Skip to main content Accessibility help

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

  • Juliana M. Harding (a1), Eric N. Powell (a2), Roger Mann (a1) and Melissa J. Southworth (a1)

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.

Corresponding author
Correspondence should be addressed to: J.M. Harding, Department of Marine Science, Coastal Carolina University, Conway, SC, USA 29528, email:
Hide All

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

Hide All
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.
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.
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.
Andrews, J.D. (1996) History of Perkinsus marinus, a pathogen of oysters in Chesapeake Bay 1950–1984. Journal of Shellfish Research 15, 1316.
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.
Asif, M. (1979) Hermaphroditism and sex reversal in the four common oviparous species of oysters from the coast of Karachi. Hydrobiologia 66, 4955.
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.
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.
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.
Bhattacharya, C.G. (1967) A simple method of resolution of a distribution into Gaussian components. Biometrics 23, 115135.
Burkenroad, M. (1931) Sex in the Louisiana oyster Ostrea virginica . Science 74, 7172.
Buroker, N. (1983) Sexuality with respect to shell length and group size in the Japanese oyster Crassostrea gigas . Malacalogia 23, 271279.
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.
Butler, P. (1952) Growth and mortality rates in sibling and unrelated oyster populations. Proceedings of the Gulf and Caribbean Fisheries Institute 4, 71.
Buxton, C. (1993) Life history changes in exploited reef fishes on the east coast of South Africa. Environmental Biology of Fishes 36, 4763.
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.
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.
Coe, W. (1936) Sex ratios and sex changes in mollusks. Memoirs of the Royal Museum of Natural History Belgium 3, 6976.
Coe, W. (1943) Sexual differentiation in mollusks. I. Pelecypods. Quarterly Review of Biology 18, 154164.
Comfort, A. (1957) The duration of life in mollusks. Proceedings of the Malacological Society of London 32, 219241.
Conover, W.J. (1980) Practical non-parametric statistics. New York; John Wiley and Sons, 493 pp.
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.
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.
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.
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.
Galtsoff, P. (1964) The American oyster Crassostrea virginica Gmelin. US Fish and Wildlife Service Fisheries Bulletin 64, 480 pp.
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.
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.
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.
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.
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.
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.
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.
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.
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
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.
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.
Kennedy, V. (1983) Sex ratios in oysters, emphasizing Crassotrea virginica from Chesapeake Bay, Maryland. Veliger 25, 329338.
Kennedy, V. (1996) The ecological role of the eastern oyster, Crassostrea virginica, with remarks on disease. Journal of Shellfish Research 15, 177183.
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.
Kirby, M.X. (2000) Paleoecological differences between Tertiary and Quaternary Crassostrea oysters, as revealed by stable isotope sclerochronology. Palaios 15, 132141.
Krebs, C. (1989) Ecological methodology. New York: Harper Collins Publishers, Inc., 654 pp.
Law, R. and Grey, D. (1989) Evolution of yields from populations with age-specific cropping. Evolutionary Ecology 3, 343359.
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.
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.
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.
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.
Menzel, R.W. (1951) Early sexual development and growth of the American oyster in Louisiana waters. Science 113, 719721.
Morbrey, Y. and Abrams, P. (2004) The interaction between reproductive lifespan and protandry in seasonal breeders. Journal of Evolutionary Biology 17, 768778.
Moore, H.F. (1897) Oysters and methods of oyster culture. Report of the US Commission of Fish and Fisheries, pp. 263340.
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.
Noreen, E.W. (1989) Computer-intensive methods for testing hypotheses: an introduction. New York: John Wiley and Sons.
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.
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.
Paniagua-Chavez, C. and Acosta-Ruiz, M. (1995) Gonadal development of Crassostrea gigas in Bahia San Quintin, Baja, California, Mexico. Ciencias Marinas 20, 225242.
Paynter, K. (1996) The effects of Perkinsus marinus infection on physiological processes in the eastern oyster, Crassostrea virginica . Journal of Shellfish Research 15, 119125.
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.
Powell, E.N. and Cummins, H. (1985) Are molluscan maximum life spans determined by long-term cycles in benthic communities? Oecologia 67, 177182.
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.
Powell, E.N. and Klinck, J.M. (2007) Is oyster shell a sustainable estuarine resource? Journal of Shellfish Research 26, 181194.
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.
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.
Rochet, M. (1998) Short term effects of fishing on life history traits of fishes. ICES Journal of Marine Science 55, 371391.
Rountree, H., Clark, W. and Mountford, K. (2007) John Smith's Chesapeake voyages 1607–1609. Charlottesville, VA: University of Virginia Press.
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.
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.
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.
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.
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.
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.
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.
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.
Ulanowicz, R. and Tuttle, J. (1992) The trophic consequences of oyster stock rehabilitation in Chesapeake Bay. Estuaries 15, 298306.
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.
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.
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? *


Type Description Title
Supplementary materials

Harding supplementary 2
Harding supplementary 2

 Word (227 KB)
227 KB
Supplementary materials

Harding supplementary 5
Harding supplementary 5

 Word (69 KB)
69 KB
Supplementary materials

Harding supplementary 3
Harding supplementary 3

 Word (69 KB)
69 KB
Supplementary materials

Harding supplementary 4
Harding supplementary 4

 Word (69 KB)
69 KB
Supplementary materials

Harding supplementary 1
Harding supplementary 1

 Word (61 KB)
61 KB
Supplementary materials

Harding supplementary 6
Harding supplementary 6

 Word (32 KB)
32 KB


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed