Can oysters crassostrea virginica develop resistance to dermo disease in the field: The impediment posed by climate cycles

Journal of Marine Research

Volumn 70, Issue 2-3, 2012, Pages 309-355

  Powell, Eric N ^a   Klinck, John M ^b   Guo, Ximing ^a   Hofmann, Eileen E ^b   Ford, Susan E ^a   Bushek, David ^a  

^a RUTGERS UNIVERSITY   (United States)

^b OLD DOMINION UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; BIVALVE; CLIMATE CONDITIONS; DISEASE RESISTANCE; FECUNDITY; GROWTH RESPONSE; HOST; MORTALITY; PATHOGEN; POPULATION DYNAMICS; SPAWNING; SURVIVAL;

ANIMALIA; CRASSOSTREA VIRGINICA; OSTREIDAE; PERKINSUS MARINUS;

EID: 84866770416     PISSN: 00222402     EISSN: 15439542     Source Type: Journal    
DOI: 10.1357/002224012802851896     Document Type: Article

References (178)

1. Addison, C. 2006. Oyster recruitment and early growth patterns in the Barataria Estuary. Masters Thesis, Nicholls State University, Thibodaux, Louisiana. 119 pp.
2. Andrews, J. D. 1954. Notes on fungus parasites of bivalve mollusks in Chesapeake Bay. Proc. Natl. Shellfish. Assoc., 45, 157-163.
3. Andrews, J. D. 1968. Oyster mortality studies in Virginia VII. Review of epizootiology and origin of Minchinia nelsoni. Proc. Natl. Shellfish. Assoc., 58, 23-36.
4. Andrews, J. D. 1988. Epizootiology of the disease caused by the oyster pathogen Perkinsus marinus and its effects on the oyster industry. Am. Fish. Soc. Spec. Publ., 18, 47-63.
5. Andrews, J. D. 1996. History of Perkinsus marinus, a pathogen of oysters in Chesapeake Bay 1950-1984. J. Shellfish Res., 15, 13-16.
6. Andrews, J. D. and W. G. Hewatt. 1957. Oyster mortality studies in Virginia. II. The fungus disease caused by Dermocystidium marinum in oysters of Chesapeake Bay. Ecol. Monogr., 27, 1-25.
7. Arizpa, C. O. 1996. Secondary production, growth and survival of the Pacific oysters Crassostrea virginica (Thunberg) in tropical waters, Bahia de la Paz, Mexico. J. Shellfish Res., 15, 601-607.
8. Attrill, M. J. and M. Power. 2002. Climatic influence on a marine fish assemblage. Nature (Lond.), 417, 275-278.
9. Audemard, C., L. M. Ragone Calvo, K. T. Paynter, K. S. Reece and E. M. Burreson. 2006. Realtime PCR investigation of parasite ecology: in situ determination of oyster parasite Perkinsus marinus transmission dynamics in lower Chesapeake Bay. Parasitology, 132, 827-842.
10. Barber, B. J., C. V. Davis and M. A. Crosby. 1998. Cultured oysters, Crassostrea virginica, genetically selected for fast growth in the Damariscotta River, Maine, are resistant to mortality caused by Juvenile Oyster Disease (JOD). J. Shellfish Res., 17, 1171-1175.
11. Barber, B. J., S. E. Ford and R. N. Wargo. 1991. Genetic variation in the timing of gonadal maturation and spawning of the Eastern oyster, Crassostrea virginica (Gmelin). Biol. Bull. (Woods Hole), 181, 216-224.
12. Bojariu, R. and L. Gimeno. 2003. Predictability and numerical modelling of the North Atlantic Oscillation. Earth-Sci. Rev., 63, 145-168.
13. Boots, M., P. J. Hudson and A. Sasaki. 2004. Large shifts in pathogen virulence relate to host population structure. Science (Wash. D.C.), 303, 842-844.
14. Brown, B. L., A. J. Butt, D. Meritt and K. T. Paynter. 2005a. Evaluation of resistance to Dermo in eastern oyster strains tested in Chesapeake Bay. Aquacult. Res., 36, 1544-1554.
15. Brown, B. L., A. J. Butt, S. W. Shelton, D. Meritt and K. T. Paynter. 2005b. Resistance of Dermo in eastern oysters, Crassostrea virginica (Gmelin), of North Carolina but not Chesapeake Bay heritage. Aquacult. Res., 36, 1391-1399.
16. Burreson, E. M. 1991. Effects of Perkinsus marinus infection in the eastern oyster, Crassostrea virginica: I. Susceptibility of native and MSX-resistant stocks. J. Shellfish Res., 10, 417-423.
17. Burreson, E. M. and S. E. Ford. 2004. A review of recent information on the Haplosporidia, with special reference to Haplosporidium nelsoni (MSX disease). Aquat. Living Resour., 17, 499-517.
18. 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. J. Shellfish Res., 15, 17-34.
19. 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. J. Aquat. Anim. Health, 12, 1-8.
20. Bushek, D. and S. K. Allen Jr. 1996. Host-parasite interactions among broadly distributed populations of the eastern oyster Crassostrea virginica and the protozoan Perkinsus marinus. Mar. Ecol. Prog. Ser., 139, 127-141.
21. Bushek D., S. E. Ford and I. Burt. 2012. Long-term patterns of an estuarine pathogen along a salinity gradient. J. Mar. Res., 70, 225-251.
22. Bushek, D., B. Landau and E. Scarpa. 2008.Perkinsus chesapeaki in stout razor clams Tagelus plebeius from Delaware Bay. Dis. Aquat. Org., 78, 243-247.
23. Cane, M. A. 2005. The evolution of El Niño, past and future. Earth Planet. Sci. Lett., 230, 227-240.
24. Carnegie, R. B. and E. M. Burreson. 2011. Declining impact of an introduced pathogen: Haplosporidium nelsoni in the oyster Crassostrea virginica in Chesapeake Bay. Mar. Ecol. Prog. Ser., 432, 1-15.
25. Choi, K-S., D. H. Lewis, E. N. Powell, P. F. Frelier and S. M. Ray. 1991. A polyclonal antibody developed from Perkinsus marinus hypnospores fails to cross react with other life stages of P. marinus in oyster (Crassostrea virginica) tissues. J. Shellfish Res., 10, 411-415.
26. Choi, K-S., D. H. Lewis, E. N. Powell and S. M. Ray. 1993. Quantitative measurement of reproductive output in the American oyster, Crassostrea virginica (Gmelin), using an enzyme-linked immunosorbent assay (ELISA). Aquacult. Fish. Manage., 24, 299-322.
27. Choi, K-S., E. N. Powell, D. H. Lewis and S. M. Ray. 1994. Instantaneous reproductive effort in female American oysters, Crassostrea virginica, measured by a new immunoprecipitation assay. Biol. Bull. (Woods Hole), 186, 41-61.
28. Choi, K-S., E. A. Wilson, D. H. Lewis, E. N. Powell and S. M. Ray. 1989. The energetic cost of Perkinsus marinus parasitism in oysters: quantification of the thioglycollate method. J. Shellfish Res., 8, 125-131.
29. Cook, T., M. Folli, J. Klinck, S. Ford and J. Miller. 1998. The relationship between increasing seasurface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuar. Coast. Shelf Sci., 46, 587-597.
30. Cotter, S. C., L. E. B. Kruuk and K. Wilson. 2004. Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J. Evol. Biol., 17, 421-429.
31. Craig, A., E. N. Powell, R. R. Fay and J. M. Brooks. 1989. Distribution of Perkinsus marinus in Gulf coast oyster populations. Estuaries, 12, 82-91.
32. Crosby, M. P. and C. F. Roberts. 1990. Seasonal infection intensity cycle of the parasite Perkinsus marinus (and an absence of Haplosporidium spp.) in oysters from a South Carolina salt marsh. Dis. Aquat. Org., 9, 149-155.
33. Dawe, E. G., E. B. Colbourne and K. F. Drinkwater. 2000. Environmental effects on recruitment of short-finned squid (Illex illecebrosus). ICES J. Mar. Sci., 57, 1002-1013.
34. Dawson, C. E. 1955. Observations on the incidence of Dermocystidium marinum infection in oysters of Apalachicola Bay, Florida. Tex. J. Sci., 7, 47-56.
35. Detilleux, J. C. 2005. Genetic management of infectious diseases: a heterogeneous epidemio-genetic model illustrated with S. aureus mastitis. Genet. Sci. Evol., 37, 437-453.
36. Dittman, D. E., S. E. Ford and D. K. Padilla. 2001. Effects of Perkinsus marinus on reproduction and condition of the eastern oyster, Crassostrea virginica, depend on timing. J. Shellfish Res., 20, 1025-1034.
37. Dong, Q. 2005. Comparative studies of sperm cryopreservation of diploid and tetraploid Pacific oysters. Ph.D. Dissertation, Louisiana State University, Baton Rouge, Louisiana, 271 pp.
38. Douglas, A. V. and P. J. Englehart. 1981. On a statistical relationship between Autumn rainfall in the central equitorial Pacific and subsequent winter precipitation in Florida. Mon. Weather Rev., 109, 2377-2382.
39. Duffy, M. A. and S. E. Forde. 2009. Ecological feedbacks and the evolution of resistance. J. Anim. Ecol., 78, 1106-1112.
40. Duffy, M. A., S. R. Hall, C. E. Cáceres and A. R. Ives. 2009. Rapid evolution, seasonality, and the termination of parasite epidemics. Ecology, 90, 1441-1448.
41. Duffy, M. A. and L. Sivars-Becker. 2007. Rapid evolution and ecological host-parasite dynamics. Ecol. Lett., 10, 44-53.
42. Dungan, C. F. and B. S. Roberson. 1993. Binding specificities of mono- and polyclonal antibodies to the protozoan oyster pathogen Perkinsus marinus. Dis. Aquat. Org., 15, 9-22.
43. Earnhart, C. G., M. A. Vogelbein, G. D. Brown, K. S. Reece and S. L. Kaattari. 2004. Supplementation of Perkinsus marinus cultures with host plasma or tissue homogenate enhances their infectivity. Appl. Environ. Microbiol., 70, 421-431.
44. Ebbesmeyer, C. C. and R. M. Strickland. 1995. Oyster condition and climate: evidence from Willapa Bay. Washington Sea Grant Program, Seattle, WN, USG-M9 95-02, 11 pp.
45. Elderd, B. D., J. Dushoff and G. Dwyer. 2008. Host-pathogen interactions, insect outbreaks, and natural selection for disease resistance. Am. Nat., 172, 829-842.
46. Encomio, V. G., S. M. Stickler, S. K. Allen Jr. and F-L. Chu. 2005. Performance of "natural Dermoresistant" oyster stocks - survival, disease, growth, condition and energy reserves. J. Shellfish Res., 24, 143-155.
47. Fabens, A. J. 1965. Properties and fitting of the von Bertalanffy growth curve. Growth, 29, 265-289.
48. Farley, C. A. 1975. Epizootic and enzootic aspects of Minchinia nelsoni (Haplosporida) disease in Maryland oysters. J. Protozool., 22, 418-427.
49. Fegley, S. R., S. E. Ford, J. N. Kraeuter and H. H. Haskin. 2003. The persistence of New Jersey's oyster seedbeds in the presence of oyster disease and harvest: the role of management. J. Shellfish Res., 22, 451-464.
50. Felsenstein, J. 1971. Inbreeding and variance effective numbers in populations with overlapping generations. Genetics, 68, 581-597.
51. Ford, S. E. 1988. Host-parasite interactions in eastern oysters selected for resistance to Haplosporidium nelsoni (MSX) disease: survival mechanisms against a natural pathogen. Am. Fish. Soc. Spec. Publ., 18, 206-224.
52. Ford, S. E. 1996. Range extension by the oyster parasite Perkinsus marinus into the northeastern United States: response to climate change. J. Shellfish Res., 15, 45-56.
53. Ford, S. E. and H. H. Haskin. 1982. History and epizootiology of Haplosporidium nelsoni (MSX), an oyster pathogen in Delaware Bay, 1957-1980. J. Invertebr. Pathol., 40, 118-141.
54. Ford, S. E., A. Schotthoefer and C. Spruck. 1999. In vivo dynamics of the microparasite Perkinsus marinus during progression and regression of infections in eastern oysters. J. Parasitol., 85, 273-285.
55. Ford, S. E. and R. Smolowitz. 2007. Infection dynamics of an oyster parasite in its newly expanded range. Mar. Biol. (Berl.), 151, 119-133.
56. Ford, S. E. and M. R. Tripp. 1996. Diseases and defense mechanisms, in The eastern oyster: Crassostrea virginica, V. S. Kennedy, R. I. E. Newell and A. F. Eble, eds., College Park, Maryland, Maryland Sea Grant College Program, 581-659.
57. Froese, R. 2006. Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. J. Appl. Ichthyol., 22, 241-253.
58. Fromentin, J-M. and B. Planque. 1996. Calanus and environment in the eastern North Atlantic. II. Influence of the North Atlantic Oscillation in C. finmarchicus and C. helgolandicus. Mar. Ecol. Prog. Ser., 134, 111-118.
59. Gaffney, P. M. and D. Bushek. 1996. Genetic aspects of disease resistance in oysters. J. Shellfish Res., 15, 135-140.
60. Gallagher, S. M. and R. Mann. 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.
61. Goedken, M., B. Morsey, I. Sunila and S. de Guise. 2005. Immunomodulation of Crassostrea gigas and Crassostrea virginica cellular defense mechanisms by Perkinsus marinus. J. Shellfish Res., 24, 487-496.
62. Gómez-León, J., L. Villamil, S. A. Salger, R. H. Sallum, A. Remacha-Triviño, D. F. Leavitt and M. Gómez-Chiarri. 2008. Survival of eastern oysters Crassostrea virginica from three lines following experimental challenge with bacterial pathogens. Dis. Aquat. Org., 79, 95-105.
63. Gompertz, B. 1825. XXIV. On the nature of the function expressive of the law of human mortality, and on a new mode of determining the value of life contingencies. Phil. Trans. R. Soc. Lond., 115, 513-585.
64. Guo, X., D. Hedgecock, W. K. Hershberger, K. Cooper and S. K. Allen Jr. 1998. Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution, 52, 394-402.
65. Gray, J. S. and H. Christie. 1983. Predicting long-term changes in marine benthic communities. Mar. Ecol. Progr. Ser., 13, 87-94.
66. Hancock, D. A. 1973. The relationship between stock and recruitment in exploited invertebrates. Rapp. P-v. Réun Cons. Int. Explor. Mer, 164, 113-131.
67. Harding, J. M., R. Mann and M. J. Southworth. 2008. Shell length-at-age relationships in James River, Virginia, oysters (Crassostrea virginica) collected four centuries apart. J. Shellfish Res., 27, 1109-1115.
68. Harding, J. M., R. Mann, M. J. Southworth and J. A. Wesson. 2010. Management of the Piankatank River,Virginia, in support of oyster (Crassostrea virginica, Gmelin 1791) fishery repletion. J. Shellfish Res., 29, 867-888.
69. Harvell, C. D., C. E. Mitchell, J. R. Ward, S. A. Altizer, A. P. Dobson, R. S. Ostfeld and M. D. Samuel. 2002. Climate warming and disease risks for terrestrial and marine biota. Science (Wash. D.C.), 296, 2158-2162.
70. 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. Mar. Fish. Rev., 41, 54-63.
71. Hasu, T., D. P. Benesh and E. T. Valtonen. 2009. Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations. J. Evol. Biol., 22, 699-707.
72. Hayes, M. L., J. Bonaventura, T. P. Mitchell, J. M. Prospero, E. A. Shinn, F. van Dolah and R. T. Barber. 2001. How are climate and marine biological outbreaks functionally linked? Hydrobiologia, 460, 213-220.
73. Hayes, P. F. and R. W. Menzel. 1981. The reproductive cycle of early setting Crassostrea virginica (Gmelin) in the northern Gulf of Mexico, and its implications for population recruitment. Biol. Bull. (Woods Hole), 160, 80-88.
74. He, Y., S. Ford, D. Bushek, E. Powell, Z. Bao and X. Guo. 2012. Effective population sizes of eastern oyster Crassostrea virginica (Gmelin) populations in Delaware Bay, USA. J. Mar. Res., 70, 357-379.
75. Hedgecock, D. 1994. Does variability in reproductive success limit effective population sizes of marine organisms?, in Genetics and Evolution of Aquatic Organisms, A. R. Beaumont, ed., Chapman & Hall, London, 122-134.
76. 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.
77. Hedgecock, D., S. Launey, A. I. Pudovkin, Y. Naciri, S. Lapègue and F. Bonhomme. 2007. Small effective number of parents (Nb) inferred for a naturally spawned cohort of juvenile European flat oysters Ostrea edulis. Mar. Biol. (Berl.), 150, 1173-1182.
78. Hedgecock, D., D. J. McGoldrick and B. L. Bayne. 1995. Hybrid vigor in Pacific oysters: an experimental approach using crosses among inbred lines. Aquaculture, 137, 285-298.
79. Hedgecock, D., D. J. McGoldrick, D. T. Manahan, J. Vavra, N. Appelmans and B. L. Bayne. 1996. Quantitative and molecular genetic analyses of heterosis in bivalve molluscs. J. Exp. Mar. Biol. Ecol., 203, 49-59.
80. Héral, M. and J. M. Deslous-Paoli. 1983. Valeur énergétique de la chain de l'hûrtre Crassostrea gigas estimée par mesures microcalorimetriques et par dosages biochimiques. Ocean. Acta, 6, 193-199.
81. Hewatt, W. G. and J. D. Andrews. 1954. Oyster mortality studies in Virginia. I Mortalities of oysters in trays at Gloucester Point, York River. Tex. J. Sci., 6, 121-133.
82. Hoenig, J. M. 1983. Empirical use of longevity data to estimate mortality rates. Fish. Bull., 83, 898-903.
83. Hofmann, E., D. Bushek, S. Ford, X. Guo, D. Haidvogel, D. Hedgecock, J. Klinck, C. Milbury, D. Narvaez, E. Powell, Y. Wang, Z. Wang, J. Wilkin, and L. Zhang. 2009. Understanding how disease and environment combine to structure resistance in estuarine bivalve populations. Oceanography, 22, 212-231.
84. Hofmann, E. E., J. M. Klinck, J. N. Kraeuter, E. N. Powell, R. E. Grizzle, S. C. Buckner and V. M. Bricelj. 2006. A population dynamics model of the hard clam, Mercenaria mercenaria: development of the age- and length-frequency structure of the population. J. Shellfish Res., 25, 417-444.
85. Hofmann, E. E., J. M. Klinck, E. N. Powell, S. Boyles and M. Ellis. 1994. Modeling oyster populations II. Adult size and reproductive effort. J. Shellfish Res., 13, 165-182.
86. Hofmann, E. E., E. N. Powell, J. M. Klinck and G. Saunders. 1995. Modeling diseased oyster populations I. Modelling Perkinsus marinus infections in oysters. J. Shellfish Res., 14, 121-151.
87. Hofmann, E. E., E. N. Powell, J. M. Klinck and E. A. Wilson. 1992. Modeling oyster populations. III. Critical feeding periods, growth and reproduction. J. Shellfish Res., 11, 399-416.
88. Hopkins, S. H. 1954. Oyster setting on the Gulf coast. Proc. Natl. Shellfish. Assoc., 45, 52-55.
89. Hurrell, J.W. and H. van Loon. 1997. Decadal variations in climate associated with the North Atlantic Oscillation. Climate Change, 36, 301-326.
90. Jaenike, J. 2002. Time-delayed effects of climate variation on host-parasite dynamics. Ecology, 83, 917-924.
91. Jensen, A. L. 1997. Origin of the relation between K and Linf and synthesis of relations among life history parameters. Can. J. Fish. Aquat. Sci., 54, 987-989.
92. Kahya, E. and J. A. Dracup. 1993. U.S. streamflow patterns in relation to the El Niño/Southern Oscillation. Wat. Resour. Res., 29, 2491-2503.
93. Kang, S-G., K-S. Choi, A. A. Bulgakov, Y. Kim and S-Y. Kim. 2003. Enzyme-linked immunosorbent assay (ELISA) used in quantification of reproductive output in the Pacific oyster, Crassostrea gigas, in Korea. J. Exp. Mar. Biol. Ecol., 282, 1-21.
94. Kennedy, V. S. 1983. Sex ratios in oysters, emphasizing Crassostrea virginica from Chesapeake Bay, Maryland. Veliger, 25, 329-338.
95. Kennedy, V. S. and C. B. Krantz. 1982. Comparative gametogenic and spawning patterns of the oyster Crassostrea virginica (Gmelin) in central Chesapeake Bay. J. Shellfish Res., 2, 133-140.
96. Kim, Y. and E. N. Powell. 1998. Influence of climate change on interannual variation in population attributes of Gulf of Mexico oysters. J. Shellfish Res., 17, 265-274.
97. Kim, Y. and E. N. Powell. 2006. Relationships among parasites and pathologies in sentinel bivalves: NOAA Status and Trends "Mussel Watch" Program. Bull. Mar. Sci., 79, 83-112.
98. Kim, Y. and E. N. Powell. 2007. Distribution of parasites and pathologies in sentinel bivalves: NOAA status and trends "Mussel Watch" program. J. Shellfish Res., 26, 1115-1151.
99. Kim, Y. and E. N. Powell. 2009. Effects of climate variability on interannual variation in parasites, pathologies, and physiological attributes of bivalves from the U.S. East, Gulf, and West coasts. Environ. Bioindicators, 4, 67-96.
100. Kim, Y., E. N. Powell, T. L. Wade, B. J. Presley and J. M. Brooks. 1999. Influence of climate change on interannual variation in contaminant body burden in Gulf of Mexico oysters. Mar. Environ. Res., 48, 459-488.
101. Kim, Y., E. N. Powell, T. L. Wade, B. J. Presley and J. M. Brooks. 2001. The geographic distribution of population health and contaminant body burden in Gulf of Mexico oysters. Arch. Environ. Contam. Toxicol., 41, 30-46.
102. Kobayashi, M., E. E. Hofmann, E. N. Powell, J. M. Klinck and K. Kusaka. 1997. A population dynamics model for the Japanese oyster, Crassostrea gigas. Aquaculture, 149, 285-321.
103. Kraeuter, J. N., S. Buckner and E. N. Powell. 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. J. Shellfish Res., 24, 1043-1052.
104. Kraeuter, J. N., S. Ford and M. Cummings. 2007. Oyster growth analysis: a comparison of methods. J. Shellfish Res., 26, 479-491.
105. Kraeuter, J. N., J. M. Klinck, E. N. Powell, E. E. Hofmann, S. C. Buckner, R. E. Grizzle and V. M. Bricelj. 2008. Effects of the fishery on the northern quahog (=hard clam, Mercenaria mercenaria L.) population in Great South Bay, New York: a modeling study. J. Shellfish Res., 27, 653-666.
106. Launey, S. and D. Hedgecock. 2001. High genetic load in the Pacific oyster Crassostrea gigas. Genetics, 159, 255-265.
107. Leethochavalit, S., K. Chalermwat, E. S. Upatham, K-S. Choi, P. Sawangwong and M. Kruatrachue. 2004. Occurrence of Perkinsus sp. in undulated surf clams Paphia undulata from the Gulf of Thailand. Dis. Aquat. Org., 60, 165-171.
108. Mackin, J. G. 1953. Incidence of infection of oysters by Dermocystidium in the Barataria Bay area of Louisiana. Natl. Shellfish. Assoc. Conv. Add., 22-35.
109. Mackin, J. G. 1959. A method of estimation of mortality rates in oysters. Proc. Natl. Shellfish. Assoc., 50, 41-51.
110. Mackin, J. G. 1962. Oyster disease caused by Dermocystidium marinus and other microorganisms in Louisiana. Publ. Inst. Mar. Sci. Univ. Texas, 7, 132-229.
111. Mackin, J. G. and S. H. Hopkins. 1962. Studies on oyster mortality in relation to natural environments and to oil fields in Louisiana. Publ. Inst. Mar. Sci. Univ. Tex., 7, 1-131.
112. Mackin, J. G. and A. K. Sparks. 1962. A study of the effect on oysters of crude oil loss from a wild well. Publ. Inst. Mar. Sci. Univ. Tex., 7, 230-261.
113. Mackin, J. G., B. Welch and C. Kent. 1950. A study of mortality of oysters of the Buras area of Louisiana. Texas A&M Research Foundation Project Report, Project #9; College Station, Texas, 41 pp.
114. Mancera, E. and J. Mendo. 1996. Population dynamics of the oyster Crassostrea rhizophorae from the Ciénaga Grande de Santa Marta, Colombia. Fish. Res., 26, 139-148.
115. Mann, R. and D. A. Evans, 2004. Site selection for oyster habitat rehabilitation in the Virginia portion of the Chesapeake Bay: a commentary. J. Shellfish Res., 23, 41-49.
116. Mann, R., M. Southworth, J. M. Harding and J. A. Wesson. 2009. Population studies of the native eastern oyster, Crassostrea virginica, (Gmelin, 1791) in the James River, Virginia, USA. J. Shellfish Res., 28, 193-220.
117. McCollough, C. B., B. W. Albright, G. R. Abbe, L. S. Barker and C. F. Dungan. 2007. Acquisition and progression of Perkinsus marinus infections by specific-pathogen-free juvenile oysters (Crassostrea virginica Gmelin) in a mesohaline Chesapeake Bay tributary. J. Shellfish Res., 26, 465-477.
118. McLaughlin, S. M., E. E. Elsayed and M. Faisal. 2000. Analysis of extracellular proteins of two Perkinsus spp. isolated from the softshell clam Mya arenaria in vitro. Comp. Biochem. Physiol. B Comp. Biochem., 126, 587-598.
119. Montes, J. F., M. Durfort and J. Garcia-Valero. 2005. Ultrastructural localization of antigenic determinants conserved during Perkinsus atlanticus trophozoite to prezoosporangium differentiation. Dis. Aquat. Org., 66, 33-40.
120. Moore, H. F. 1907. Survey of oyster bottoms in Matagorda Bay, Texas. U.S. Bur. Fish Doc., 610, 86 pp.
121. Morton, B. 1990. Life cycle and sexual strategy of Saccostrea cucullata (Bivalvia: Ostreidae) from a Hong Kong mangrove. Am. Malacol. Bull., 8, 1-8.
122. Mouritsen, K. N. and R. Poulin. 2002. Parasitism, climate oscillations and the structure of natural communities. Oikos, 97, 462-468.
123. Mullin, M. M. 1995. The Californian El Niño of 1992 and the fall of Calanus. CCOFI Rep., 36, 175-178.
124. Ngo, T. T. T. and K-S. Choi. 2004. Seasonal changes of Perkinsus and Cercaria infections in the Manila clam Ruditapes philippinarum from Jeju, Korea. Aquaculture, 239, 57-68.
125. Ngo, T. T. T., S-G. Kang, D-H. Kang, P. Sorgeloos and K-S. Choi. 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.
126. Notaro, M., W-C. Wang and W. Gong. 2006. Model and observational analysis of the northeast U.S. regional climate and its relationship to the PNA and NAO patterns during early winter. Mon. Weather Rev., 134, 3479-3505.
127. Oliva M. E., I. Barrios, S. Thatje and J. Laudie. 2008. Changes in prevalence and intensity of infection of Profilicollis altmani (Perry, 1942) cystacanth (Acanthocephala) parasitizing the mole crab Emerica analoga (Stimpson, 1857): an El Niño cascade effect? Helgol. Mar. Res., 62 (Suppl. 1), S57-S62.
128. Oliver, L. M., W. S. Fisher, A. K. Volety and Z. Malaeb. 2003. Greater hemocyte bactericidal activity in oysters (Crassostrea virginica) from a relatively contaminated site in Pensacola Bay, Florida. Aquat. Toxicol., 64, 363-373.
129. Owen, H. M. 1953. The relationship of high temperatures and low rainfall to oyster production in Louisiana. Bull. Mar. Sci. Gulf Caribb., 3, 34-43.
130. Panko, C., V. Encomio, J. Barreto and A. K. Volety. 2008. In vitro and in vivo evaluation of quinine as a potential anti-protozoal for the eastern oyster parasite Perkinsus marinus. J. Shellfish Res., 27, 789-793.
131. Parry, G. D. 1981. The meanings of r- and k-selection. Oecologia (Berl.), 48, 260-264.
132. Paynter, K. T. 1996. The effects of Perkinsus marinus infection on physiological processes in the eastern oyster, Crassostrea virginica. J. Shellfish Res., 15, 119-125.
133. Peterson, C. H. and H. C. Summerson. 1992. Basin-scale coherences of population dynamics of an exploited marine invertebrate, the bay scallop: implications of recruitment limitation. Mar. Ecol. Prog. Ser., 90, 257-272.
134. 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. J. Shellfish Res., 27, 729-755.
135. Powell, E. N. and H. C. Cummins. 1985. Are molluscan maximum life spans determined by long-term cycles in benthic communities? Oecologia (Berl.), 67, 177-182.
136. Powell, E. N., J. D. Gauthier, E.A. Wilson, A. Nelson, R. R. Fay and J. M. Brooks. 1992. Oyster disease and climate change. Are yearly changes in Perkinsus marinus parasitism in oysters (Crassostrea virginica) controlled by climatic cycles in the Gulf of Mexico? P.S.Z.N.I.: Mar. Ecol., 13, 243-270.
137. Powell, E. N., J. M. Klinck, K. A. Ashton-Alcox and J. N. Kraeuter. 2009a. Multiple stable reference points in oyster populations: biological relationships for the eastern oyster (Crassostrea virginica) in Delaware Bay. Fish. Bull., 107, 109-132.
138. Powell, E. N., J. M. Klinck, K. A. Ashton-Alcox and J. N. Kraeuter 2009b. Multiple stable reference points in oyster populations: implications for reference pointbased management. Fish. Bull., 107, 133-147.
139. Powell, E. N., J. M. Klinck, X. Guo, E. E. Hofmann, S. E Ford and D. Bushek. 2011a. The potential for oysters, Crassostrea virginica, to develop resistance to Dermo disease in the field: evaluation using a gene-based population dynamics model. J. Shellfish Res., 30, 685-712.
140. Powell, E. N., J. M. Klinck and E. E. Hofmann. 1996. Modeling diseased oyster populations. II. Triggering mechanisms for Perkinsus marinus epizootics. J. Shellfish Res., 15, 141-165.
141. Powell, E. N., J. M. Klinck and E. E. Hofmann. 2011b. Generation time and the stability of sex-determining alleles in oyster populations as deduced using a gene-based population dynamics model. J. Theor. Biol., 271, 27-43.
142. Powell, E. N., J. M. Morson, K. A. Ashton-Alcox and Y. Kim. 2012. Accommodation of the sex ratio in eastern oysters Crassostrea virginica to variation in growth and mortality across the estuarine salinity gradient in Delaware Bay. J. Mar. Biol. Assoc. U. K.
143. Powell, E. N., J. Morson and J. M. Klinck. 2011c. Application of a gene-based population dynamics model to the optimal egg size problem: why do bivalve planktotrophic eggs vary in size? J. Shellfish Res. 30, 403-423.
144. Powell, E. N. and R. J. Stanton Jr. 1985. Estimating biomass and energy flow of molluscs in paleocommunities. Palaeontology (Lond.), 28, 1-34.
145. Press, W. H., B. P. Flannery, S. A. Teukolsky and W. T. Vettering. 1986. Numerical recipes, the art of scientific computing. Cambridge University Press, Cambridge.
146. Quick Jr., J. A. and J. G. Mackin. 1971. Oyster parasitism by Labyrinthomyxa marina in Florida. Fl. Dept. Nat. Resour. Prof. Pap. Ser., No. 13, 55 pp.
147. 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.
148. Ragone Calvo, L. M., R. L. Wetzel and E. M. Burreson. 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. J. Shellfish Res., 20, 231-241.
149. Ray, S.M. 1996. Historical perspective on Perkinsus marinus disease of oysters in the Gulf of Mexico. J. Shellfish Res., 15, 9-11.
150. Ray, S.M. and A. C. Chandler. 1955. Dermocystidium marinum, a parasite of oysters. Exp. Parasitol., 4, 172-200.
151. Reece, K. S., D. Bushek, K. L. Hudson and J. E. Graves. 2001. Geographic distribution of Perkinsus marinus genetic strains along the Atlantic and Gulf coasts of the USA. Mar. Biol. (Berl.), 139, 1047-1055.
152. Rothschild, B. J., J. S. Ault, P. Goulletquer and M. Héral. 1994. Decline of the Chesapeake Bay oyster populations: a century of habitat destruction and overfishing. Mar. Ecol. Prog. Ser., 111, 29-39.
153. Saunders, G. L., E. N. Powell and D. H. Lewis. 1993. A determination of in vivo growth rates for Perkinsus marinus, a parasite of the Eastern oyster Crassostrea virginica (Gmelin, 1791). J. Shellfish Res., 12, 229-240.
154. Schmidt, N. and M. E. Luther. 2002. ENSO impacts on salinity in Tampa Bay, Florida. Estuaries, 25, 976-984.
155. Schneider, D. S. and J. S. Ayres. 2008. Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat. Rev. Immunol., 8, 889-895.
156. Schoener, A. and D. F. Tufts. 1987. Changes in oyster condition index with El Niño-Southern Oscillation events at 46° N in an eastern Pacific bay. J. Geophys. Res., 92, 14429-14435.
157. Sokolova, I. M., J. D. Oliver and L. J. Leamy. 2006. An AFLP approach to identify genetic markers associated with resistance in Vibrio vulnificus and Perkinsus marinus in eastern oysters. J. Shellfish Res., 25, 95-100.
158. Soniat, T. M. 1985. Changes in levels of infection of oysters by Perkinsus marinus, with special reference to the interaction of temperature and salinity upon parasitism. N.E. Gulf Sci., 7, 171-174.
159. Soniat, T. M. and M. S. Brody. 1988. Field validation of a habitat suitability index model for the American oyster. Estuaries, 11, 87-95.
160. Soniat, T. M. and J. D. Gauthier. 1989. The prevalence and intensity of Perkinsus marinus from the mid northern Gulf of Mexico, with comments on the relationship of the oyster parasite to temperature and salinity. Tul. Stud. Zool. Bot., 27, 21-27.
161. Soniat, T. M., E. E. Hofmann, J. M. Klinck and E. N. Powell. 2009. Differential modulation of eastern oyster (Crassostrea virginica) disease parasites by the El Niño-Southern Oscillation and the North Atlantic Oscillation. Int. J. Earth Sci., 98, 99-114.
162. Soniat, T. M., J. M. Klinck, E. N. Powell and E. E. Hofmann. 2006. Understanding the success and failure of oyster populations: climatic cycles and Perkinsus marinus. J. Shellfish Res., 25, 83-93.
163. Stauber, L. A. 1950. The problem of physiological species with special reference to oysters and oyster drills. Ecology, 31, 109-118.
164. Stearns, S. 1976. Life-history tactics: a review of the ideas. Quart. Rev. Biol., 51, 3-47.
165. Thatje, S., O. Heilmayer and J. Laudien. 2008. Climate variability and El Niño Southern Oscillation: implications for natural coastal resources and management. Helgol. Mar. Res., 62 (Suppl. 1), S5-S14.
166. Tolan, J. M. 2007. El Niño-Southern Oscillation impacts translated to the watershed scale: estuarine salinity patterns along the Texas Gulf coast, 1982 to 2004. Estuar. Coast. Shelf Sci., 72, 247-260.
167. Tunberg, B. G. and W. G. Nelson. 1998. Do climatic oscillations influence cyclical patterns of soft bottom macrobenthic communities in the Swedish west coast? Mar. Ecol. Prog. Ser., 170, 85-94.
168. Volety, A. K., F. O. Perkins, R. Mann and P. R. Hershberg. 2000. Progression of diseases caused by the oyster parasites, Perkinsus marinus and Haplosporidium nelsoni, in Crassostrea virginica on constructed intertidal reefs. J. Shellfish Res., 19, 341-347.
169. Waaij, E. H. van der, P. Bijma, S. C. Bishop and J. A. M. van Arendonk. 2000. Modeling selection for production traits under constant infection pressure. J. Anim. Sci., 78, 2809-2820.
170. Wang, Y. and X. Guo. 2007. Development and characterization of EST-SSR markers in the eastern oyster Crassostrea virginica. Mar. Biotechnol., 9, 500-511.
171. Wang, Y., Z. Xu, J. C. Pierce and X. Guo. 2005. Characterization of eastern oyster (Crassostrea virginica Gmelin) chromosomes by fluorescence in situ hybridization with bacteriophage P1 clones. Mar. Biotechnol., 7, 207-214.
172. Wang, Z. P., X. Guo, S. K. Allen Jr. and R. Wang. 1999. Aneuploid Pacific oyster (Crassostrea gigas Thunberg) as incidentals from triploid production. Aquaculture, 173, 347-357.
173. Wilson, E. A., E. N. Powell, M. A. Craig, T. L. Wade and J. M. Brooks. 1990. The distribution of Perkinsus marinus in Gulf coast oysters: its relationship with temperature, reproduction, and pollutant body burden. Int. Rev. Gesamten Hydrobiol., 75, 533-550.
174. Wilson, E. A., E. N. Powell, T. L. Wade, R. J. Taylor, B. J. Presley and J. M. Brooks. 1992. Spatial and temporal distributions of contaminant body burden and disease in Gulf of Mexico oyster populations: the role of local and large-scale climatic controls. Helgol. Meeresunters., 46, 201-235.
175. Wilson-Ormond, E. A., E. N. Powell and S. M. Ray. 1997. Short-term and small-scale variation in food availability to natural oyster populations: food, flow and flux. P.S.Z.N.I. Mar. Ecol., 18, 1-34.
176. Yoo, S. K. and M. S. Yoo, 1973. Biological studies on oyster culture (II) morphological characteristics of the oyster, Crassostrea gigas. Bull. Korean Fish. Soc., 6, 65-74.
177. Zbinden, M., C. R. Haag and D. Ebert. 2008. Experimental evolution of field populations of Daphnia magna in response to parasite treatment. J. Evol. Biol., 21, 1068-1078.
178. Zuur, A. F. and G. J. Pierce. 2004. Common trends in northeast Atlantic squid time series. J. Sea Res., 52, 57-72.