Oceanography The Official Magazine of
The Oceanography Society
Volume 22 Issue 04

View Issue TOC
Volume 22, No. 4
Pages 212 - 231

OpenAccess

Understanding How Disease and Environment Combine to Structure Resistance in Estuarine Bivalve Populations

By Eileen Hofmann , David Bushek, Susan Ford , Ximing Guo , Dale Haidvogel , Dennis Hedgecock , John Klinck, Coren Milbury, Diego Narvaez, Eric Powell , Yongping Wang , Zhiren Wang, John Wilkin , and Liusuo Zhang  
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

Delaware Bay oyster (Crassostrea virginica) populations are influenced by two lethal parasites that cause Dermo and MSX diseases. As part of the US National Science Foundation Ecology of Infectious Diseases initiative, a program developed for Delaware Bay focuses on understanding how oyster population genetics and population dynamics interact with the environment and these parasites to structure the host populations, and how these interactions might be modified by climate change. Laboratory and field studies undertaken during this program include identifying genes related to MSX and Dermo disease resistance, potential regions for refugia and the mechanisms that allow them to exist, phenotypic and genotypic differences in oysters from putative refugia and high-disease areas, and spatial and temporal variability in the effective size of the spawning populations. Resulting data provide inputs to oyster genetics, population dynamics, and larval growth models that interface with a three-dimensional circulation model developed for Delaware Bay. Reconstruction of Lagrangian particle tracks is used to infer transport pathways of oyster larvae and MSX and Dermo disease pathogens. Results emerging from laboratory, field, and modeling studies are providing an understanding of long-term changes in Delaware Bay oyster populations that occur as the oyster population responds to climate, environmental, and biological variability.

Citation

The Delaware Bay Ecology of Infectious Diseases Group. 2009. Understanding how disease and environment combine to structure resistance in estuarine bivalve populations. Oceanography 22(4):212–231, https://doi.org/10.5670/oceanog.2009.110.

References

Ackerman E., L.R. Elveback, and J.P. Fox. 1984. Simulation of Infectious Disease Epidemics. Charles C. Thomas, Springfield, IL, 202 pp. 

Andrews, J.D. 1983. Minchinia nelsoni (MSX) infections in the James River seed-oyster area and their expulsion in spring. Estuarine, Coastal and Shelf Science 16:255–269.

Andrews, J.D., and J.L. Wood. 1967. Oyster mortality studies in Virginia. VI. History and distribution of Minchinia nelsoni, a pathogen of oysters, in Virginia. Chesapeake Science 8:1–13.

Bochenek, E.A., J.M. Klinck, E.N. Powell, and E.E. Hofmann. 2001. Biochemically based model of the growth and development of Crassostrea gigas larvae. Journal of Shellfish Research 20:243–265. 

Bower, S.M., S.E. McGladdery, and I.M. Price. 1994. Synopsis of infectious diseases and parasites of commercially exploited shellfish. Annual Review of Fish Diseases 4:1–200.

Brown, B.L., A.J. Butt, S.W. Shelton, D. Meritt, and K. T. Paynter. 2005. Resistance to Dermo in eastern oysters, Crassostrea virginica (Gmelin), of North Carolina but not Chesapeake Bay heritage. Aquaculture Research 36:1,391–1,399.

Burreson, E.M., and S. Ford. 2004. A review of recent information on the Haplosporidia, with a special reference to Haplosporidium nelsoni (MSX disease). Aquatic Living Resources 17:499–517.

Burreson, E.M., and L.M. Ragone Calvo. 1996. Epizootiology of Perkinsus marinus disease of oysters in Chesapeake Bay, with emphasis on data since 1985. Journal of Shellfish Research 15:17–34.

Burreson, E.M., N.A. Stokes, and C.S. Friedman. 2000. Increased virulence in an introduced pathogen: Haplosporidium nelsoni (MSX) in the eastern oyster Crassostrea virginica. Journal of Aquatic Animal Health 12:1–8.

Bushek, D., C.F. Dugan, and A.J. Lewitus. 1994. Serological affinities of the oyster pathogen Perkinsus marinus (Apicomplexa) with some dinoflagellates (Dinophyceae). Journal of Eukaryotic Microbiology 49:11–16. 

Chu, F.-L.E., J.F. La Peyre, and C.S. Burreson. 1993. Perkinsus marinus susceptibility and defense-related activities in eastern oysters, Crassostrea virginica: Salinity effects. Journal of Invertebrate Pathology 62:226–232.

Coen, L.D., and M.W. Luckenbach. 2000. Developing success criteria and goals for evaluating oyster reef restoration: Ecological function or resource exploitation? Ecological Engineering 15:323–343.

Cook T., M. Folli, J. Klinck, S. Ford, J. Miller. 1998. The relationship between increasing sea surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuarine, Coastal and Shelf Science 40:587–597.

Culloty, S.C, M.A. Cronin, and M.F. Mulcahy. 2003. Possible limitations of diagnostic methods recommended for the detection of the protistan, Bonamia ostreae in the European flat oyster, Ostrea edulis. Bulletin of the European Association of Fish Pathology 23(2):67–71. 

Dekshenieks, M.M., E.E. Hofmann, J.M. Klinck, and E.N. Powell. 1996. Modeling the vertical distribution of oyster larvae in response to environmental conditions. Marine Ecology Progress Series 136:97–110. 

Dekshenieks, M.M., E.E. Hofmann, J.M. Klinck, and E.N. Powell. 1997. A modeling study of the effects of size- and depth-dependent predation on larval survival. Journal of Plankton Research 19:1,583–1,598. 

Dekshenieks, M.M., E.E. Hofmann, J.M. Klinck, and E.N. Powell. 2000. Quantifying the effects of environmental variability on an oyster population using a coupled oyster-circulation model. Estuaries 23:593–610. 

Dekshenieks, M.M., E.E. Hofmann, and E.N. Powell. 1993. Environmental effects on the development of larvae of Crassostrea virginica: A modeling study. Journal of Shellfish Research 12:241–254. 

Encomio, V.G., S.M. Stickler, S.K. Allen, and F.L. Chu. 2005. Performance of “natural dermo-resistant” oyster stocks: Survival, disease, growth, condition and energy reserves. Journal of Shellfish Research 24:143–155.

Fairall, C.W., E.F. Bradley, J.E. Hare, A.A. Grachev, and J.B. Edson. 2003. Bulk parameterization of air-sea fluxes: Updates and verification for the COARE algorithm. Journal of Climate 16:571–591. 

Flather, R.A. 1976. A tidal model of the northwest European continental shelf. Memoirs de Société Royale des Sciences de Liège, Series 6 10:141–164.

Ford, S.E. 1996. Range extension by the oyster parasite Perkinsus marinus into the northeastern US: Response to climate change? Journal of Shellfish Research 15:45–56.

Ford, S.E., and H.H. Haskin. 1982. History and epizootiology of Haplosporidium nelsoni (MSX), an oyster pathogen in Delaware Bay, 1957–1980. Journal of Invertebrate Pathology 40:118–141.

Ford, S.E., J.N. Kraeuter, R.D. Barber, and G. Mathis. 2002. Aquaculture associated factors in QPX disease of hard clams: Density and seed source. Aquaculture 208:23–38.

Ford, S.E., E.N. Powell, J.M. Klinck, and E.E. Hofmann. 1999. Modeling the MSX parasite in eastern oyster (Crassostrea virginica) populations. I. Model development, implementation, and verification. Journal of Shellfish Research 18:475–500.

Gaffney, P.M., and D. Bushek. 1996. Genetic aspects of disease resistance in oysters. Journal of Shellfish Research 15:135–140.

Garvine, R.W., R.K. McCarthy, and K.C. Wong. 1992. The axial salinity gradient distribution in the Delaware estuary and its weak response to river discharge. Estuarine, Coastal and Shelf Science 13:157–165.

Haidvogel, D.B., H. Arango, W.P. Budgell, B.D. Cornuell, E. Curchitser, E. Di Lorenzo, K. Fennel, W.R. Geyer, A.J. Hermann, L. Lanerolle, and others. 2008. Ocean forecasting in terrain-following coordinates: Formulation and skill assessment of the Regional Ocean Modeling System. Journal of Computational Physics 227:3,595–3,624. 

Haskin, H.H. 1964. The distribution of oyster larvae. Pp. 76–80 in Occasional Publication 2. N. Marshall, H.P. Jeffries, T.A. Napora, and J.M. Sieburth, eds, Symposium on Experimental Marine Ecology, Graduate School of Oceanography, University of Rhode Island. 

Haskin, H.H., and S.E. Ford. 1979. Development of resistance to Minchinia nelsoni (MSX) mortality in laboratory-reared and native oyster stocks in Delaware Bay. US National Marine Fisheries Service. Marine Fisheries Review 41:54–63.

Haskin, H.H., and S.E. Ford. 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.

Haskin, H., and H.H. Hidu. 1978. Swimming speeds of oyster larvae Crassostrea virginica in different salinities and temperatures. Estuaries 1:252–255. 

Haskin, H.H., L.A. Stauber, and J.A. Mackin. 1966. Minchinia nelsoni n. sp. (Haplosporida, Haplosporidiidae): Causative agent of the Delaware Bay oyster epizootic. Science 153:1,414–1,416.

Hedgecock, D. 1994. Does variability in reproductive success limit effective population sizes of marine organisms? Pp. 122–134 in Genetics and Evolution of Aquatic Organisms. A. Beaumont, ed., Chapman & Hall, London.

Hedgecock, D., V. Chow, and R.S. Waples. 1992. Effective population numbers of shellfish broodstocks estimated from the temporal variance in allelic frequencies. Aquaculture 108:215–232.

Hedgecock, D., J.M. Klinck, E.N. Powell, L. Plough, and E. Hofmann. 2008. Insights into oyster population genetics from an Individual Based Model. Journal of Shellfish Research 27:1015. (abstract)

Hofmann, E.E., E.N. Powell, J.M. Klinck, and G. Saunders. 1995. Modeling diseased oyster populations. I. Modeling Perkinsus marinus infections in oysters. Journal of Shellfish Research 14:121–151.

Hofmann, E.E., E.N. Powell, J.M. Klinck, and E.A. Wilson. 1992. Modeling oyster populations. III. Critical feeding periods, growth and reproduction. Journal of Shellfish Research 11:399–416.

Hufnagel L., D. Brockmann, and T. Geisel. 2004. Forecast and control of epidemics in a globalized world. Proceedings of the National Academy of Science of the United States of America 101:15,124–15,129, doi:10.1073/pnas.0308344101. 

Kennedy, V.S., and W. van Heukelme. 1986. Responses to environmental factors by larval oysters Crassostrea virginica. American Malacological Bulletin 4:101. 

Kermack, W.O., and A.G. McKendrick. 1927. A contribution to the mathematical theory of epidemics. Proceedings of the Royal Society of London A 115:700–721.

Klinck, J.M., E.N. Powell, E.E. Hofmann, and M.M. Dekshenieks. 2002. Impact of channelization on oyster production: A hydrodynamic-oyster population model for Galveston Bay, Texas. Environmental Modeling and Assessment 7:273–289. 

Lafferty, K., and A.M. Kuris. 1993. Mass mortality of abalone Haliotis cracherodii on the California Channel Islands: Tests of epidemiological hypotheses. Marine Ecology Progress Series 96:239–248.

Lafferty, K.D., J.A. Porter, and S.E. Ford. 2004. Are diseases increasing in the ocean? Annual Review of Ecology and Systematics 35:31–54.

MacCready, P., 2004. Toward a unified theory of tidally-averaged estuarine salinity structure. Estuaries 27:561−570.

Mackin, J.G., 1956. Dermocystidium marinum and salinity. Proceedings of the National Shellfisheries Association 46:116–133.

Mackin, J.G., H.M. Owen, and A. Collier. 1950. Preliminary note on the occurrence of a new protistan parasite, Dermocystidium marinum n. sp. in Crassostrea virginica (Gmelin). Science 111:328–329.

Mann, R. 1991. Swimming rate and responses of larvae of three mactrid bivalves to salinity discontinuities. Marine Ecology Progress Series 92:107–116. 

Mesinger, F., G. DiMego, E. Kalnay, K. Mitchell, P.C. Shafran, W. Ebisuzaki, D. Jovic, J. Woollen, E. Rogers, and others. 2006. North American Regional Reanalysis. Bulletin of the American Meteorological Society 87:343–360. 

Milbury, C., X. Guo, D. Bushek, and S.E. Ford. 2008. Spatial population structure in Delaware Bay oysters. Journal of Shellfish Research 27(4):1033. (abstract)

Mukai, A., S. Takemoto, T. Higashi, and Y. Fukuda. 2001. Oceanic tidal loadings estimated from gravity observations in Kyoto and Bandung. Journal of the Geodynamics Society of Japan 47:261–266.

Najjar, R.G., H.A. Walker, P.J. Anderson, E.J. Barron, R.J. Bord, J.R. Gibson, V.S. Kennedy, C.G. Knight, J.P. Megonigal, R.E. O’Connor, and others. 2000. The potential impacts of climate change on the mid-Atlantic coastal region. Climate Research 14:219–233. 

National Research Council (NRC). 2004. Nonnative Oysters in the Chesapeake Bay. National Academy Press, Washington, DC, 325 pp.

Nell, J.A., and R.E. Hand. 2003. Evaluation of the progeny of second-generation Sydney rock oyster Saccostrea glomerata (Gould, 1850) breeding lines for resistance to QX disease Marteilia sydneyi. Aquaculture 228:27–35.

Oke, P.R., J.S. Allen, R.N. Miller, G.D. Egbert, J.A. Austin, J.A. Barth, T.J. Boyd, P.M. Kosro, and M.D. Levine. 2002. A modeling study of the three-dimensional continental shelf circulation off Oregon. Part I: Model-data comparisons. Journal of Physical Oceanography 32:1,360–1,382.

Powell, E.N., K.A. Ashton-Alcox, J.N. Kraeuter, S.E. Ford, and D. Bushek. 2008. Long-term trends in oyster population dynamics in Delaware Bay: Regime shifts and response to disease. Journal of Shellfish Research 27:729–755.

Powell, E.N., E.E. Hofmann, and J.M. Klinck. 1996. Modeling diseased oyster populations. II. Triggering mechanisms for Perkinsus marinus epizootics. Journal of Shellfish Research 15:141–165.

Powell, E.N., E.E. Hofmann, J.M. Klinck, and S.M. Ray. 1992. Modeling oyster populations. I. A commentary on filtration rate. Is faster always better? Journal of Shellfish Research 11:387–398.

Powell, E.N., J.M. Klinck, S.E. Ford, E.E. Hofmann, and S.J. Jordan. 1999. Modeling the MSX parasite in eastern oyster (Crassostrea virginica) populations. III. Regional application and the problem of transmission. Journal of Shellfish Research 18:517–537.

Powell, E.N., J. Song, M.S. Ellis, and E.A. Wilson-Ormond. 1995. The status and long-term trends in oyster reefs in Galveston Bay, Texas. Journal of Shellfish Research 14:439–457. 

Ragone Calvo, L.M., G.W. Calvo, and E.M. Burreson. 2003. Dual disease resistance in a selectively bred eastern oyster, Crassostrea virginica, strain tested in Chesapeake Bay. Aquaculture 220:69–87.

Rose, C.G., K.T. Paynter, and M.P. Hare. 2006. Isolation by distance in the eastern oyster, Crassostrea virginica, in Chesapeake Bay. Journal of Heredity 97:158–170, doi:10.1093/jhered/esj019.

Shchepetkin, A.F., and J.C. McWilliams. 2005. The regional oceanic modeling system (ROMS): A split-explicit, free-surface, topography-following-coordinate ocean model. Ocean Modelling 9:347–404. 

Smolarkiewicz, P.K., and J. Szmelter. 2005. Multidimensional positive definite advection transport algorithm (MPDATA): An edge-based unstructured-data formulation. International Journal for Numerical Methods in Fluids 47:1,293–1,295. 

Stokes, N.A., J.G. Walker, and E.M. Burreson. 1996. Comparison of Haplosporidium nelsoni diagnostic techniques: Polymerase chain reaction outperforms histology. Journal of Shellfish Research 15:498. (abstract)

Taylor, K.E. 2001. Summarizing multiple aspects of model performance in a single diagram. Geophysical Research Letters 106:7,183–7,192.

Versar, Inc. 2001. Pre-construction oyster, water quality, and sediment monitoring study for the Delaware River main channel deepening project, 2000/2001. Report prepared for US Army Corps of Engineers, Contract No. DCAW61-95-D-0011. Available online at: http://www.nap.usace.army.mil/cenap-pl/drmcdp/deldocs.html (accessed October 7, 2009).

Wang, Y., and X. Guo. 2008. Mapping disease-resistance genes in the eastern oyster (Crassostrea virginica). Journal of Shellfish Research 27(4):1,061–1,062. (abstract)

Whitney, M., and R. Garvine. 2006. Simulating the Delaware Bay buoyant outflow: Comparison with observations. Journal of Physical Oceanography 36:3–21.

Wong, K.-C., 1994. On the nature of transverse variability in a coastal plain estuary. Journal of Geophysical Research 99:14,209–14,222.

Yu, Z., and X. Guo. 2006. Identification and mapping of disease-resistance QTL in the eastern oyster, Crassostrea virginica Gmelin. Aquaculture 254:160–170. 

Zhang, L., X. Guo, D. Bushek, and S.E. Ford. 2008. Mapping quantitative trait loci conferring Dermo resistance in the eastern oyster Crassostrea virginica. Journal of Shellfish Research 27(4):1067. (abstract)

Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.