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Accommodation of the sex-ratio in eastern oysters Crassostrea virginica to variation in growth and mortality across the estuarine salinity gradient

Published online by Cambridge University Press:  24 April 2012

Eric N. Powell ,
Jason M. Morson ,
Kathryn A. Ashton-Alcox  and
Yungkul Kim
Eric N. Powell*
Affiliation:
Haskin Shellfish Research Laboratory, Rutgers University, 6959 Miller Avenue, Port Norris, NJ 08349
Jason M. Morson
Affiliation:
Haskin Shellfish Research Laboratory, Rutgers University, 6959 Miller Avenue, Port Norris, NJ 08349
Kathryn A. Ashton-Alcox
Affiliation:
Haskin Shellfish Research Laboratory, Rutgers University, 6959 Miller Avenue, Port Norris, NJ 08349
Yungkul Kim
Affiliation:
Department of Biology, Jackson State University, 1400 Lynch Street, Jackson, MS 39217
*
Correspondence should be addressed to: E.N. Powell, Haskin Shellfish Research Laboratory, Rutgers University, 6959 Miller Avenue, Port Norris, NJ 08349 email: eric@hsrl.rutgers.edu
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Abstract

Protandric oysters generate a relatively uniform reproductive potential over a wide range of environmental conditions that impose variations in growth rate and life span. Sex-at-length keys applied to survey data show that the female fraction routinely fell between 0.4 and 0.5, regardless of location in the salinity gradient. About 70% of population biomass is female over the same salinity range. Due to the necessary local modulation of the rate of male-to-female conversion to limit the influence of varying growth and life span over the salinity gradient, the number of males always exceeds by a small amount the number of females; thus improving the likelihood of a female having neighbouring males, a necessity for an immobile broadcast spawner. However, oysters at the extremes of the estuarine gradient all yielded populations with divergent sex-ratios. One consequence of reduced generation time brought about by increased mortality from disease should be selection favouring the switch from male to female at smaller size, if disease mortality is strongly female-biased. The site with the longest record of high mortality manifests such an increase. Sites up coastal rivers, putative refuges from disease, harbour animals with the slowest male-to-female conversion rates. Arguably these animals are most similar to the ancestral oyster pre-disease. Marketed animals range from 62% to 69% female. The principal influence of the fishery, and of oyster disease, would seem to be a reduction in lifetime egg production. Dermo disease may have reduced lifetime fecundity of females by nearly a factor of four.

Keywords

sex-ratiooystersalinity gradientsize-dependentage-dependentlifetime fecundityprotandryfishery bias
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Special Issue 2: Fish and Fisheries , March 2013 , pp. 533 - 555
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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References

REFERENCES

Adams, S.L., Smith, J.F., Roberts, R.D., Janke, A.R., Kaspar, H.F., Tervit, H.R., Pugh, P.A., Webb, S.C. and King, N.G. (2004) Cryopreservation of sperm of the Pacific oyster (Crassostrea gigas): development of a practical method for commercial spat production. Aquaculture 242, 271–282.CrossRefGoogle Scholar
Babcock, R.C., Mundy, C.N. and Whitehead, D. (1994) Sperm diffusion models and in situ confirmation of long distance fertilization in the free-spawning asteroid Acanthaster planci . Biological Bulletin. Marine Biological Laboratory, Woods Hole 186, 17–28.Google Scholar
Bayne, B.L. (1999) Physiological components of growth differences between individual oysters (Crassostrea gigas) and a comparison with Saccostrea commercialis . Physiological and Biochemical Zoology 72, 705–713.CrossRefGoogle Scholar
Bayne, B.L. and Newell, R.C. (1983) Physiological energetics of marine molluscs. In Salleuddin, S.D.M. and Wilbur, K.M. (eds) The Mollusca. Volume 4 physiology, Part I. New York: Academic Press Inc., pp. 407–515.Google Scholar
Bayne, B.L., Salkeld, P.N. and Worrall, C.M. (1983) Reproductive effort and value in different populations of the marine mussel, Mytilus edulis L. Oecologia (Berlin) 59, 18–26.Google Scholar
Bell, G. (1980) The costs of reproduction and their consequences. American Naturalist 116, 45–76.Google Scholar
Berrigan, M., Candies, T., Cirino, J., Dugas, R., Dyer, C., Gray, J., Herrington, T., Keithly, W., Leard, R., Nelson, J.R. and van Hoose, M. (1991) The oyster fishery of the Gulf of Mexico, United States: a regional management plan. Ocean Springs, MS: Gulf States Marine Fisheries Commission.Google Scholar
Burkenroad, M.D. (1931) Sex in the Louisiana oyster, Ostrea virginica . Science (Washington, DC) 74, 71–72.CrossRefGoogle ScholarPubMed
Bushek, D., Kornbluh, A., Wang, H., Guo, X., DeBrosse, G. and Quinlan, J. (2008) Fertilization interference between Crassostrea ariakensis and Crassostrea virginica: a gamete sink? Journal of Shellfish Research 27, 593–600.Google Scholar
Buxton, C.D. (1993) Life-history changes in exploited reef fishes on the east coast of South Africa. Environmental Biology of Fishes 36, 47–63.Google Scholar
Calow, P. (1973) The relationship between fecundity, phenology, and longevity: a systems approach. American Naturalist 107, 559–574.CrossRefGoogle Scholar
Carriker, M.R. (1955) Critical review of biology and control of oyster drills Urosalpinx and Eupleura . United States Fish and Wildlife Service Special Science Report—Fisheries 148, 1–150.Google Scholar
Castro, E.M., Urpf, O.P., Madriz, E.Z., Quesada, R.Q. and Montoya, J.A. (1985) Tasa de filtración del ostión de manglar, (Crassostrea rhizophorae, Guilding 1828), a diferentes salinidades y temperaturas. Revista de Biologia Tropical 33, 77–79.Google Scholar
Charnov, E.L. and Hannah, R.W. (2002) Shrimp adjust their sex ratio to fluctuating age distributions. Evolutionary Ecology Research 4, 239–246.Google Scholar
Choi, K-S., Lewis, D.H., Powell, E.N. and Ray, S.M. (1993) Quantitative measurement of reproductive output in the American oyster, Crassostrea virginica (Gmelin) using an enzyme-linked immunosorbent assay (ELISA). Aquaculture and Fishery Management 24, 299–322.Google Scholar
Choi, K-S., Powell, E.N., Lewis, D.H. and Ray, S.M. (1994) Instantaneous reproductive effort in female American oysters, Crassostrea virginica, measured by a new immunoprecipitation assay. Biological Bulletin. Marine Biological Laboratory, Woods Hole 186, 41–61.Google Scholar
Coe, W.R. (1936) Sex ratios and sex changes in mollusks. Mémoires du Musée Royal d'histoire Naturelle de Belgique Série 10 Fascicule 3, 69–76.Google Scholar
Coe, W.R. (1938) Conditions influencing change of sex in mollusks of the genus Crepidula . Journal of Experimental Zoology 77, 401–424.Google Scholar
Collin, R. (2006) Sex ratio, life-history invariants, and patterns of sex change in a family of protandrous gastropods. Evolution 60, 735–745.Google Scholar
Comfort, A. (1957) The duration of life in mollusks. Proceedings of the Malacological Society of London 32, 219–241.Google Scholar
Conover, W.J. (1980) Practical nonparametric statistics. New York: John Wiley & Sons, 493 pp.Google Scholar
Custer, J.F. and Doms, K.R. (1990) Analysis of microgrowth patterns of the American oyster (Crassostrea virginica) in the Middle Atlantic region of North America: archaeological applications. Journal of Archaeological Science 17, 151–160.Google Scholar
Dekshenieks, M.M., Hofmann, E.E., Klinck, J.M. and Powell, E.N. (2000) Quantifying the effects of environmental change on an oyster population: a modeling study. Estuaries 23, 593–610.Google Scholar
Devillers, N., Eversole, A.G. and Isely, J.J. (1998) A comparison of four growth models for evaluating growth of the northern quahog Mercenaria mercenaria (L.). Journal of Shellfish Research 17, 191–194.Google Scholar
Dickie, L.M., Kerr, S.R. and Boudreau, P.R. (1987) Size-dependent processes underlying regularities in ecosystem structure. Ecological Monographs 57, 233–250.Google Scholar
Dinamani, P. (1974) Reproductive cycle and gonadal changes in the New Zealand rock oyster Crassostrea glomerata . New Zealand Journal of Marine and Freshwater Research 8, 39–65.Google Scholar
Dong, Q. (2005) Comparative studies of sperm cryopreservation of diploid and tetraploid Pacific oysters. PhD thesis. Louisiana State University, 271 pp.Google Scholar
Engle, J.B. (1953) Effect of Delaware River flow on oysters in the natural seed beds of Delaware Bay. National Shellfisheries Association Convention Addresses, pp. 1–26.Google Scholar
Ford, S.E. (1996) Range extension by the oyster parasite Perkinsus marinus into the northeastern United States: response to climate change. Journal of Shellfish Research 15, 45–56.Google Scholar
Ford, S.E. and Haskin, H.H. (1982) History and epizootiology of Haplosporidium nelsoni (MSX), an oyster pathogen in Delaware Bay, 1957–1980. Journal of Invertebrate Pathology 40, 118–141.Google Scholar
Ford, S., Powell, E., Klinck, J. and Hofmann, E. (1999) Modeling the MSX parasite in eastern oyster (Crassostrea virginica) populations. I. Model development, implementation, and verification. Journal of Shellfish Research 18, 475–500.Google Scholar
Ford, S.E. and Smolowitz, R. (2007) Infection dynamics of an oyster parasite in its newly expanded range. Marine Biology (Berlin) 151, 119–133.Google Scholar
Gaffney, P.M. and Bushek, D. (1996) Genetic aspects of disease resistance in oysters. Journal of Shellfish Research 15, 135–140.Google Scholar
Galindo-Sánchez, C.E., Gaffney, P.M., Pérez-Rostro, C.I., de la Rosa-Vélez, J., Candela, J. and Cruz, P. (2008) Assessment of genetic diversity of the eastern oyster Crassostrea virginica in Vera Cruz, Mexico using microsatellite markers. Journal of Shellfish Research 27, 721–727.Google Scholar
Gallager, S.M. and Mann, R. (1986) Growth and survival of larvae of Mercenaria mercenaria (L) and Crassostrea virginica (Gmelin) relative to broodstock conditioning and lipid content of eggs. Aquaculture 56, 105–121.Google Scholar
Galtsoff, P.S. (1964) The American oyster Crassostrea virginica Gmelin. Fishery Bulletin of the United States Fish and Wildlife Service Bureau of Commercial Fisheries 64, 1–480.Google Scholar
Gardner, A., Allsop, D.J., Charnov, E.L. and West, S.A. (2005) A dimensionless invariant for relative size at sex change in animals: explanation and implications. American Naturalist 165, 551–565.Google Scholar
Gunter, G. (1979) Studies of the southern oyster borer, Thais haemastoma . Gulf Research Reports 6, 249–260.Google Scholar
Guo, X., Hedgecock, D., Hershberger, W.K., Cooper, K. and Allen, S.K. Jr (1998) Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution 52, 394–402.Google Scholar
Halliday, R.G. and Pinhorn, A.T. (2002) A review of the scientific and technical bases for policies on the capture of small fish in North Atlantic groundfish fisheries. Fisheries Research 57, 211–222.Google Scholar
Harding, J.M., Mann, R. and Kilduff, C.W. (2007) The effects of female size on fecundity in a large marine gastropod Rapana venosa (Muricidae). Journal of Shellfish Research 26, 33–42.Google Scholar
Harding, J.M., Mann, R. and Southworth, M.J. (2008) Shell length-at-age relationships in James River, Virginia, oysters (Crassostrea virginica) collected four centuries apart. Journal of Shellfish Research 27, 1109–1115.Google Scholar
Haskin, H.H. and Ford, S.E. (1982) Haplosporidium nelsoni (MSX) on Delaware Bay seed oyster beds: a host–parasite relationship along a salinity gradient. Journal of Invertebrate Pathology 40, 388–405.Google Scholar
Hawkins, A.J.S. and Bayne, B.L. (1992) Physiological interrelations and the regulation of production. In Gosling, E. (ed.) The mussel Mytilus: ecology, physiology, genetics, and culture. Amsterdam: Elsevier, pp. 171–222.Google Scholar
Hayes, P.F. and Menzel, R.W. (1981) The reproductive cycle of early setting Crassostrea virginica (Gmelin) in the northern Gulf of Mexico, and its implications for population recruitment. Biological Bulletin. Marine Biological Laboratory, Woods Hole 160, 80–88.Google Scholar
Héral, M. and Deslous-Paoli, J.M. (1983) Valeur énergétique de la chain de l'hûrtre Crassostrea gigas estimée par mesures microcalorimetriques et par dosages biochimiques. Oceanologica Acta 6, 193–199.Google Scholar
Hoagland, K.E. (1978) Protandry and the evolution of environmentally-mediated sex change: a study of the Mollusca. Malacologia 17, 365–391.Google Scholar
Hodgson, A.N., Quesne, W.J.F. le, Hawkins, S.J. and Bishop, J.D.D. (2007) Factors affecting fertilization success in two species of patellid limpet (Mollusca: Gastropoda) and development of fertilization kinetics models. Marine Biology (Berlin) 150, 415–426.Google Scholar
Hoenig, J.M. (1983) Empirical use of longevity data to estimate mortality rates. Fishery Bulletin 83, 898–903.Google Scholar
Hofmann, E., Bushek, D., Ford, S., Guo, X., Haidvogel, D., Hedgecock, D., Klinck, J., Milbury, C., Narváez, D., Powell, E., Wang, Y., Wang, Z., Wilkin, J. and Zhang, L. (2009) Understanding how disease and environment combine to structure resistance in estuarine bivalve populations. Oceanography 22, 212–231.Google Scholar
Hofmann, E.E., Klinck, J.M., Kraeuter, J.N., Powell, E.N., Grizzle, R.E., Buckner, S.C. and Bricelj, V.M. (2006) A population dynamics model of the hard clam, Mercenaria mercenaria: development of the age- and length-frequency structure of the population. Journal of Shellfish Research 25, 417–444.Google Scholar
Hofmann, E.E., Powell, E.N., Klinck, J.M. and Wilson, E.A. (1992) Modeling oyster populations. III. Critical feeding periods, growth and reproduction. Journal of Shellfish Research 11, 399–416.Google Scholar
HSRL (2008) Report of the 2008 Stock Assessment Workshop (10th SAW) for the New Jersey Delaware Bay oyster beds. Port Norris, NJ: Haskin Shellfish Research Laboratory, Rutgers University, 111 pp.Google Scholar
HSRL (2009) Report of the 2009 Stock Assessment Workshop (11th SAW) for the New Jersey Delaware Bay oyster beds. Port Norris, NJ: Haskin Shellfish Research Laboratory, Rutgers University, 128 pp.Google Scholar
Jordan, S.J. and Coakley, J.M. (2004) Long-term projections of eastern oyster populations under various management scenarios. Journal of Shellfish Research 23, 63–72.Google Scholar
Jordan, S.J., Greenhawk, K.N., McCollough, C.B., Vanisko, J. and Homer, M.L. (2002) Oyster biomass, abundance, and harvest in northern Chesapeake Bay: trends and forecasts. Journal of Shellfish Research 21, 733–741.Google Scholar
Kang, S-G., Choi, K-S., Bulgakov, A.A., Kim, Y. and Kim, S-Y. (2003) Enzyme-linked immunosorbent assay (ELISA) used in quantification of reproductive output in the Pacific oyster, Crassostrea gigas, in Korea. Journal of Experimental Marine Biology and Ecology 282, 1–21.Google Scholar
Kennedy, V.S. (1983) Sex ratios in oysters, emphasizing Crassostrea virginica from Chesapeake Bay, Maryland. Veliger 25, 329–338.Google Scholar
Kennedy, A.V. and Battle, H.I. (1964) Cyclic changes in the gonad of the American oyster, Crassostrea virginica (Gmelin). Canadian Journal of Zoology 42, 305–321.Google Scholar
Kennedy, V.S. and Krantz, C.B. (1982) Comparative gametogenic and spawning patterns of the oyster Crassostrea virginica (Gmelin) in central Chesapeake Bay. Journal of Shellfish Research 2, 133–140.Google Scholar
Kiørboe, T. (2006) Sex, sex-ratios, and the dynamics of pelagic copepod populations. Oecologia (Berlin) 148, 40–50.Google ScholarPubMed
Kimmel, D.G. and Newell, R.I.E. (2007) The influence of climate variation on eastern oyster (Crassostrea virginica) juvenile abundance in Chesapeake Bay. Limnology and Oceanography 52, 959–965.Google Scholar
Kirby, M.X. (2000) Paleoecological differences between Tertiary and Quaternary Crassostrea oysters, as revealed by stable isotope sclerochronology. Palaios 15, 132–141.Google Scholar
Klinck, J.M., Powell, E.N., Kraeuter, J.N., Ford, S.E. and Ashton-Alcox, K.A. (2001) A fisheries model for managing the oyster fishery during times of disease. Journal of Shellfish Research 20, 977–989.Google Scholar
Koehn, R.K. and Shumway, S.E. (1982) A genetic/physiological explanation for differential growth rate among individuals of the American oyster, Crassostrea virginica (Gmelin). Marine Biology Letters 3, 35–42.Google Scholar
Kraeuter, J.N., Buckner, S. and Powell, E.N. (2005) A note on a spawner–recruit relationship for a heavily exploited bivalve: the case of northern quahog (hard clams), Mercenaria mercenaria in Great South Bay New York. Journal of Shellfish Research 24, 1043–1052.Google Scholar
Kraeuter, J.N., Ford, S. and Canzonier, W. (2003) Increased biomass yield from Delaware Bay oysters (Crassostrea virginica) by alteration of planting season. Journal of Shellfish Research 22, 39–49.Google Scholar
Kraeuter, J.N., Ford, S. and Cummings, M. (2007) Oyster growth analysis: a comparison of methods. Journal of Shellfish Research 26, 479–491.Google Scholar
Langdon, C., Evans, F., Jacobson, D. and Blouin, M. (2003) Yields of cultured Pacific oysters Crassostrea gigas Thunberg improved after one generation of selection. Aquaculture 220, 227–244.Google Scholar
Lango-Reynoso, F., Chávez-Villaba, J. and Pennec, M. le (2006) Reproductive patterns of the Pacific oyster Crassostrea gigas in France. Invertebrate Reproduction & Development 49, 41–50.Google Scholar
Levitan, D.R. (2005) The distribution of male and female reproductive success in a broadcast spawning marine invertebrate. Integrative and Comparative Biology 45, 848–855.Google Scholar
Lundberg, S. and Persson, L. (1993) Optimal body size and resource density. Journal of Theoretical Biology 164, 163–180.Google Scholar
Mace, P.M. and Sissenwine, M.P. (1993) How much spawning per recruit is enough? Canadian Special Publications of Fisheries and Aquatic Sciences 120, 101–118.Google Scholar
Malley, A.L. and Haley, L.E. (1983) Growth rate and survival in pure population matings and crosses of the oyster Crassostrea virginica . Canadian Journal of Fisheries and Aquatic Sciences 40, 948–954.CrossRefGoogle Scholar
Mancera, E. and Mendo, J. (1996) Population dynamics of the oyster Crassostrea rhizophorae from the Ciénaga Grande de Santa Marta, Colombia. Fisheries Research 26, 139–148.Google Scholar
Mann, R. (2000) Restoring the oyster reef communities in the Chesapeake Bay: a commentary. Journal of Shellfish Research 19, 335–339 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, 239–253.Google Scholar
McCormick, M.I. (2006) Mothers matter: crowding leads to stressed mothers and smaller offspring in marine fish. Ecology 87, 1104–1109.Google Scholar
McCuaig, J.M. and Green, R.H. (1983) Unionid growth curves derived from annual rings: a baseline model for Long Point Bay, Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 40, 436–442.Google Scholar
McNamara, J.M. (1993) State-dependent life-history equations. Acta Biotheoretica 41, 165–174.Google Scholar
Nelson, T.C. (1959) Oyster seed production on Cape May's tidal flats. Cape May Geographic Society 13, 12–16.Google Scholar
Newell, R.I.E., Alspach, G.S. Jr, Kennedy, V.S. and Jacobs, D. (2000) Mortality of newly metamorphosed eastern oysters (Crassostrea virginica) in mesohaline Chesapeake Bay. Marine Biology (Berlin) 136, 665–676.Google Scholar
Ngo, T.T.T., Kang, S-G., Kang, D-H., Sorgeloos, P. and Choi, K-S. (2006) Effect of culture depth on the proximate composition and reproduction of the Pacific oyster, Crassostrea gigas from Gosung Bay, Korea. Aquaculture 253, 712–720.Google Scholar
Noreen, E.W. (1989) Computer-intensive methods for testing hypotheses: an introduction. New York: John Wiley & Sons, 229 pp.Google Scholar
O'Beirn, F.X., Heffernan, P.B., Walker, R.L. and Jansen, M.L. (1996) Young-of-the-year oyster, Crassostrea virginica, reproduction in coastal Georgia. Estuaries 19, 651–658.Google Scholar
O'Beirn, F.X., Walker, R.L. and Jansen, M.L. (1998) Microgeographical variation in gametogenesis and sex ratios in the eastern oyster at two marsh sites in Georgia. Transactions of the American Fisheries Society 27, 298–308.Google Scholar
Ohnishi, S. and Akamine, T. (2006) Extension of von Bertalanffy growth model incorporating growth patterns of soft and hard tissues in bivalve molluscs. Fisheries Science 72, 787–795.Google Scholar
Orton, J.H. (1927) Observations and experiments on sex-change in the European oyster (O. edulis) Part I. The change from female to male. Journal of the Marine Biological Association of the United Kingdom 14, 967–1045.Google Scholar
Orton, J.H. (1936) Observations and experiments on sex-change in the European oyster (O. edulis) Part V. A simultaneous study of spawning in 1927 in two distinct geographical localities. Mémoires du Musée Royal d'histoire Naturelle de Belgique Série 10 Fascicule 3, 997–1056.Google Scholar
Paniagua-Chávez, C.G. and Acosta-Ruiz, M. de J. (1995) Gonadal development of Crassostrea gigas in Bahía San Quintín, Baja California, Mexico. Ciencias Marinas 20, 225–242.Google Scholar
Paraso, M.C., Ford, S.E., Powell, E.N., Hofmann, E.E. and Klinck, J.M. (1999) Modeling the MSX parasite in Eastern oyster (Crassostrea virginica) populations. II. Salinity effects. Journal of Shellfish Research 18, 501–516.Google Scholar
Paynter, K.T. and Burreson, E.M. (1991) Effects of Perkinsus marinus infection in the eastern oyster, Crassostrea virginica: II. Disease development and impact on growth rate at different salinities. Journal of Shellfish Research 10, 425–431.Google Scholar
Powell, E.N., Ashton-Alcox, K.A., Kraeuter, J.N., Ford, S.E. and Bushek, D. (2008) Long-term trends in oyster population dynamics in Delaware Bay: regime shifts and response to disease. Journal of Shellfish Research 27, 729–755.Google Scholar
Powell, E.N., Gendek, J.J. and Ashton-Alcox, K.A. (2005) Fisherman choice and incidental catch: size frequency of oyster landings in the New Jersey oyster fishery. Journal of Shellfish Research 24, 469–476.Google Scholar
Powell, E.N., Hofmann, E.E., Klinck, J.M. and Ray, S.M. (1992) Modeling oyster populations I. A commentary on filtration rate. Is faster always better? Journal of Shellfish Research 11, 387–398.Google Scholar
Powell, E.N., Klinck, J.M. and Hofmann, E.E. (1996) Modeling diseased oyster populations. II. Triggering mechanisms for Perkinsus marinus epizootics. Journal of Shellfish Research 15, 141–165.Google Scholar
Powell, E.N., Klinck, J.M., Ashton-Alcox, K.A. and Kraeuter, J.N. (2009a) Multiple stable reference points in oyster populations: biological relationships for the eastern oyster (Crassostrea virginica) in Delaware Bay. Fishery Bulletin 107, 109–132.Google Scholar
Powell, E.N., Klinck, J.M., Ashton-Alcox, K.A. and Kraeuter, J.N. (2009b) Multiple stable reference points in oyster populations: implications for reference point-based management. Fishery Bulletin 107, 133–147.Google Scholar
Powell, E.N., Klinck, J.M. and Hofmann, E.E. (2011a) 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, 27–43.Google Scholar
Powell, E.N., Morson, J. and Klinck, J.M. (2011b) Application of a gene-based population dynamics model to the optimal egg size problem: why do bivalve planktotrophic eggs vary in size? Journal of Shellfish Research 30, 403–423.Google Scholar
Powell, E.N., Klinck, J.M., Ashton-Alcox, K.A., Hofmann, E.E. and Morson, J.A. (in press) The rise and fall of Crassostrea virginica oyster reefs: the role of disease and fishing in their demise and a vignette on their management. Journal of Marine Research.Google Scholar
Provenzano, A.J. Jr (1961) Effects of the flatworm Stylochus ellipticus (Girard) on oyster spat in two salt water ponds in Massachusetts. Proceedings of the National Shellfisheries Association 50, 83–88.Google Scholar
Rago, P.J., Sosebee, K.A., Brodziak, J.K.T., Murawski, S.A. and Anderson, E.D. (1998) Implications of recent increases in catches on the dynamics of northwest Atlantic spiny dogfish (Squalus acanthias). Fisheries Research 39, 165–181.Google Scholar
Ragone Calvo, L.M., Wetzel, R.L. and Burreson, E.M. (2001) Development and verification of a model for the population dynamics of the protistan parasite, Perkinsus marinus, within its host, the eastern oyster, Crassostrea virginica, in Chesapeake Bay. Journal of Shellfish Research 20, 231–241.Google Scholar
Rothschild, B.J., Ault, J.S., Goulletquer, P. and Héral, M. (1994) Decline of the Chesapeake Bay oyster populations: a century of habitat destruction and overfishing. Marine Ecology Progress Series 111, 29–39.Google Scholar
Sattar, S.A., Jørgensen, C. and Fiksen, Ø. (2008) Fisheries-induced evolution of energy and sex allocation. Bulletin of Marine Science 83, 235–250.Google Scholar
Shumway, S.E. (1982) Oxygen consumption in oysters: an overview. Marine Biology Letters 3, 1–23.Google Scholar
Siddiqui, G. and Ahmed, M. (2002) Gametogenic patterns of the larviparous oyster Ostrea nomades from Karachi, Pakistan (northern Arabian Sea). Aquaculture Research 33, 1049–1058.Google Scholar
Sinclair, A.F., Swain, D.P. and Hanson, J.M. (2002a) Measuring changes in the direction and magnitude of size-selective mortality in a commercial fish population. Canadian Journal of Fisheries and Aquatic Sciences 59, 361–371.Google Scholar
Sinclair, A.F., Swain, D.P. and Hanson, J.M. (2002b) Disentangling the effects of size-selective mortality, density, and temperature on length-at-age. Canadian Journal of Fisheries and Aquatic Sciences 59, 372–382.Google Scholar
Sissenwine, M.P. and Shepherd, J.G. (1987) An alternative perspective on recruitment overfishing and biological reference points. Canadian Journal of Fisheries and Aquatic Sciences 44, 913–918.CrossRefGoogle Scholar
Soniat, T.M. and Brody, M.S. (1988) Field validation of a habitat suitability index model for the American oyster. Estuaries 11, 87–95.Google Scholar
Spight, T.M. and Emlen, J. (1976) Clutch size of two marine snails with a changing food supply. Ecology 57, 1162–1178.Google Scholar
Swain, D.P., Sinclair, A.F. and Hanson, J.M. (2007) Evolutionary response to size-selective mortality in an exploited fish population. Proceedings of the Royal Society of London Series B—Biological Sciences 274, 1015–1022.Google Scholar
Taris, N., Batista, F.M. and Boudry, P. (2007) Evidence of response to unintentional selection for faster development and inbreeding depression in Crassostrea gigas larvae. Aquaculture 272 (Supplement 1), S69–S79.Google Scholar
Thomas, F.I.M. (1994) Transport and mixing of gametes in three free-spawning polychaete annelids, Phragmatopoma californica (Fewkes), Sabellaria cementarium (Moore), and Schizobranchia insignis (Bush). Journal of Experimental Marine Biology and Ecology 179, 11–27.Google Scholar
Vølstad, J.H., Dew, J. and Tarnowski, M. (2008) Estimation of annual mortality rates for eastern oysters (Crassostrea virginica) in Chesapeake Bay based on box counts and application of these rates to project population growth of C. virginica and C. ariakensis . Journal of Shellfish Research 27, 525–533.Google Scholar
von Bertalanffy, L. (1938) A quantitative theory of organic growth (inquiries on growth laws. II.). Human Biology 10, 181–213.Google Scholar
Walsh, M.R., Munch, S.B., Chiba, S. and Conover, D.O. (2006) Maladaptive changes in multiple traits caused by fishing: impediments to population recovery. Ecology Letters 9, 142–148.Google Scholar
Warner, R.R., Robertson, D.R. and Leigh, E.G. Jr (1975) Sex change and sexual selection. Science (Washington, DC) 190, 633–638.Google Scholar