Modeling diseased oyster populations. II. Triggering mechanisms for Perkinsus marinus epizootics

Journal of Shellfish Research

Volumn 15, Issue 1, 1996, Pages 141-165

  Powell, Eric N ^a,c   Klinck, John M ^b   Hofmann, Eileen E ^b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b OLD DOMINION UNIVERSITY   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Crassostrea virginica; Disease model; Eastern oysters; Oyster disease; Perkinsus marinus disease

Indexed keywords

EPIZOOTICS; MODELLING; OYSTER POPULATIONS; TRIGGERING MECHANISMS;

CRASSOSTREA VIRGINICUS; PERKINSUS MARINUS;

EID: 0029753740     PISSN: 07308000     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (108)

1. Ackerman, E., L. R. Elveback & J. P. Fox. 1984. Simulation of Infectious Disease Epidemics. Charles C. Thomas, Springfield, Illinois, 202 pp.
2. Anderson, R. M. 1991. Discussion: the Kermack-McKendrick epidemic threshold theorem. Bull. Math. Biol. 53:3-32.
3. Anderson, R. S., K. T. Paynter & E. M. Burreson. 1992. Increased reactive oxygen intermediate production by hemocytes withdrawn from Crassostrea virginica infected with Perkinsus marinus. Biol. Bull. 183:476-481.
4. Andrews, J. D. 1965. Infection experiments in nature with Dermocystidium marinum in Chesapeake Bay. Chesapeake Sci. 6:60-67.
5. Andrews, J. D. 1988. Epizootiology of the disease caused by the oyster pathogen Perkinsus marinus and its effects on the oyster industry. Amer. Fish. Soc. Spec. Publ. 18:47-63.
6. Andrews, J. D. & S. M. Ray. 1988. Management strategies to control the disease caused by Perkinsus marinus. Amer. Fish. Soc. Spec. Publ. 18:257-264.
7. Bartlett, M. S. 1960. The critical community size for measles in the United States. J. Royal Stat. Soc. Ser. A 123:37-44.
8. Baughman, J. L. & B. B. Baker, Jr. 1949. Oysters in Texas. Texas Game Fish. Oyster Comm. Bull. 29, Mar. Lab. Ser. 1, 38 pp.
9. Black, F. L. 1966. Measles endemicity in insular populations: critical community size and its evolutionary implication. J. Theo. Biol. 11: 207-211.
10. Brousseau, D. J., J. A. Baglivo & G. E. Lang, Jr. 1982. Estimation of equilibrium settlement rates for benthic marine invertebrates: its application to Mya arenaria (Mollusca: Pelecypoda). U.S. Fish Wild. Ser. Fish. Bull. 80:642-644.
11. Burrell, V. G., Jr., M. Y. Bobo & J. J. Manzi. 1984. A comparison of seasonal incidence and intensity of Perkinsus marinus between subtidal and intertidal oyster populations in South Carolina. J. World Maricult. Soc. 153:301-309.
12. Chanley, P. E. 1957. Survival of some juvenile bivalves in water of low salinity. Proc. Natl. Shellfish. Assoc. 48:52-65.
13. Cheng, T. C. 1983. Triggering of immunologic defense mechanisms of molluscan shellfish by biotic and abiotic challenge and its applications. J. Mar. Tech. Soc. 17:18-25.
14. Chintala, M. M. & W. S. Fisher. 1991. Disease incidence and potential mechanisms of defense for MSX-resistant and -susceptible Eastern oysters held in Chesapeake Bay. J. Shellfish Res. 10:439-443.
15. Choi, K.-S., E. N. Powell, D. H. Lewis & S. M. Ray. 1994. Instantaneous reproductive effort in female American oysters, Crassostrea virginica, measured by a new immunoprecipitation assay. Biol. Bull. 186:41-61.
16. Choi, K.-S., E. A. Wilson, D. H. Lewis, E. N. Powell & S. M. Ray. 1989. The energetic cost of Perkinsus marinus parasitism in oysters: quantification of the thioglycollate method. J. Shellfish Res. 8:125-131.
17. Chu, F-L. E. & K. H. Greene. 1989. Effect of temperature and salinity on in vitro culture of the oyster pathogen Perkinsus marinus (Apicomplexa: Perkinsea). J. Invertebr. Pathol. 53:260-268.
18. Chu, F-L. E. & J. F. La Peyre. 1993. Development of disease caused by the parasite Perkinsus marinus and defense-related hemolymph factors in three populations of oysters from Chesapeake Bay, USA. J. Shellfish Res. 12:21-27.
19. Craig, A., E. N. Powell, R. R. Fay & J. M. Brooks. 1989. Distribution of Perkinsus marinus in Gulf coast oyster populations. Estuaries 12:82-91.
20. Crosby, M. P. & 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.
21. Cummins, H., E. N. Powell, R. J. Stanton, Jr. & G. Staff. 1986. The size-frequency distribution in palaeoecology: the effects of taphonomic processes during formation of death assemblages in Texas bays. Palaeontology (London) 29:495-518.
22. Dame, R. F. 1976. Energy flow in an intertidal oyster population. Estuarine Coastal Mar. Sci. 4:243-253.
23. Dekshenieks, M. M., E. E. Hofmann & E. N. Powell. 1993. Environmental effects on the growth and development of Crassostrea virginica (Gmelin) larvae: a modeling study. J. Shellfish Res. 12:241-254.
24. Dobson, A. P. 1988. The population biology of parasite-induced changes in host behavior. Quart. Rev. Biol. 63:139-165.
25. Doering, P. H. & C. A. Oviatt. 1986. Application of filtration rate models to field populations of bivalves: an assessment using experimental mesocosms. Mar. Ecol. Prog. Ser. 31:265-275.
26. Dungan, C. F. & B. S. Roberson. 1993. Binding specificities of mono-and polyclonal antibodies to the protozoan oyster pathogen Perkinsus marinus. Dis. Aquat. Org. 15:9-22.
27. Dwyer, G. & J. S. Elkinton. 1993. Using simple models to predict virus epizootics in gypsy moth populations. J. Anim. Ecol. 62:1-11.
28. Fenchel, T. & B. J. Finlay. 1983. Respiration rates in heterotrophic, free-living protozoa. Microb. Ecol. 9:99-122.
29. Fisher, W. S. 1988. In vitro binding of parasites (Bonamia ostreae) and latex particle by hemocytes of susceptible and insusceptible oysters. Dev. Comp. Immunol. 12:43-53.
30. Fisher, W. S., M. M. Chintala & M. A. Moline. 1989. Annual variation of estuarine and oceanic oyster Crassostrea virginica Gmelin hemocyte capacity. J. Exp. Mar. Biol. Ecol. 127:105-120.
31. Fisher, W. S., J. D. Gauthier & J. T. Winstead. 1992. Infection intensity of Perkinsus marinus disease in Crassostrea virginica (Gmelin, 1791) from the Gulf of Mexico maintained under different laboratory conditions. J. Shellfish Res. 11:363-369.
32. Fisher, W. S. & R. I. E. Newell. 1986. Salinity effects on the activity of granular hemocytes of American oysters, Crassostrea virginica. Biol. Bull. 170:122-134.
33. Fisher, W. S. & M. Tamplin. 1988. Environmental influence on activities and foreign-particle binding by hemocytes of American oysters, Crassostrea virginica. Can. J. Fish. Aquat. Sci. 45:1309-1315.
34. Ford, S. E. 1986. Comparison of hemolymph proteins from resistant and susceptible oysters, Crassostrea virginicia, exposed to the parasite Haplosporidium nelsoni (MSX). J. Invertebr. Pathol. 47:283-294.
35. Ford, S. E. 1992. Avoiding the transmission of disease in commercial culture of molluscs, with special reference to Perkinsus marinus (Dermo) and Haplosporidium nelsoni (MSX). J. Shellfish Res. 11: 539-546.
36. Ford, S. E. & H. H. Haskin. 1988. Comparison of in vitro salinity tolerance of the oyster parasite, Haplosporidium nelsoni (MSX) and hemocytes from the host, Crassostrea virginica. Comp. Biochem. Physiol. 90:183-187.
37. Gee, J. M. & J. T. Davey. 1986. Experimental studies on the infestation of Mytilus edulis (L.) by Mytilicola intestinalis Steuer (Copepoda, Cyclopoida). J. Cons. Int. Explor. Mer 42:254-264.
38. Gill, C. A. 1928. The Genesis of Epidemics and the Natural History of Disease. William Wood and Company, New York, 550 pp.
39. Goggin, C. L., K. B. Sewell & R. J. G. Lester. 1990. Tolerances of Perkinsus spp. (Protozoa, Apicomplexa) to temperature, chlorine and salinity. J. Shellfish Res. 9:145-148.
40. Gunter, G. 1953. The relationship of the Bonnet Carre Spillway to oyster beds in Mississippi Sound and the "Louisiana marsh," with a report on the 1950 opening. Publ. Inst. Mar. Sci. Univ. Texas 3:17-71.
41. Hadeler, K. P. & H. I. Freedman. 1989. Predator-prey populations with parasitic infection. J. Math. Biol. 27:609-631.
42. Hall, R. P. 1967. Nutrition and growth of protozoa. In: T-T. Chen (ed.). Research in Protozoology, vol. 1. Pergamon Press, New York, pp. 337-404.
43. Hibbert, C. J. 1977. Growth and survivorship in a tidal-flat population of bivalve Mercenaria mercenaria from Southampton Water. Mar. Biol. 44:71-76.
44. Hofmann, E. E., E. N. Powell, J. M. Klinck & G. Saunders. 1995. Modeling diseased oyster populations. 1. Modeling Perkinsus marinus infections in oysters. J. Shellfish Res. 14:121-151.
45. Hofmann, E. E., E. N. Powell, J. M. Klinck & E. A. Wilson. 1992. Modeling oyster populations. III. Critical feeding periods, growth and reproduction. J. Shellfish Res. 11:399-416.
46. Hofstetter, R. P. 1977. Trends in population levels of the American oyster, Crassostrea virginica (Gmelin), on public reefs in Galveston Bay, Texas. Texas Parks Wildl. Dept. Tech. Ser. 24:1-90.
47. Hofstetter, R. P. 1990. The Texas oyster fishery. Texas Parks Wildl. Dept. Bull. No. 40, 21 pp.
48. Hunter, M. D. & P. W. Price. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724-732.
49. Jakobsen, P. J., G. H. Johnsen & P. Larsson. 1988. Effects of predation risk and parasitism on the feeding ecology, habitat use, and abundance of lacustrine three spine stickleback (Gasterosteus aculeatus). Can. J. Fish. Aquat. Sci. 45:426-431.
50. Jarosz, A. M. & J. J. Burdon. 1992. Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini III. Influence of pathogen epidemics on host survivorship and flower production. Oecologia 89:53-61.
51. Kent, M. L., R. A. Elston, M. T. Wilkinson & A. S. Drum. 1989. Impaired defense mechanisms in bay mussels, Mytilus edulis, with heroic neoplasia. J. Invertebr. Pathol. 53:378-386.
52. Kermack, W. O. & A. G. McKendrick. 1991a. Contributions to the mathematical theory of epidemics-I. Bull. Math. Biol. 53:33-55.
53. Kermack, W. O. & A. G. McKendrick. 1991b. Contributions to the mathematical theory of epidemics-II. The problems of epidemicity. Bull. Math. Biol. 53:57-87.
54. Laybourn-Parry, J. 1987. Protozoa. In: T. J. Pandian & F. J. Vernberg (eds.). Animal Energetics, Vol. 1. Protozoa through Insecta. Academic Press, Inc., New York, pp. 1-25.
55. Lenski, R. E. & R. M. May. 1994. The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J. Theor. Biol. 169:253-265.
56. Lewis, E. J., F. G. Kern, A. Rosenfield, S. A. Stevens, R. L. Walker & P. B. Heffernan. 1992. Lethal parasites in oysters from coastal Georgia with discussion of disease and management implications. Mar. Fish. Rev. 54:1-6.
57. Lund, E. J. 1957. A quantitative study of clearance of a turbid medium and feeding by the oyster. Publ. Inst. Mar. Sci. Univ. Texas 4:296-312.
58. Mackin, J. G. 1952. Incidence of infection of oysters by Dermocystidium in the Barataria Bay area of Louisiana. Natl. Shellfish Assoc. Conv. Add. for 1951, 22-35.
59. Mackin, J. G. 1961. Mortality of oysters. Proc. Natl. Shellfish. Assoc. 50:21-40.
60. Mackin, J. G. 1962. Oyster disease caused by Dermocystidium marinum and other microorganisms in Louisiana. Publ. Inst. Mar. Sci. Univ. Texas 7:132-299.
61. Mackin, J. G. & J. L. Boswell. 1954. The relation of forced closure of oysters and acceleration of reproduction of Dermocystidium marinum. Texas A&M Univ. Res. Found. Tech. Rep. Proj. 23 17:1-6.
62. Mackin, J. G. & S. H. Hopkins. 1961. Studies on oyster mortality in relation to natural environments and to oil fields in Louisiana. Publ. Inst. Mar. Sci. Univ. Texas 7:1-131.
63. Mackin, J. G. & S. M. Ray. 1955. Studies on the effect of infection by Dermocystidium marinum on ciliary action in oysters (Crassostrea virginica). Proc. Natl. Shellfish. Assoc. 45:168-181.
64. Mann, R., E. M. Burreson & P. K. Baker. 1991. The decline of the Virginia oyster fishery in Chesapeake Bay: Considerations for introduction of a non-endemic species, Crassostrea gigas (Thunberg, 1793). J. Shellfish Res. 10:379-388.
65. May, E. B. 1971. A survey of the oyster and oyster shell resources of Alabama. Ala. Mar. Res. Bull. 4:1-53.
66. McCallum, H. I. 1990. Covariance in parasite burdens: the effect of predisposition to infection. Parasitology 100:153-159.
67. McCallum, H. I. & G. R. Singleton. 1989. Models to assess the potential of Capillaria hepatica to control population outbreaks of house mice. Parasitology 98:425-437.
68. Medcof, J. C. 1961. Oyster farming in the maritimes. Bull. Fish. Res. Board Can. 131:1-155.
69. Menzel, R. W. & S. H. Hopkins. 1955. The growth of oysters parasitized by the fungus Dermocystidium marinum and by the trematode Bucephalus cuculus. J. Parasitol. 41:333-342.
70. Möller, H. 1990. Association between diseases of flounder (Platichthys flesus) and environmental conditions in the Elbe estuary, FRG. J. Cons. Int. Explor. Mer 46:187-199.
71. Mollison, D. 1987. Population dynamics of mammalian diseases. Symp. Zool. Soc. Lond. 58:329-342.
72. Muschenheim, D. K. 1987. The dynamics of near-bed seston flux and suspension-feeding benthos. J. Mar. Res. 45:473-496.
73. Newell, R. I. E. 1985. Physiological effects of the MSX parasite Haplosporidium nelsoni (Haskin, Stauber & Mackin) on the American oyster Crassostrea virginica (Gmelin). J. Shellfish Res. 5:91-95.
74. NOAA. 1991. Recreational shellfishing in the United States. United States Department of Commerce, National Oceanic and Atmospheric Administration, 22 pp.
75. Ogle, J. & K. Flurry. 1980. Occurrence and seasonality of Perkinsus marinus (Protozoa: Apicomplexa) in Mississippi oysters. Gulf Res. Rep. 6:423-425.
76. Onstad, D. W. & J. V. Maddox. 1989. Modeling the effects of the microsporidium, Nosema pyrausta, on the population dynamics of the insect, Ostrinia nubilalis. J. Invertebr. Pathol. 53:410-421.
77. Paynter, K. T. & E. M. Burreson. 1991. Effects of Perkinsus marinus infection in the Eastern oyster, Crassostrea virginica: II. Disease development and impact on growth rate at different salinities. J. Shellfish Res. 10:425-431.
78. Plowright, W. 1982. The effects of rinderpest and rinderpest control on wildlife in Africa. Symp. Zool. Soc. Lond. 50:1-28.
79. Powell, E. N., H. Cummins, R. J. Stanton, Jr. & G. Staff. 1984. Estimation of the size of molluscan larval settlement using the death assemblage. Estuarine Coastal Shelf Sci. 18:367-384.
80. Powell, E. N., J. D. Gauthier, E. A. Wilson, A. Nelson, R. R. Fay & J. M. Brooks. 1992a. 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.
81. Powell, E. N., E. E. Hofmann, J. M. Klinck & S. M. Ray. 1992b. Modeling oyster populations I. A commentary on filtration rate. Is faster always better? J. Shellfish Res. 11:387-398.
82. Powell, E. N., E. E. Hofmann, J. M. Klinck, E. Wilson-Ormond & M. S. Ellis. 1995a. Modeling oyster populations V. Declining phytoplankton stocks and the population dynamics of American oyster (Crassostrea virginica) populations. Fish. Res. 24:199-222.
83. Powell, E. N., J. M. Klinck, E. E. Hofmann & S. M. Ray. 1994. Modeling oyster populations. IV. Population crashes and management. U. S. Fish Wildl. Serv. Fish. Bull. 92:347-373.
84. Powell, E. N., J. Song, M. S. Ellis & E. A. Wilson-Ormond. 1995b. The status and long-term trends of oyster reefs in Galveston Bay, Texas. J. Shellfish Res. 14:439-457.
85. Powell, E. N. & R. J. Stanton, Jr. 1985. Estimating biomass and energy flow of molluscs in paleo-communities. Palaeontology (Lond) 28:1-34.
86. Quick, J. A., Jr. & J. G. Mackin. 1971. Oyster parasitism by Labyrinthomyxa marina in Florida. Fla. Dept. Nat. Res. Mar. Res. Lab. Prof. Paper Ser. 13:1-55.
87. Ragone, L. M. & E. M. Burreson. 1993. Effect of salinity on infection progression and pathogenicity of Perkinsus marinus in the Eastern oyster, Crassostrea virginicia (Gmelin). J. Shellfish Res. 12:1-7.
88. Ray, S. M. 1954. Biological studies of Dermocystidium marinum a fungus parasite of oysters. Rice Inst. Pamph. Monogr. Biol. Spec. Issue 114 pp.
89. Ray, S. M. 1966. A review of the culture method for detecting Dermocystidium marinum, with suggested modifications and precautions. Proc. Natl. Shellfish. Assoc. 54:55-69.
90. Ray, S. M. 1987. Salinity requirements of the American oyster, Crassostrea virginicia. In: A. J. Muller & G. A. Matthews (eds.). Freshwater Inflow Needs of the Matagorda Bay System with Focus on the Needs of Penaeid Shrimp. National Oceanic and Atmospheric Administration, Technical Memorandum NMFS-SEFC-189, pp. E.1-E.28.
91. Ray, S. M. & A. C. Chandler. 1955. Dermocystidium marinum, a parasite of oysters. Exp. Parasitol. 4:172-200.
92. Robinson, A. 1992. Dietary supplements for reproductive conditioning of Crassostrea gigas kumamoto (Thunberg). I. effects on gonadal development, quality of ova and larvae through metamorphosis. J. Shellfish Res. 11:437-441.
93. Ross, J. 1982. Myxomatosis: the natural evolution of the disease. Symp. Zool. Soc. London 50:77-95.
94. Saunders, G. L., E. N. Powell & D. H. Lewis. 1993. A determination of in vivo growth rates for Perkinsus marinus, a parasite of Crassostrea virginica. J. Shellfish Res. 12:229-240.
95. Schmid-Hempel, P. & R. Schmid-Hempel. 1988. Parasitic flies (Conopidae, Diptera) may be important stress factors for the ergonomics of their bumblebee hosts. Ecol. Entomol. 13:469-472.
96. Shields, J. D. & A. M. Kuris. 1988. Temporal variation in abundance of the egg predator Carcinonemertes epialti (Nemertea) and its effect on egg mortality of its host, the shore crab, Hemigrapsus oregonensis. Hydrobiologia 156:31-38.
97. Sindermann, C. J. 1993. Disease risks associated with importation of non-indigenous marine animals. Mar. Fish. Rev. 54:1-10.
98. Sittel, M. C. 1994. Marginal probabilities of the extremes of ENSO events for temperature and precipitation in the southeastern United States. Florida State University Technical Report, 94-1, 155 pp.
99. 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. Northeast Gulf Sci. 7:171-174.
100. Soniat, T. M. & M. S. Brody. 1988. Field validation of a habitat suitability index model for the American oyster. Estuaries 11:87-95.
101. Soniat, T. M. & S. M. Ray. 1985. Relationships between possible available food and the composition, condition and reproductive state of oysters from Galveston Bay, Texas. Contrib. Mar. Sci. 28:109-121.
102. Turrell, W. R. 1992. New hypotheses concerning the circulation of the northern North Sea and its relation to North Sea fish stock recruitment. ICES J. Mar. Sci. 49:107-123.
103. Warburton, F. E. 1958. Control of the boring sponge on oyster beds. Fish. Res. Bd. Can. Prog. Rep. Atlantic Coast Stat. 69:7-11.
104. Wells, H. W. 1961. The fauna of oyster beds, with special reference to the salinity factor. Ecol. Monogr. 31:239-266.
105. White, M. E., E. N. Powell & S. M. Ray. 1988. Effects of parasitism by the pyramidellid gastropod Boonea impressa on the net productivity of oysters (Crassostrea virginica). Estuarine Coastal Shelf Sci. 26:359-377.
106. Wilson, E. A., E. N. Powell, M. A. Craig, T. L. Wade & 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.
107. Wilson-Ormond, E. A., E. N. Powell & S. M. Ray. in press. Short-term and small-scale variation in food availability to natural oyster populations: food, flow and flux. P.S.Z.N.I.: Mar. Ecol.
108. Wright, D. A. & E. W. Hetzel. 1985. Use of RNA:DNA ratios as an indicator of nutritional stress in the American oyster Crassostrea virginica. Mar. Ecol. Progr. Ser. 25:199-206.