Understanding the ecology of disease in Great Lakes fish populations

Authors

  • Stephen C. Riley U.S. Geological Survey, Great Lakes Science Center, 1451 Green Road, Ann Arbor, MI USA 48105
  • Kelly R. Munkittrick Canadian Rivers Institute, University of New Brunswick, Saint John, New Brunswick, Canada E2L 4L5
  • Allison N. Evans Great Lakes Fishery Commission, 2100 Commonwealth Blvd., Suite 100, Ann Arbor, MI USA 48105
  • Charles C. Krueger Great Lakes Fishery Commission, 2100 Commonwealth Blvd., Suite 100, Ann Arbor, MI USA 48105

Keywords:

disease ecology, population dynamics, fish health

Abstract

Disease may be an important factor affecting wild fish population dynamics in the Great Lakes, but a lack of information on the ecology of fish disease currently precludes the prediction of risks to fish populations. Here we propose a conceptual framework for conducting ecologically-oriented fish health research that addresses the inter-relationships among fish health, fish populations, and ecosystem dysfunction in the Great Lakes. The conceptual framework describes potential ways in which disease processes and the population-level impacts of disease may relate to ecosystem function, and suggests that functional ecosystems are more likely to be resilient with respect to disease events than dysfunctional ecosystems. We suggest that ecosystem- or population-level research on the ecology of fish disease is necessary to understand the relationships between ecosystem function and fish health, and to improve prediction of population-level effects of diseases on wild fish populations in the Great Lakes. Examples of how the framework can be used to generate research questions are provided using three disease models of current interest in the Great Lakes: thiamine deficiency complex, botulism, and bacterial kidney disease.

References

Anderson, R. M. and May, R. M. 1979. Population biology of infectious diseases. Nature, 280: 361–367.

Arkoosh, M. R., Casillas, E., Clemons, E., Kagley, A., Olson, R., Reno, P. and Stein, J. E. 1998. Effect of pollution on fish diseases: potential impacts on salmonid populations. J. Aquat. Anim. Health, 10: 182–190.

Arkoosh, M. R., Clemons, E., Kagley, A. N., Stafford, C., Glass, A. C., Jacobson, K., Reno, P., Myers, M. S., Casillas, E., Loge, F., Johnson, L. L. and Collier, T. K. 2004. Survey of pathogens in juvenile salmon Oncorhynchus spp migrating through Pacific Northwest estuaries. J. Aquat. Anim. Health, 16: 186–196.

Bakke, T. A. and Harris, P. D. 1998. Diseases and parasites in wild Atlantic salmon (Salmo salar) populations. Can. J. Fish. Aquat. Sci., 55(Suppl. 1): 247–266.

Bar-David, S., Lloyd-Smith, J. O. and Getz, W. M. 2006. Dynamics and management of infectious disease in colonizing populations. Ecol., 87: 1215–1224.

Barras, S. C. and Kadlec, J. A. 2000. Abiotic predictors of avian botulism outbreaks in Utah. Wild. Soc. Bull., 28: 724–729.

Beacham, T. D. and Evelyn, T. P. T. 1992. Genetic variation in disease resistance and growth of Chinook, coho, and chum salmon with respect to vibriosis, furunculosis, and bacterial kidney disease. Trans. Am. Fish. Soc., 121: 456–485.

Beyerle, J. and Hnath, J. G. 2002. History of fish health inspections, State of Michigan, 1970–1999 Michigan DNR Fisheries Technical Report 2002–2

Bierman, V. J., Kaur, J., DePinto, J. V., Feist, T. J. and Dilks, D. W. 2005. Modeling the role of zebra mussels in the proliferation of blue-green algae in Saginaw Bay, Lake Huron. J. Great Lakes Res., 31: 32–55.

Bogue, M. B. 2000. Fishing the Great Lakes: An Environmental History, 1783–1933, Madison, WI: University of Wisconsin Press.

Bos, M. and Kozik, A. 2000. Some molecular and enzymatic properties of a homogeneous preparation of thiaminase I purified from carp liver. J. Protein Chem., 19(2): 75–84.

Bott, T. L., Deffner, J. S., McCoy, E. and Foster, E. M. 1966. Clostridium botulinum type E in fish from the Great Lakes. J. Bacteriol., 91: 919–924.

Bott, T. L., Johnson, J., Foster, E. M. and Sugiyama, H. 1968. Possible origin of the high incidence of Clostridium botulinum type E in an inland bay (Green Bay of Lake Michigan). J. Bacteriol., 95: 1542–1547.

Bradley, T. M., Medina, D. J., Chang, P. W. and McClain, J. R. 1989. Epizootic epitheliotropic disease of lake trout (Salvelinus namaycush): history and viral etiology. Diseases of Aquatic Organisms, 7: 195–201.

Brand, C. J., Duncan, R. M., Garrow, S. P., Olson, D. and Schumann, L. E. 1983. Waterbird mortality from botulism type E in Lake Michigan: an update. Wilson Bull., 95: 269–275.

Brown, S. B., Arts, M. T., Brown, L. R., Brown, M., Fitzsimons, J. D., Honeyfield, D. C., Tillitt, D. E., Zajicek, J. L., Wolgamood, M. and Hnath, J. G. 2005a. Can diet-dependent factors help explain fish-to-fish variation in thiamine-dependent early mortality syndrome?. J. Aquat. Anim. Health, 17: 36–47.

Brown, S. B., Honeyfield, D. C., Hnath, J. G., Wolgamood, M., Marquenski, S. V., Fitzsimons, J. D. and Tillitt, D. E. 2005b. Thiamine status in adult salmonines in the Great Lakes. J. Aquat. Anim. Health, 17: 59–64.

Cáceres, C. E., Hall, S. R., Duffy, M. A., Tessier, A. J., Helmle, C. and MacIntyre, S. M. 2006. Physical structure of lakes constrains epidemics in Daphnia populations. Ecol., 87: 1438–1444.

Cairns, M. A., Ebersole, J. L., Baker, J. P., Wigington, P. J., Lavigne, H. R. and Davis, S. M. 2005. Influence of summer stream temperatures on black spot infestation of juvenile coho salmon in the Oregon Coast Range. Trans. Am. Fish. Soc., 134: 1471–1479.

Cunningham, A. A. and Daszak, P. 1998. Extinction of a species of land snail due to infection with a Microsporidian parasite. Cons. Biol., 12: 1139–1141.

Daszak, P., Cunningham, A. A. and Hyatt, A. D. 2000. Emerging infectious disease of wildlife–threats to biodiversity and human health. Science, 287: 443–449.

Daszak, P., Cunningham, A. A. and Hyatt, A. D. 2001. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica, 78: 103–116.

Davis, H. S. 1944. Infectious diseases among wild fishes. Trans. Am. Fish. Soc., 74: 21–25.

Duffy, M. A., Hall, S. R., Tessier, A. J. and Huebner, M. 2005. Selective predators and their parasitized prey: are epidemics in zooplankton under top-down control?. Limnol. Oceanogr., 50: 412–420.

Duggan, I. C., Bailey, S. A., Colautti, R. I., Gray, D. K., Makarewicz, J. C. and MacIsaac, H. J. 2003. “Biological invasions in Lake Ontario: past, present and future”. In State of Lake Ontario–Past, Present and Future, Ecovision World Monograph Series Edited by: Munawar, M. 541–558. Burlington, ON: Aquatic Ecosystem Health and Management Society.

Elsayed, E., Faisal, M., Thomas, M., Whelan, G., Batts, W. and Winton, J. 2006. Isolation of viral haemorrhagic septicaemia virus from muskellunge, Esox masquinongy (Mitchill), in Lake St Clair, Michigan, USA reveals a new sublineage of the North American genotype. J. Fish Dis., 29: 611–619.

Fahnenstiel, G. L., Land, G. A., Nalepa, T. F. and Johengen, T. H. 1995. Effects of zebra mussel (Dreissena polymorpha) colonization on water quality parameters in Saginaw Bay, Lake Huron. J. Great Lakes Res., 21: 435–448.

Farnsworth, M. L., Hoeting, J. A., Hobbs, N. T. and Miller, M. W. 2006. Linking chronic wasting disease to mule deer movement scales: A hierarchical Bayesian approach. Ecol. Appl., 16: 1026–1036.

Fisher, J. P., Fitzsimons, J. D., Combs, G. F. and Spitsbergen, J. M. 1996. Naturally occurring thiamine deficiency causing reproductive failure in Finger Lakes Atlantic salmon and Great Lakes lake trout. Trans. Am Fish. Soc., 125: 167–178.

Fitzsimons, J. D., Brown, S. B. and Vandenbyllaardt, L. 1998. Thiamine levels in food chains of the Great Lakes. American Fisheries Society Symposium, 21: 90–98.

Fitzsimons, J. D., Williston, B., Zajicek, J. L., Tillitt, D. E., Brown, S. B., Brown, L. R., Honeyfield, D. C., Warner, D. M., Rudstam, L. G. and Pearsall, W. 2005. Thiamine content and thiaminase activity of ten freshwater stocks and one marine stock of alewives. J. Aquat. Anim. Health, 17: 26–35.

Folke, C., Carpenter, S., Walker, B., Scheffer, M., Elmqvist, T., Gunderson, L. and Holling, C. S. 2004. Regime shifts, resilience, and biodiversity in ecosystem management. Annu. Rev. Ecol. Evol. Syst., 35: 557–581.

Friend, M., McLean, R. G. and Dein, F. J. 2001. Disease emergence in birds: challenges for the twenty-first century. Auk, 118: 290–303.

Fryer, J. L and Sanders, J. E. 1981. Bacterial kidney disease of salmonid fish. Annual Review of Microbiology., 35: 273–298.

Getchell, R. G., Culligan, W. J., Kirchgessner, M., Sutton, C. A., Casey, R. M. and Bowser, P. R. 2006. Quantitative polymerase chain reaction assay used to measure the prevalence of Clostridium botulinum type E in fish in the lower Great Lakes. J. Aquat. Anim Health, 18: 39–50.

Goldberg, T. L., Grant, E. C., Inendino, K. R., Kassler, T. W., Claussen, J. E. and Philipp, D. P. 2005. Increased infectious disease susceptibility resulting from outbreeding depression. Cons. Biol., 19: 455–462.

Gozlan, R. E., St-Hilaire, S., Feist, S. W., Martin, P. and Kent, M. L. 2005. Disease threat to European fish. Nature, 435: 1046

Gozlan, R. E., Peeler, E. J., Longshaw, M., St-Hilaire, S. and Feist, S. W. 2006. Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe. Microbes and Infection, 8: 1358–1364.

Hall, S. R., Tessier, A. J., Duffy, M. A., Huebner, M. and Cáceres, C. E. 2006. Warmer does not have to mean sicker: temperature and predators can jointly drive timing of epidemics. Ecol., 87: 1684–1695.

Harvell, C. D., Kim, K., Burkholder, J. M., Colwell, R. R., Epstein, P. R., Grimes, D. J., Hofmann, E. E., Lipp, E. K., Osterhaus, A. D. M.E., Overstreet, R. M., Porter, J. W., Smith, G. W. and Vasta, G. R. 1999. Emerging marine diseases – climate links and anthropogenic factors. Science, 285: 1505–1510.

Hecky, R. E., Smith, R. E. H., Barton, D. R., Guilford, S. J. and Taylor, W. D. 2004. The nearshore phosphorus shunt: a consequence of ecosystem engineering by dreissenids in the Laurentian Great Lakes. Can. J. Fish. Aquat. Sci., 61: 1285–1293.

Hedrick, R. P. 1998. Relationships of the host, pathogen, and environment: implications for diseases of cultured and wild fish populations. J. Aquat. Anim. Health, 10: 107–111.

Hinterkopf, J. P., Honeyfield, D. C., Makarewicz, J. and Lewis, T. 1999. “Abundance of plankton species in Lake Michigan and incidence of early mortality syndrome from 1983 to 1992”. In Great Lakes Fishery Commission Board of Technical Experts Report on Early Mortality Syndrome Workshop, MI: Great Lakes Fishery Commission. http://www.glfc.org/staff/emsmeet7.pdf

Hochachka, W. M. and Dhondt, A. A. 2000. Density-dependent decline of host abundance resulting from a new infectious disease. Proc. Nat. Acad. Sci., 97: 5303–5306.

Holey, M. E., Elliott, R. F., Marcquenski, S. V., Hnath, J. G. and Smith, K. D. 1998. Chinook salmon epizootics in Lake Michigan: possible contributing factors and management implications. J. Aquat. Anim. Health, 10: 202–210.

Holmlund, C. M. and Hammer, M. 1999. Ecosystem services generated by fish populations. Ecol. Econom., 29: 253–268.

Honeyfield, D. C., Fitzsimons, J. D., Brown, S. B., Marcquenski, S. V. and McDonald, G. 1998. Introduction and overview of early life stage mortality. American Fisheries Society Symposium, 21: 1–7.

Honeyfield, D. C., Hinterkopf, J. P. and Brown, S. B. 2002. Isolation of thiaminase-positive bacteria from alewife. Trans. Am. Fish. Soc., 131: 171–175.

Inendino, K. R., Grant, E. C., Philipp, D. P. and Goldberg, T. L. 2005. Effects of factors related to water quality and population density on the sensitivity of juvenile largemouth bass to mortality induced by viral infection. J. Aquat. Anim. Health, 17: 304–314.

Jensen, W. I. and Allen, J. P. A possible relationship between aquatic invertebrates and avian botulism. Trans. N. Am. Wildl. Nat. Res. Conf. Vol. 25, pp.171–180.

Ji, Y. Q. and Adelman, I. R. 1998. Thiaminase activity in alewives and smelt in Lakes Huron, Michigan, and Superior. American Fisheries Society Symposium, 21: 154–159.

Johnson, P. T. J., Stanton, D. E., Preu, E. R., Forshay, K. J. and Carpenter, S. R. 2006. Dining on disease: how interactions between infection and environment affect predation risk. Ecol., 87: 1973–1980.

Jónsdóttir, H., Malmquist, H. J., Snorrason, S. S., Gudbergsson, G. and Gudmundsdóttir, S. 1998. Epidemiology of Renibacterium salmoninarum in wild Arctic charr and brown trout in Iceland. J. Fish Biol., 53: 322–339.

Kadlec, J. A. 2002. Avian botulism in Great Salt Lake marshes: perspectives and possible mechanisms. Wildl. Soc. Bull., 30: 983–989.

Kaeser, A. J., Rasmussen, C. and Sharpe, W. E. 2006. An examination of environmental factors associated with Myxobolus cerebralis infection of wild trout in Pennsylvania. J. Aquat. Anim. Health, 18: 90–100.

Klindt, R. M. and Town, B. Lake sturgeon restoration and botulism E, 2004. NYSDEC Lake Ontario Annual Report 2004. Presented at the Lake Ontario Committee meeting. March 29–30 2005. Niagara Falls, Ontario: New York State Department of Environmental Conservation.

Lafferty, K. D. and Gerber, L. 2002. Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv. Biol., 16: 593–604.

Lafferty, K. and Holt, R. D. 2003. How should environmental stress affect the population dynamics of disease?. Ecol. Lett., 6: 654–664.

Lafferty, K. D., Porter, J. W. and Ford, S. E. 2004. Are diseases increasing in the ocean?. Annu. Rec. Ecol. Evol. Syst., 35: 31–54.

LaPatra, S. E. 1998. Factors affecting pathogenicity of infectious hematpoietic necrosis virus (IHNV) for salmonid fish. J. Aquat. Anim. Health, 10: 121–131.

Lester, S. E., Tobin, E. D. and Behrens, M. D. 2007. Disease dynamics and the potential role of thermal stress in the sea urchin, Strongylocentotus purpuratus. Can. J. Fish. Aquat. Sci., 64: 314–323.

Lozano, S. J., Sharold, J. V. and Nalepa, T. F. 2001. Recent declines in benthic macroinvertebrate densities in Lake Ontario. Can. J. Fish. Aquat. Sci., 58: 518–529.

Marty, G. D., Quinn, T. J., Carpenter, G., Myers, T. R. and Willits, N. H. 2003. Role of disease in abundance of a Pacific herring (Clupea pallasi) population. Can. J. Fish. Aquat. Sci., 60: 1258–1265.

Mayer, C. M., Keats, R. A, Rudstam, L. G. and Mills, E. L. 2002. Scale-dependent effects of zebra mussels on benthic invertebrates in a large eutrophic lake. J. N. Am. Benth. Soc., 21: 616–633.

McCallum, H. I., Kuris, A., Harvell, C. C., Lafferty, K. D., Smith, G. W. and Porter, J. 2004. Does terrestrial epidemiology apply to marine systems?.. Trends Ecol Evol., 19: 585–591.

McCann, K. W. 2000. The diversity-stability debate. Nature, 405: 228–233.

McCarty, C. W. and Miller, M. W. 1998. A versatile model of disease transmission applied to forecasting bovine tuberculosis dynamics in white-tailed deer populations. J. Wildl. Dis., 34: 722–730.

MDNR (Michigan Department of Natural Resources). 2004. Muskie Piscirickettsia (Muskie Pox) Update MDNR Fisheries Division Public Update, 11 May 2004

MDNR (Michigan Department of Natural Resources). 2007a. Department of Natural Resources Confirms Spread of Viral Hemorrhagic Septicemia (VHS) in Great Lakes. MDNR press release, 25 January 2007

MDNR (Michigan Department of Natural Resources). 2007b. Fish Disease Halts Walleye, Pike and Muskellunge Production and Stocking. MDNR press release, 3 April 2007

Mesa, M. G., Poe, T. P., Maule, A. G. and Schreck, C. B. 1998. Vulnerability to predation and physiological stress response in juvenile Chinook salmon (Oncorhynchus tshawytscha) experimentally infected with Renibacterium salmoninarum. Can. J. Fish. Aquat. Sci., 55: 1599–1606.

Mitchell, A. J. 2001. Finfish health in the United States (1609 – 1969): historical perspective, pioneering researchers and fish health workers, and annotated bibliography. Aquaculture, 196: 347–438.

Mitchell, A. J. 2003. Reports of fish kills prior to 1900 in the United States. Rev. Fisheries Sci., 11: 1–11.

Moffitt, C. M., Stewart, B. C, LaPatra, S. E., Brunson, R. D., Bartholomew, J. L., Peterson, J. E. and Amos, K. H. 1998. Pathogens and diseases of fish in aquatic ecosystems: implications in fisheries management. J. Aquat. Anim. Health, 10: 95–100.

Munkittrick, K. R. and Dixon, D. G. 1989. A holistic approach to ecosystem health using fish population characteristics. Hydrobiologia, 188/189: 123–135.

Munkittrick, K. R., McMaster, M., Van Der Kraak, G., Portt, C., Gibbons, W., Farwell, A. and Gray, M. 2000. Development of methods for effects-based cumulative effects assessment using fish populations: Moose River Project, Pensacola, FL: SETAC Press.

Mydlarz, L. D., Jones, L. E. and Harvell, C. D. 2006. Innate immunity, environmental drivers, and disease ecology of marine and freshwater invertebrates. Ann. Rev. Ecol. Evol. Syst., 37: 251–258.

Nepszy, S. J., Budd, J. and Dechtiar, A. O. 1978. Mortality of young-of-the-year rainbow smelt (Osmerus mordax) in Lake Erie associated with the occurrence of Glugea hertwigi. J. Wildl. Diseases, 14: 233–239.

Nicholls, K. H., Hopkins, G. J. and Standke, S. J. 1999. Reduced chlorophyll to phosphorus ratios in nearshore Great Lakes waters coincide with the establishment of dreissenid mussels. Can. J. Fish. Aquat. Sci., 56: 153–161.

Nicholson, M. C. and Mather, T. N. 1996. Methods for evaluating Lyme disease risks using geographic information systems and geospatial analysis. J. Med. Entomol., 33: 711–720.

NYSDEC (New York State Department of Environmental Conservation). 2006. DEC continues investigation of death of Lake Ontario shore birds and fish. NYSDEC press release, 20 July 2006

Ögüt, H. 2001. Modeling of fish disease dynamics: a new approach to an old problem. Turk. J. Fish. Aquat. Sci., 1: 67–74.

Patterson, K. R. 1996. Modelling the impact of disease-induced mortality in an exploited population: the outbreak of the fungal parasite Ichthyophonus hoferi in the North Sea herring (Clupea harengus). Can J. Fish. Aquat. Sci., 53: 2870–2887.

Perez-Fuentetaja, A., Clapsadl, M. D., Einhouse, D., Bowser, P. R., Getchell, R. G. and Lee, W. T. 2006. Influence of limnological conditions on Clostridium botulinum type E presence in Eastern Lake Erie sediments (Great Lakes, USA). Hydrobiolgia, 563: 189–200.

Pillsbury, R. W., Lowe, R. L., Pan, Y. D. and Greenwood, J. L. 2002. Changes in the benthic algal community and nutrient limitation in Saginaw Bay, Lake Huron, during the invasion of the zebra mussel (Dreissena polymorpha). J. N. Am. Benth. Soc., 21: 238–252.

Power, M. 2002. “Assessing fish population responses to stress”. In Biological indicators of aquatic ecosystem stress, Edited by: Adams, S. M. 379–430. Bethesda, MD: American Fisheries Society.

Price, C. S. and Schreck, C. B. 2003. Effects of bacterial kidney disease on saltwater preference of juvenile spring chinook salmon. Oncorhynchus tshawytscha Aquaculture, 222: 331–341.

Rapport, D. J., Constanza, R. and McMichael, A. J. 1998. Assessing ecosystem health. Trends Eco. Evol., 13: 397–402.

Rapport, D. J. 1999. Epidemiology and Ecosystem Health: Natural Bridges. Ecosystem Health, 5: 174–180.

Rathbun, R. 1893. Report upon the inquiry respecting food-fishes and the fishing grounds United States Commission of Fish and Fisheries, Part XVII. Report of the Commissioner for 1893

Real, L. A. 1996. Sustainability and the ecology of infectious disease. BioScience, 46: 88–97.

Reed, T. M. and Rocke, T. E. 1992. The role of avian carcasses in botulism epizootics. Wildl. Soc. Bull., 20: 175–182.

Reno, P. W. 1998. Factors involved in the dissemination of disease in fish populations. J. Aquat. Anim. Health, 10: 160–171.

Ricker, W. E. 1945. Natural mortality among Indiana bluegill sunfish. Ecol., 26: 111–121.

Rocke, T. E. and Samuel, M. D. 1999. Water and sediment characteristics associated with avian botulism outbreaks in wetlands. J. Wildl. Manage., 63: 1249–1260.

Rocke, T. E., Euliss, N. H. and Samuel, M. D. 1999. Environmental characteristics associated with the occurrence of avian botulism in wetlands of a northern California refuge. J. Wildl. Manage., 63: 358–368.

Sanders, J. E., Long, J. E., Arakawa, D. K., Bartholomew, J. L. and Rohovec, J. S. 1992. Prevalence of Renibacterium salmoninarum among downstream-migrating salmonids in the Columbia River. J. Aquat. Anim. Health, 4: 72–75.

Sayler, G. S., Nelson, J. D., Justice, A. D. and Colwell, R. R. 1976. Incidence of Salmonella spp., Clostridium botulinum, and Vibrio parahaemolyticus in an estuary. App. Env. Microbiol., 31: 723–730.

Schneider, J. C. 1998. Fate of dead fish in a small lake. Am. Midl. Nat., 140: 192–196.

Shuter, B. J. 1990. Population-level indicators of stress. Am. Fish. Soc. Symp., 8: 145–166.

Sinderman, C. J. 1987. Effects of parasites on fish populations: practical considerations. Int. J. Parasit., 17: 371–382.

Smith, H. M. 1892. Report on an investigation of the fisheries of Lake Ontario. Bull. U. S. Fish Comm., Vol. 10 for 1890

Smith, K. F., Sax, D. F. and Lafferty, K. D. 2005. Evidence for the role of infectious disease in species extinction and endangerment. Cons. Biol., 20: 1349–1357.

Snieszko, S. F. 1973. “Recent advances in scientific knowledge and developments pertaining to diseases of fishes”. In Advances in Veterinary Science and Comparative Medicine, Edited by: Brandly, C. A. and Cornelius, C. E. 291–314. NY: Academic Press.

Snieszko, S. F. 1974. The effects of environmental stress on outbreaks of infectious diseases of fishes. J. Fish. Biol., 6: 197–208.

Stephen, C. and Thorburn, M. 2002. Formulating a vision for fish health research in the Great Lakes, MI: Great Lakes Fishery Commission Project Completion Report.

Tillitt, D. E., Zajicek, J. L., Brown, S. B., Brown, L. R., Fitzsimons, J. D., Honeyfield, D. C., Holey, M. E. and Wright, G. M. 2005. Thiamine and thiaminase status in forage fish of salmonines from Lake Michigan. J. Aquat. Anim. Health, 17: 13–25.

USDA (U. S. Department of Agriculture). 2006. Viral Hemorrhagic Septicemia in the Great Lakes. Animal and Plant Health Inspection Service Veterinary Services, Centers for Epidemiology and Animal Health. Emerging Disease Notice, http://www.aphis.usda.gov/vs/ceah/cei/taf/emergingdiseasenotice_files/vhsgreatlakes.htm July 2006

Vanderploeg, H. A., Nalepa, T. F., Jude, D. J., Mills, E. L., Holeck, K. T., Liebig, J. R., Grigorivich, I. A. and Ojaveer, H. 2002. Dispersal and emerging ecological impacts of Ponto-Caspian species in the Laurentian Great Lakes. Can. J. Fish. Aquat. Sci., 59: 1209–1228.

Van Oosten, J. 1944. Mortality of smelt, Osmerus mordax (Mitchill), in lakes Huron and Michigan during the fall and winter of 1942–1943. Trans. Am. Fish. Soc., 74: 310–337.

Ward, J. R. and Lafferty, K. D. 2004. The elusive baseline of marine disease: are diseases in ocean ecosystems increasing?. PloS Biology, 2: 542–547. http://biology.plosjournals.org

Whittington, R. J., Jones, J. B., Hine, P. H. and Hyatt, A. D. 1997. Epizootic mortality in the pilchard Sardinops sagax neopilchardus in Australia and New Zealand in 1995. I. Pathology and epizootiology. Dis. Aquat. Org., 28: 1–16.

Zajicek, J. L., Tillitt, D. E., Honeyfield, D. C., Brown, S. B. and Fitzsimons, J. D. 2005. A method for measuring total thiaminase activity in fish tissues. Journal of Aquatic Animal Health, 17: 82–94.

Published

2008-08-25

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Research article