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Variations in eastern oyster (Crassostrea virginica) sex-ratios from three Virginia estuaries: protandry, growth and demographics

Published online by Cambridge University Press:  01 May 2012

Juliana M. Harding*
Affiliation:
Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA, USA23062
Eric N. Powell
Affiliation:
Haskin Shellfish Research Laboratory, Rutgers University, 6959 Miller Avenue, Port Norris, NJ, USA08349
Roger Mann
Affiliation:
Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA, USA23062
Melissa J. Southworth
Affiliation:
Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, VA, USA23062
*
Correspondence should be addressed to: J.M. Harding, Department of Marine Science, Coastal Carolina University, Conway, SC, USA29528, email: [email protected]

Abstract

Oyster population reproductive capacity and dynamics are controlled at the most basic level by the observed sex-ratios. Since oysters are sequential, protandric hermaphrodites the population sex-ratio is related to the demographics (shell length, age, and biomass). Oysters were collected from June through to August 2008 at twelve bars in the James, Rappahannock and Great Wicomico Rivers, Virginia, USA. Bars were aggregated into five groups on the basis of similar age–length relationships. Sex-ratios (fraction female), age–length, and biomass–length relationships were determined for each group. The fraction female increased within increasing shell length, age, and biomass at all sites. Simultaneous hermaphrodites were rarely observed. Group specific differences in shell length (SL, mm) and age (yr) for the timing of the protandric shift were observed with the earliest shift from male to female occurring at ~60 mm SL and ~1.6 yr. The proportion of females observed in the larger or older individuals was at least 70–80%. Sex-ratios from summer 2008 were used to develop sex–length, sex–age, and sex–biomass keys that were applied to autumn-survey data from 2006, 2007, 2008 and 2009. In these years, sex-ratios by shell length and age were strongly biased towards males while the sex-ratio by biomass was strongly biased towards females. Disease mortality compounds natural and fishing mortality resulting in age/size specific cropping yielding truncated population demographics and an earlier protandric shift in populations on the extremes of the range examined. Regardless of location, market (>76 mm SL) oysters are predominantly female.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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Footnotes

2

Current address: Department of Marine Science, Coastal Carolina University, Conway, SC, USA 29528

References

REFERENCES

Andrews, J.D. (1968) Oyster mortality studies in Virginia. VII. Review of the epizootiology and origin of Minchinia nelsoni . Proceedings of the National Shellfisheries Association 58, 2336.Google Scholar
Andrews, J.D. (1979) Pelecypoda: Ostreidae. In Giese, A.C. and Pearse, J.S. (eds) Reproduction of marine invertebrates. New York: Academic Press, pp. 293341.CrossRefGoogle Scholar
Andrews, J.D. (1988) Epizootiology of the disease caused by the oyster pathogen Perkinsus marinus and its effects on the oyster industry. American Fisheries Society Special Publication 18, 4763.Google Scholar
Andrews, J.D. (1996) History of Perkinsus marinus, a pathogen of oysters in Chesapeake Bay 1950–1984. Journal of Shellfish Research 15, 1316.Google Scholar
Andrews, J.D. and Wood, J.L. (1967) Oyster mortality studies in Virginia. VI. History and distribution of Minchinia nelsoni, a pathogen of oysters in Virginia. Chesapeake Science 8, 113.CrossRefGoogle Scholar
Asif, M. (1979) Hermaphroditism and sex reversal in the four common oviparous species of oysters from the coast of Karachi. Hydrobiologia 66, 4955.Google Scholar
Bahr, L. and Lanier, W. (1981) The ecology of intertidal oyster reefs of the South Atlantic coast: a community profile. US Fish and Wildlife Service, Washington, DC FWS/OBS-81/15, 105 pp.Google Scholar
Barber, B., Ford, S. and Haskin, H. (1988) Effects of the parasite MSX (Haplosporidium nelsoni) on oyster (Crassostrea virginia) energy metabolism I. Condition index and relative fecundity. Journal of Shellfish Research 7, 2531.Google Scholar
Barot, S., Heino, M., O'Brien, L. and Dieckmann, U. (2004) Long-term trend in the maturation reaction norm of two cod stocks. Ecological Applications 14, 12571271.Google Scholar
Bhattacharya, C.G. (1967) A simple method of resolution of a distribution into Gaussian components. Biometrics 23, 115135.Google Scholar
Burkenroad, M. (1931) Sex in the Louisiana oyster Ostrea virginica . Science 74, 7172.Google Scholar
Buroker, N. (1983) Sexuality with respect to shell length and group size in the Japanese oyster Crassostrea gigas . Malacalogia 23, 271279.Google Scholar
Burreson, E.M. and Ragone Calvo, L.M. (1996) Epizootiology of Perkinsus marinus disease of oysters in the Chesapeake Bay with emphasis on data since 1985. Journal of Shellfish Research 15, 1734.Google Scholar
Butler, P. (1952) Growth and mortality rates in sibling and unrelated oyster populations. Proceedings of the Gulf and Caribbean Fisheries Institute 4, 71.Google Scholar
Buxton, C. (1993) Life history changes in exploited reef fishes on the east coast of South Africa. Environmental Biology of Fishes 36, 4763.Google Scholar
Carnegie, R. and Burreson, E.M. (2009) Status of the major oyster diseases in Virginia 2006–2008: a summary of the annual oyster disease monitoring program. Virginia Institute of Marine Science Report, Gloucester Point, Virginia, 20 pp.Google Scholar
Carriker, M. and Gaffney, P. (1996) A catalogue of selected species of living oysters. In Kennedy, V., Newell, R. and Eble, A. (eds) The eastern oyster Crassostrea virginica . College Park, MD: Maryland Sea Grant College, pp. 118.Google Scholar
Coe, W. (1936) Sex ratios and sex changes in mollusks. Memoirs of the Royal Museum of Natural History Belgium 3, 6976.Google Scholar
Coe, W. (1943) Sexual differentiation in mollusks. I. Pelecypods. Quarterly Review of Biology 18, 154164.Google Scholar
Comfort, A. (1957) The duration of life in mollusks. Proceedings of the Malacological Society of London 32, 219241.Google Scholar
Conover, W.J. (1980) Practical non-parametric statistics. New York; John Wiley and Sons, 493 pp.Google Scholar
Cook, T., Folli, M., Klinck, J., Ford, S. and Miller, J. (1998) The relationship between increasing sea surface temperatures and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuarine, Coastal and Shelf Science 46, 587597.CrossRefGoogle Scholar
Cox, C. and Mann, R. (1992) Temporal and spatial changes in fecundity of eastern oysters Crassostrea virginica (Gmelin 1791) in the James River, Virginia. Journal of Shellfish Research 11, 4954.Google Scholar
Dame, R.F., Zingmark, R.G. and Haskin, E. (1984) Oyster reefs as processors of estuarine materials. Journal of Experimental Marine Biology and Ecology 83, 239247.Google Scholar
Dinamani, P. (1974) Reproductive cycle and gonadial changes in the New Zealand rock oyster Crassotrea glomerata . New Zealand Journal of Marine and Freshwater Research 8, 3965.Google Scholar
Galtsoff, P. (1964) The American oyster Crassostrea virginica Gmelin. US Fish and Wildlife Service Fisheries Bulletin 64, 480 pp.Google Scholar
Gunter, G. (1950) Seasonal population changes and distributions as related to salinity of certain invertebrates of the Texas coast, including the commercial shrimp. Publications of the Institute of Marine Science, University of Texas 1, 751.Google Scholar
Guo, X., Hedgecock, D., Herhberger, W., Cooper, K. and Allen, S.K. Jr (1998) Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution 52, 394402.Google Scholar
Harding, J.M. and Mann, R. (1999) Observations on the biology of the veined rapa whelk, Rapana venosa (Valenciennes, 1846) in the Chesapeake Bay. Journal of Shellfish Research 18, 918.Google Scholar
Harding, J.M and Mann, R. (2005) Veined rapa whelk Rapana venosa range extensions in Virginia waters of Chesapeake Bay, USA. Journal of Shellfish Research 24, 381385.Google Scholar
Harding, J.M., Mann, R. and Southworth, M.J. (2008) Shell length-at-age relationships in James River oysters (Crassostrea virginica) collected four centuries apart. Journal of Shellfish Research 27, 11091115.Google Scholar
Harding, J.M., Mann, R., Southworth, M.J. and Wesson, J.A. (2010) Management of the Piankatank River, Virginia in support of oyster (Crassostrea virginica, Gmelin 1791) fishery repletion. Journal of Shellfish Research 29, 867888.Google Scholar
Hargis, W.J. Jr (1999) The evolution of the Chesapeake oyster reef system during the Holocene Epoch. In Luckenbach, M.W., Mann, R. and Wesson, J.A. (eds) Oyster reef habitat restoration: a synopsis of approaches. Gloucester Point, VA: Virginia Institute of Marine Science, pp. 524.Google Scholar
Haven, D.S., Hargis, W.J. Jr and Kendall, P. (1978) The oyster industry of Virginia: its status, problems, and promise. Virginia Institute of Marine Science Special Papers in Marine Science No. 4, Gloucester Point, Virginia, 1024 pp.Google Scholar
Haven, D.S. and Whitcomb, J.P. (1986) The public oyster bottoms in Virginia: an overview of their size, location, and productivity. American Malacological Bulletin Special Edition No 3, 1723 Google Scholar
Hayes, P. and Menzel, R. (1981) The reproductive cycle of early setting Crassostrea virginica (Gmelin) in the northeast Gulf of Mexico, and its implications for population recruitment. Biologial Bulletin . Marine Biological Laboratory, Woods Hole 160, 8088.Google Scholar
Heffernan, P., Walker, R. and Carr, J. (1989) Gametogeneic cycle of three marine bivalves in Wassaw Sound, Georgia. II. Crassostrea virginica (Gmelin, 1791). Journal of Shellfish Research 8, 6170.Google Scholar
Kennedy, V. (1983) Sex ratios in oysters, emphasizing Crassotrea virginica from Chesapeake Bay, Maryland. Veliger 25, 329338.Google Scholar
Kennedy, V. (1996) The ecological role of the eastern oyster, Crassostrea virginica, with remarks on disease. Journal of Shellfish Research 15, 177183.Google Scholar
Kennedy, V., Newell, R., Krantz, G. and Otto, S. (1995) Reproductive capacity of the eastern oyster, Crassostrea virginica, infected with the parasite Perkinsus marinus . Diseases of Aquatic Organisms 23, 135144.Google Scholar
Kirby, M.X. (2000) Paleoecological differences between Tertiary and Quaternary Crassostrea oysters, as revealed by stable isotope sclerochronology. Palaios 15, 132141.Google Scholar
Krebs, C. (1989) Ecological methodology. New York: Harper Collins Publishers, Inc., 654 pp.Google Scholar
Law, R. and Grey, D. (1989) Evolution of yields from populations with age-specific cropping. Evolutionary Ecology 3, 343359.Google Scholar
Mann, R., Rainer, J.S. and Morales-Alamo, R. (1994) Reproductive activity of oysters, Crassostrea virginica (Gmelin, 1791) in the James River, Virginia, during 1987–1988. Journal of Shellfish Research 13, 157164.Google Scholar
Mann, R. and Evans, D.A. (1998) Estimation of oyster, Crassostrea virginica, standing stock, larval production and advective loss in relation to observed recruitment in the James River, Virginia. Journal of Shellfish Research 17, 239254.Google Scholar
Mann, R., Southworth, M.J., Harding, J.M. and Wesson, J.A. (2009a) Population studies of the native oyster, Crassostrea virginica (Gmelin), in the James River, Virginia, USA. Journal of Shellfish Research 28, 193220.Google Scholar
Mann, R., Harding, J.M. and Southworth, M.J. (2009b) Reconstructing pre-colonial oyster demographics in the Chesapeake Bay, USA. Estuarine, Coastal and Shelf Science 85, 217222.Google Scholar
Menzel, R.W. (1951) Early sexual development and growth of the American oyster in Louisiana waters. Science 113, 719721.Google Scholar
Morbrey, Y. and Abrams, P. (2004) The interaction between reproductive lifespan and protandry in seasonal breeders. Journal of Evolutionary Biology 17, 768778.Google Scholar
Moore, H.F. (1897) Oysters and methods of oyster culture. Report of the US Commission of Fish and Fisheries, pp. 263340.Google Scholar
Newell, R. (1988) Ecological changes in Chesapeake Bay: are they the result of overharvesting the American oyster, Crassostrea virginica? In Lynch, M.P. and Mihursky, J.A. (eds) Understanding the estuary: advances in Chesapeake Bay research. Chesapeake Bay Research Consortium Publication 129, pp. 536546.Google Scholar
Noreen, E.W. (1989) Computer-intensive methods for testing hypotheses: an introduction. New York: John Wiley and Sons.Google Scholar
O'Beirn, F.X., Walker, R.L. and Jansen, M. (1998) Microgeographical variations in gametogenesis and sex ratios in the eastern oyster at two marsh sites in Georgia. Transactions of the American Fisheries Society 127, 298308.Google Scholar
Olsen, E., Helme, M., Lilly, G., Morgan, M., Brattey, J., Ernande, B. and Dieckmann, U. (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428, 932935.Google Scholar
Paniagua-Chavez, C. and Acosta-Ruiz, M. (1995) Gonadal development of Crassostrea gigas in Bahia San Quintin, Baja, California, Mexico. Ciencias Marinas 20, 225242.CrossRefGoogle Scholar
Paynter, K. (1996) The effects of Perkinsus marinus infection on physiological processes in the eastern oyster, Crassostrea virginica . Journal of Shellfish Research 15, 119125.Google Scholar
Perharda, M., Mladineo, I., Bolotin, J., Kekez, L. and Skaramuca, B. (2006) The reproductive cycle and potential protandric development of the Noah's Ark Shell, Arca noae L.: implications for aquaculture. Aquaculture 252, 317327.Google Scholar
Powell, E.N. and Cummins, H. (1985) Are molluscan maximum life spans determined by long-term cycles in benthic communities? Oecologia 67, 177182.Google Scholar
Powell, E.N., Kraeuter, J.N. and Ashton-Alcox, K.A. (2006) How long does oyster shell last on an oyster reef? Estuarine, Coastal and Shelf Science 69, 531542.Google Scholar
Powell, E.N. and Klinck, J.M. (2007) Is oyster shell a sustainable estuarine resource? Journal of Shellfish Research 26, 181194.Google Scholar
Powell, E.N., Klinck, J.M. and Hofmann, E.E. (2010) Generation time and the stability of sex determining alleles in oyster populations as deduced using a gene based population dynamics model. Journal of Theoretical Biology 271, 2743.Google Scholar
Powell, E.N., Morson, J., Ashton-Alcox, K.A. and Kim, Y. (2012) Accomodation of the sex ratio in eastern oysters Crassostrea virginica to variation in growth and mortality across the estuarine salinity gradient in Delaware Bay. Journal of the Marine Biological Association of the United Kingdom.Google Scholar
Rochet, M. (1998) Short term effects of fishing on life history traits of fishes. ICES Journal of Marine Science 55, 371391.Google Scholar
Rountree, H., Clark, W. and Mountford, K. (2007) John Smith's Chesapeake voyages 1607–1609. Charlottesville, VA: University of Virginia Press.Google Scholar
Rothschild, B., Ault, J. and Heral, M. (1994) Decline of the Chesapeake Bay oyster population: a century of habitat destruction and overfishing. Marine Ecology Progress Series 111, 2939.Google Scholar
Shumway, S.E. (1996) Natural environmental factors. In Kennedy, V., Newell, R. and Eble, A. (eds) The eastern oyster Crassostrea virginica . College Park, MD: Maryland Sea Grant College, pp. 467513.Google Scholar
Soniat, T., Hofmann, E.E., Klinck, J.M. and Powell, E.N. (2009) Differential modulation of eastern oyster (Crassostrea virginica) disease parasites by the El-Niño-Southern Oscillation and the North Atlantic Oscillation. International Journal of Earth Science 98, 99114.CrossRefGoogle Scholar
Southworth, M.J., Harding, J.M. and Mann, R. (2009) The status of Virginia's public oyster resource 2008. Molluscan Ecology Program Report, Virginia Institute of Marine Science, Gloucester Point, Virginia, 51 pp.Google Scholar
Southworth, M.J., Harding, J.M., Mann, R. and Wesson, J.A. (2010) Oyster (Crassostrea virginica; Gmelin 1791) population dynamics on public reefs in the Great Wicomico River, Virginia, USA. Journal of Shellfish Research 29, 271290.Google Scholar
Stenzel, H. (1971) Oysters. In Moore, R. (ed.) Treatise on invertebrate paleontology, Part N. Volume 3. Bivalvia. Lawrence, KS: Geological Society of America, University of Kansas Press, pp. N953N1224.Google Scholar
Thompson, R., Newell, R., Kennedy, V. and Mann, R. (1996) Reproductive processes and early development. In Kennedy, V., Newell, R. and Eble, A. (eds) The eastern oyster Crassostrea virginica . College Park, MD: Maryland Sea Grant College, pp. 335370.Google Scholar
Tranter, D.J. (1958) Reproduction in Australian pearl oysters (Lamellibranchia). III. Pinctada albina (Lamarck): breeding season and sexuality. Australian Journal of Marine and Freshwater Research 9, 191216.Google Scholar
Ulanowicz, R. and Tuttle, J. (1992) The trophic consequences of oyster stock rehabilitation in Chesapeake Bay. Estuaries 15, 298306.Google Scholar
Walsh, M.R., Munch, S., Chiba, S. and Conover, D. (2006) Maladaptive changes in multiple traits caused by fishing: impediments to population recovery. Ecology Letters 9, 142148.Google Scholar
Woods, H., Hargis, W., Hershner, C. and Mason, P. (2005) Disappearance of the natural emergent 3-dimensional oyster reef system of the James River, Virginia, 1871–1948. Journal of Shellfish Research 24, 139142.Google Scholar
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