pp. 197–220.CrossRefGoogle Scholar
Cash, C.E. and Bauer, R.T. (1993) Adaptations of the branchial ectoparasite Probopyrus pandalicola (Isopoda: Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio (Caridea: Palaemonidae). Journal of Crustacean Biology 13, 111–124.CrossRefGoogle Scholar
Conner, S.L. and Bauer, R.T. (2010) Infection of adult migratory river shrimps, Macrobrachium ohione, by the branchial bopyrid isopod Probopyrus pandalicola. Invertebrate Biology 129, 344–352.Google Scholar
Curtis, M.C. and Jones, C.M. (1995) Observation on monosex culture of redclaw crayfish Cherax quadricarinatus von Martens (Decapoda: Parastacidae) in earthen ponds. Journal of the World Aquaculture Society 26, 154–159.Google Scholar
Depledge, M.H. and Billinghurst, Z. (1999) Ecological significance of endocrine disruption in marine invertebrates. Marine Pollution Bulletin 39, 32–38.Google Scholar
Dumbauld, B.R., Chapman, J.W., Torchin, M.E. and Kuris, A.M. (2011) Is the collapse of mud shrimp (Upogebia pugettensis) populations along the Pacific coast of North America caused by outbreaks of a previously unknown bopyrid isopod parasite (Orthione griffenis)? Estuaries and Coasts 34, 336–350.Google Scholar
Dworschak, P.C. (1987) Feeding behaviour of Upogebia pusilla and Callianassa tyrrhena (Crustacea, Decapoda, Thalassinidea). Investigación Pesquera 51, 421–429.Google Scholar
Fantucci, M.Z., Biagi, R. and Mantelatto, F.L. (2007) Intersexuality in the western Atlantic hermit crab Isocheles sawayai (Anomura: Diogenidae). Marine Biodiversity Records 1, e68, 1–3.Google Scholar
Farmer, A.S. (1972) A bilateral gynandromorph of Nephrops norvegicus (L.) (Decapoda: Nephropidae). Marine Biology 15, 344–349.Google Scholar
Ford, A.T. (2012) Intersexuality in Crustacea: an environmental issue? Aquatic Toxicology 108, 125–129.CrossRefGoogle ScholarPubMed
Fukue, M., Sato, Y., Morinobu, S., Souji, N. and Yamasaki, S. (2003) Influence of contaminated sediments on Japanese horseshoe crab. Proceedings of the 2nd International Symposium on Contaminated Sediments, Quebec 26–28 May 2003, pp. 339–342.Google Scholar
Gusmão, L.F.M. and McKinnon, A.D. (2009) Sex ratios, intersexuality and sex change in copepods. Journal of Plankton Research 31, 1101–1117.Google Scholar
Harkey, G.A., Lydy, M.J., Kukkonen, J. and Landrum, P.F. (1994) Feeding selectivity and assimilation of PAH and PCB in Diporeia spp. Environmental Toxicology and Chemistry 13, 1445–1455.Google Scholar
Itani, G. (2004) Host specialization in symbiotic animals associated with thalassinidean shrimps in Japan. In Tamaki, A. (ed.) Proceedings of the symposium on ‘Ecology of large bioturbators in tidal flats and shallow sublittoral sediments—from individual behavior to their role as ecosystem engineers, 1–2 November 2003. Nagasaki: Nagasaki University, pp. 33–43.Google Scholar
Itow, T., Loveland, R.E. and Botton, M.L. (1998) Developmental abnormalities in horseshoe crab embryos caused by exposure to heavy metals. Archives of Environmental Contamination and Toxicology 35, 33–40.Google Scholar
Johnson, T.P. and Otto, S.V. (1981) Histology of a bilateral gynadromorph of the blue crab Callinectes sapidus Rathbun (Decapoda: Portunidae). Biological Bulletin. Marine Biological Laboratory, Woods Hole 161, 236–245.CrossRefGoogle Scholar
Juchault, P., Louis, C., Martin, G. and Noulin, G. (1991) Masculinization of female isopods (Crustacea) correlated with non-mendelian inheritance of cytoplasmic viruses. Proceedings of the National Academy of Sciences of the United States of America 88, 10460–10464.Google Scholar
Kelly, A., Hatcher, M.J. and Dunn, A.M. (2004) Intersexuality in the amphipod Gammarus duebeni results from incomplete feminisation by the vertically transmitted parasitic sex ratio distorter Nosema granulosis. Evolutionary Ecology 18, 121–132.Google Scholar
Kinoshita, K., Wada, M., Kogure, K. and Furota, T. (2003) Mud shrimp burrows as dynamic traps and processors of tidal-flat materials. Marine Ecology Progress Series 247, 159–164.Google Scholar
Langston, W.J. and Pope, N.D. (1995) Determinants of TBT adsorption and desorption in estuarine sediments. Marine Pollution Bulletin 31, 32–43.CrossRefGoogle Scholar
LeBlanc, G.A. (2007) Crustacean endocrine toxicology: a review. Ecotoxicology 16, 61–81.Google Scholar
Lee, S.J., Kim, J.H., Chang, Y.S. and Moon, M.H. (2006) Characterization of polychlorinated dibenzo-p-dioxins and dibenzofurans in different particle size fractions of marine sediments. Environmental Pollution 144, 554–561.Google Scholar
Markham, J.C. (2001) A review of the bopyrid isopods parasitic on thalassinidean decapods. In Kensley, B. and Brusca, R.C. (eds) Isopod systematics and evolution. Crustacean Issues 13. Boca Raton, FL: CRC Press, pp. 195–204.Google Scholar
Mitchell, S.E. (2001) Intersex and male development in Daphnia magna. Hydrobiologia 442, 145–156.Google Scholar
Moore, C.G. and Stevenson, J.M. (1991) The occurrence of intersexuality in harpacticoid copepods and its relationship with pollution. Marine Pollution Bulletin 22, 72–74.Google Scholar
Mukai, H. and Koike, I. (1984) Behavior and respiration of the burrowing shrimps Upogebia major (De Haan) and Callianassa japonica (De Haan). Journal of Crustacean Biology 4, 191–200.Google Scholar
Nanri, T., Fukushige, M., Ubaldo, J.P., Kang, B.J., Masunari, N., Takada, Y., Hatakeyama, M. and Saigusa, M. (2011) Occurrence of abnormal sexual dimorphic structures in the gonochoristic crustacean, Upogebia major (Thalassinidea: Decapoda) inhabiting mud tidal flats in Japan. Journal of the Marine Biological Association of the United Kingdom 91, 1049–1057.Google Scholar
O'Brien, J. and Van Wyk, P.M. (1985) Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. In Wenner, A.M. (ed.) Crustacean Issues 3: Factors in adult growth. Rotterdam: A.A. Balkema, pp. 191–218.Google Scholar
Olmstead, A.W. and LeBlanc, G.A. (2007) The environmental–endocrine basis of gynandromorphism (intersex) in a crustacean. International Journal of Biological Sciences 3, 77–84.Google Scholar
Pike, R.B. (1960) The biology and post-larval development of the bopyrid parasites Pseudione affinis G.O. Sars and Hemiarthrus abdominalis (Kröyer) [=Phryxus abdominalis Kröyer]. Journal of the Linnaean Society of London, Zoology 44, 239–251.Google Scholar
Pinn, E.H., Atkinson, R.J.A. and Rogerson, A. (1998) Particle size selectivity and resource partitioning in five species of Thalassinidea (Crustacea: Decapoda). Marine Ecology Progress Series 169, 243–250.Google Scholar
Pinn, E.H., Atkinson, R.J.A. and Rogerson, A. (2001) Sexual dimorphism and intersexuality in Upogebia stellata (Crustacea: Decapoda: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom 81, 1061–1062.Google Scholar
Rasband, W.S. (1997–2012) ImageJ, US National Institutes of Health, Bethesda, MD. Available at: http://imagej.nih.gov/ij/ (accessed 8 October 2013).Google Scholar
Reinhard, E.G. (1956) Parasitic castration of Crustacea. Parasitology 5, 79–107.Google Scholar
Repetto, M. and Griffen, B.D. (2012) Physiological consequences of parasite infection in the burrowing mud shrimp, Upogebia pugettensis, a widespread ecosystem engineer. Marine and Freshwater Research 63, 60–67.Google Scholar
Rigaud, T. and Juchault, P. (1998) Sterile intersexuality in an isopod induced by the interaction between a bacterium (Wolbachia) and the environment. Canadian Journal of Zoology 76, 493–499.Google Scholar
Rudolph, E., Verdi, A. and Tapia, J. (2001) Intersexuality in the burrowing crayfish Parastacus varicosus Faxon, 1898 (Decapoda, Parastacidae). Crustaceana 74, 27–37.Google Scholar
Rudolph, E.H. (2002) New records of intersexuality in the freshwater crayfish Samastacus spinifrons (Decapoda, Parastacidae). Journal of Crustacean Biology 22, 377–389.Google Scholar
Sagi, A., Khalaila, I., Barki, A., Hulata, G. and Karplus, I. (1996) Intersex red claw crayfish, Cherax quadricarinatus (von Martens): functional males with pre-vitellogenic ovaries. Biological Bulletin. Marine Biological Laboratory, Woods Hole 190, 16–23.Google Scholar
Shiino, S.M. (1939) Bopyrids from Kyusyu and Ryukyu. Records of Oceanographic Works in Japan 10, 79–99.Google Scholar
Smith, A.E., Chapman, J.W., and Dumbauld, B.R. (2008) Population structure and energetics of the bopyrid isopod parasite, Orthione griffenis in mud shrimp, Upogebia pugettensis. Journal of Crustacean Biology 28, 228–233.Google Scholar
Takahashi, T., Araki, A., Nomura, Y., Koga, M. and Arizono, K. (2000) The occurrence of dual-gender imposex in Japanese freshwater crab. Journal of Health Science 46, 376–379.Google Scholar
Tucker, B.W. (1930) On the effects of an epicaridean parasite, Gyge branchialis, on Upogebia littoralis. Quarterly Journal of Microscopical Science 74, 1–118.Google Scholar
Tunberg, B. (1986) Studies on the population ecology of Upogebia deltaura (Leach) (Crustacea, Thalassinidea). Estuarine, Coastal and Shelf Science 22, 753–765.Google Scholar
Turra, A. (2004) Intersexuality in hermit crabs: reproductive role and fate of gonopores in intersex individuals. Journal of the Marine Biological Association of the United Kingdom 84, 757–759.CrossRefGoogle Scholar
Weis, J.S. and Kim, K. (1988) Tributyltin is a teratogen in producing deformities in limbs of the fiddler crab, Uca pugilator. Archives of Environmental Contamination and Toxicology 17, 583–587.Google Scholar
Yang, G., Short, S., Kille, P. and Ford, A.T. (2011) Microsporidia infections in the amphipod, Echinogammarus marinus (Leach): suggestions of varying causal mechanisms to intersexuality. Marine Biology 158, 461–470.Google Scholar
Zou, E. and Fingerman, M. (2000) External features of an intersex fiddler crab, Uca pugilator (Bosc, 1802) (Decapoda, Brachyura). Crustaceana 73, 417–423.Google Scholar