Potential Reservoirs and Risk Factors for VHSV IVb in an Enzootic System: Budd Lake, Michigan

References

• AFS–FHS (American Fisheries Society–Fish Health Section). 2005. Standard procedures for aquatic animal health inspections. In AFS–FHS. Fish Health Section blue book: suggested procedures for the detection and identification of certain finfish and shellfish pathogens, 2005 edition. AFS–FHS, Bethesda, Maryland.
   Google Scholar
• Bain, M. B., E. R. Cornwell, K. M. Hope, G. E. Eckerlin, R. N. Casey, G. H. Groocock, R. G. Getchell, P. R. Bowser, J. R. Winton, W. N. Batts, A. Cangelosi, and J. W. Casey. 2010. Distribution of an invasive aquatic pathogen (viral hemorrhagic septicemia virus) in the Great Lakes and its relationship to shipping. PLOS (Public Library of Science) ONE [online serial] 5(4):e10156.
   PubMed Web of Science ®Google Scholar
• Clady, M. D. 1981. Survival and shifts in food of young-of-year Micropterus penned at high densities in an Oklahoma pond. Proceedings of the Oklahoma Academy of Sciences 61:15–22.
   Google Scholar
• Coffey, B. T., and C. D. McNabb. 1974. Eurasian watermilfoil in Michigan. Michigan Botanist 13:159–165.
   Google Scholar
• Cornwell, E. R., G. B. Anderson, D. Coleman, R. G. Getchell, G. H. Groocock, J. V. Warg, A. M. Cruz, J. W. Casey, M. B. Bain, and P. R. Bowser. 2015. Applying multi-scale occupancy models to infer host and site occupancy of an emerging viral fish pathogen in the Great Lakes. Journal of Great Lakes Research 41:520–529.
   Web of Science ®Google Scholar
• Cornwell, E. R., A. Primus, P. T. Wong, G. B. Anderson, T. M. Thompson, G. Kurath, G. H. Groocock, M. B. Bain, P. R. Bowser, and R. G. Getchell. 2014. Round Gobies are an important part of VHSV genotype IVb ecology in the St. Lawrence River and eastern Lake Ontario. Journal of Great Lakes Research 40:1002–1009.
   Web of Science ®Google Scholar
• Crowder, L. N., and W. E. Cooper. 1982. Habitat structural complexity and the interaction between Bluegills and their prey. Ecology 63:1802–1813.
   Web of Science ®Google Scholar
• Dorai-Raj, S. 2014. binom: binomial confidence intervals for several parameterizations. R package version 1.1-1. Available: http://CRAN.R-project.org/package=binom. (February 2016).
   Google Scholar
• Dua, K. 2012. Infectious diseases of farm animals. Morgan and Claypool, St. Rafael, California.
   Google Scholar
• Eckerlin, G. E., J. M. Farrell, R. N. Casey, K. M. Hope, G. H. Groocock, P. R. Bowser, and J. Casey. 2011. Temporal variation in prevalence of viral hemorrhagic septicemia virus type IVb among upper St. Lawrence River Smallmouth Bass. Transactions of the American Fisheries Society 140:529–536.
   Web of Science ®Google Scholar
• Elsayed, E., M. Faisal, M. Thomas, G. Whelan, W. Batts, and J. Winton. 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. Journal of Fish Diseases 29:611–619.
   PubMed Web of Science ®Google Scholar
• Faisal, M., and C. A. Schulz. 2009. Detection of viral hemorrhagic septicemia virus (VHSV) from the leech Myzobdella lugubris Leidy, 1851. Parasites and Vectors [online serial] 2:45.
   Web of Science ®Google Scholar
• Faisal, M., M. Shavalier, R. K. Kim, E. V. Millard, M. R. Gunn, A. D. Winters, C. A. Schulz, A. Eissa, M. V. Thomas, M. Wolgamood, G. E. Whelan, and J. Winton. 2012. Spread of the emerging viral hemorrhagic septicemia virus strain, genotype IVb, in Michigan, USA. Viruses 4:734–760.
   PubMed Web of Science ®Google Scholar
• Faisal, M., and A. D. Winters. 2011. Detection of viral hemorrhagic septicemia virus (VHSV) from Diporeia spp. (Pontoporeiidae, Amphipoda) in the Laurentian Great Lakes, USA. Parasites and Vectors [online serial] 4:2.
   PubMed Web of Science ®Google Scholar
• Faust, C., D. Stallknecht, D. Swayne, and J. Brown. 2009. Filter-feeding bivalves can remove avian influenza viruses from water and reduce infectivity. Proceedings of the Royal Society B 276:3727–3735.
   Google Scholar
• Fijan, N., D. Sulimanović, M. Bearzotti, D. Muzinić, L. O. Zwillenberg, S. Chilmonczyk, J. F. Vautherot, and P. De Kinkelin. 1983. Some properties of the epithelioma papulosum cyprini (EPC) cell line from carp Cyprinus carpio. Annales de l’Institute Pasteur Virologie 134:207–220.
   Google Scholar
• Gerba, C. P. 1984. Applied and theoretical aspects of virus adsorption to surfaces. Advances in Applied Microbiology 30:133–168.
   PubMed Web of Science ®Google Scholar
• Getchell, R. G., E. R. Cornwell, G. H. Groocock, P. T. Wong, L. L. Coffee, G. A. Wooster, and P. R. Bowser. 2013. Experimental transmission of VHSV genotype IVb by predation. Journal of Aquatic Animal Health 25:221–229.
   PubMed Web of Science ®Google Scholar
• Goodwin, A. E., and G. E. Merry. 2011. Replication and persistence of VHSV IVb in freshwater turtles. Diseases of Aquatic Organisms 94:173–177.
   PubMed Web of Science ®Google Scholar
• Groocock, G. H., S. A. Frattini, E. R. Cornwell, L. L. Coffee, G. A. Wooster, R. G. Getchell, and P. R. Bowser. 2012. Experimental infection of four aquacultured species with viral hemorrhagic septicemia virus type IVb. Journal of the World Aquaculture Society 43:459–476.
   Web of Science ®Google Scholar
• Groocock, G. H., R. G. Getchell, G. A. Wooster, K. L. Britt, W. N. Batts, J. R. Winton, R. N. Casey, J. W. Casey, and P. R. Bowser. 2007. Detection of viral hemorrhagic septicemia in Round Gobies in New York State (USA) waters of Lake Ontario and the St. Lawrence River. Diseases of Aquatic Organisms 76:187–192.
   PubMed Web of Science ®Google Scholar
• Hawley, L. M., and K. A. Garver. 2008. Stability of viral hemorrhagic septicemia virus (VHSV) in freshwater and seawater at various temperatures. Diseases of Aquatic Organisms 82:171–178.
   PubMed Web of Science ®Google Scholar
• Hershberger, P. K., J. Gregg, C. Pacheco, J. Winton, J. Richard, and G. Traxler. 2007. Larval Pacific Herring, Clupea pallasii (Valenciennes), are highly susceptible to viral haemorrhagic septicaemia and survivors are partially protected after their metamorphosis to juveniles. Journal of Fish Diseases 30:445–458.
   PubMed Web of Science ®Google Scholar
• Kim, R., and M. Faisal. 2010a. Comparative susceptibility of representative Great Lakes fish species to the North American viral hemorrhagic septicemia virus Sublineage IVb. Diseases of Aquatic Organisms 91:23–34.
   PubMed Web of Science ®Google Scholar
• Kim, R. K., and M. Faisal. 2010b. The Laurentian Great Lakes strain (MI03) of the viral haemorrhagic septicaemia virus is highly pathogenic for juvenile Muskellunge, Esox masquinongy (Mitchell). Journal of Fish Diseases 33:513–527.
   PubMed Web of Science ®Google Scholar
• Kim, R. K., and M. Faisal. 2012. Shedding of viral hemorrhagic septicemia virus (Genotype IVb) by experimentally infected Muskellunge (Esox masquinongy). Journal of Microbiology 50:278–284.
   PubMed Web of Science ®Google Scholar
• Kocan, R., M. Bradley, N. Elder, T. Meyers, B. Batts, and J. Winton. 1997. North American strain of viral haemorrhagic septicaemia virus is highly pathogenic for laboratory-reared Pacific Herring. Journal of Aquatic Animal Health 9:279–290.
   Web of Science ®Google Scholar
• Kocan, R. M., P. K. Hershberger, N. E. Elder, and J. R. Winton. 2001. Epidemiology of viral hemorrhagic septicemia (VHS) among juvenile Pacific Herring and Pacific Sandlances in Puget Sound, Washington. Journal of Aquatic Animal Health 13:77–85.
   Web of Science ®Google Scholar
• Li-ping, M., F. Zhao, L. Yao, L. Xin-guang, D. Zhou, and R. Zhang. 2013. The presence of genogroup II norovirus in retail shellfish from seven coastal cities in China. Food and Environmental Virology 5:81–86.
   PubMed Web of Science ®Google Scholar
• Lumsden, J. S., B. Morrison, C. Yason, S. Russell, K. Young, A. Yazdanpanah, P. Huber, L. Al-Hussinee, D. Stone, and K. Way. 2007. Mortality event in Freshwater Drum Aplodinotus grunniens from Lake Ontario, Canada, associated with viral hemorrhagic septicemia virus, type IV. Diseases of Aquatic Organisms 76:99–111.
   PubMed Web of Science ®Google Scholar
• Marty, G. D., T. J. Quinn II, G. Carpenter, T. R. Meyers, and N. H. Willits. 2003. Role of disease in abundance of a Pacific Herring (Clupea pallasi) population. Canadian Journal of Fisheries and Aquatic Sciences 60:1258–1265.
   Web of Science ®Google Scholar
• Matejusova, I., P. McKay, and M. Snow. 2010. Application of a sensitive, specific and controlled real-time PCR assay to surveillance indicates a low prevalence of viral hemorrhagic septicemia virus (VHSV) in wild herring, Clupea harengus L., in Scottish waters. Journal of Fish Diseases 33:841–847.
   PubMed Web of Science ®Google Scholar
• Pavoni, E., M. Consoli, E. Suffredini, G. Arcangeli, L. Serracca, R. Battistini, I. Rossini, L. Croci, and M. N. Losio. 2013. Noroviruses in seafood: a 9-year monitoring in Italy. Foodborne Pathogens and Disease 10:533–539.
   PubMed Web of Science ®Google Scholar
• Pham, P. H., J. Jung, J. S. Lumsden, B. Dixon, and N. C. Bols. 2012. The potential of waste items in aquatic environments to act as fomites for viral haemorrhagic septicaemia virus. Journal of Fish Diseases 3:73–77.
   Web of Science ®Google Scholar
• Phillips, K. A., A. Noyes, L. Shen, and G. Whelan. 2014. Model program for fish health management in the Great Lakes. Great Lakes Fishery Commission, Special Publication 14-02, Ann Arbor, Michigan.
   Google Scholar
• Pierce, L. R., and C. A. Stepien. 2012. Evolution and biogeography of an emerging quasispecies: diversity patterns of the fish viral hemorrhagic septicemia virus (VHSv). Molecular Phylogenetics and Evolution 63:327–341.
   PubMed Web of Science ®Google Scholar
• Pothoven, S. A., and T. F. Nalepa. 2006. Feeding ecology of Lake Whitefish in Lake Huron. Journal of Great Lakes Research 32:489–501.
   Web of Science ®Google Scholar
• Pothoven, S. A., T. F. Nalepa, P. J. Schneeberger, and S. B. Brandt. 2001. Changes in diet and body condition of Lake Whitefish in southern Lake Michigan associated with changes in benthos. North American Journal of Fisheries Management 21:876–883.
   Web of Science ®Google Scholar
• Purcell, M. K., K. J. Laing, and J. R. Winton. 2012. Immunity to fish rhabdoviruses. Viruses 4:140–166.
   PubMed Web of Science ®Google Scholar
• R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
   Google Scholar
• Randall, R. D., and C. G. Scalet. 1975. Food habits of young-of-the-year fishes in Abbey Pond, South Dakota. Proceedings of the South Dakota Academy of Sciences 54:96–119.
   Google Scholar
• Roldán, E. M., E. E. Rodriguez, M. E. García, and M. F. Navajas. 2013. Prevalence of hepatitis A virus in bivalve molluscs sold in Granada (Spain) fish markets. Foodborne Pathogens and Disease 10:528–532.
   PubMed Web of Science ®Google Scholar
• Schönherz, A. A., M. H. H. Hansen, H. B. H. Jørgensen, P. Berg, N. Lorenzen, and K. Einer-Jensen. 2012. Oral transmission as a route of infection for viral haemorrhagic septicaemia virus in Rainbow Trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 35:395–406.
   PubMed Web of Science ®Google Scholar
• Schramm, H. L. Jr., and K. J. Jirka. 1989. Epiphytic macroinvertebrates as a food resource for Bluegills in Florida lakes. Transactions of the American Fisheries Society 118:416–426.
   Web of Science ®Google Scholar
• Schramm, H. L. Jr., J. V. Shireman, D. E. Hammond, and D. M. Powell. 1985. Effect of commercial harvest of sport fish on the Black Crappie population in Lake Okeechobee, Florida. North American Journal of Fisheries Management 5:217–226.
   Google Scholar
• Standish, I. F. 2016. Eliciting protection and herd immunity in fish against viral hemorrhagic septicemia virus genotype IVb. Doctoral dissertation. Michigan State University, East Lansing.
   Google Scholar
• Thompson, T. M., W. N. Batts, M. Faisal, P. Bowser, J. W. Casey, K. Phillips, K. A. Garver, J. Winton, and G. Kurath. 2011. Emergence of viral hemorrhagic septicemia virus in the North American Great Lakes region is associated with low viral genetic diversity. Diseases of Aquatic Organisms 96:29–43.
   PubMed Web of Science ®Google Scholar
• Throckmorton, E., A. Peters, T. Brenden, and M. Faisal. 2015. Direct and indirect evidence suggests the continuous presence of viral hemorrhagic septicemia virus (genotype IVb) in Budd Lake, Michigan: management implications. North American Journal of Fisheries Management 35:503–511.
   Web of Science ®Google Scholar
• Warg, J. V., T. Clement, E. R. Cornwell, A. Cruz, R. G. Getchell, C. Giray, A. E. Goodwin, G. H. Groocock, M. Faisal, R. Kim, G. E. Merry, N. B. Phelps, M. M. Reising, I. Standish, Y. Zhang, and K. Toohey-Kurth. 2014. Detection and surveillance of viral hemorrhagic septicemia virus using RT-PCR. II. Diagnostic evaluation of two protocols. Diseases of Aquatic Organisms 111:15–22.
   PubMed Web of Science ®Google Scholar
• Williams, C. J., and C. M. Moffitt. 2005. Estimation of pathogen prevalence in pooled samples using maximum likelihood methods and open-source software. Journal of Aquatic Animal Health 17:386–391.
   Web of Science ®Google Scholar
• Wisconsin Department of Natural Resources. 2007. Lake Winnebago fish preliminarily test positive for VHS. Wisconsin Department of Natural Resources, Madison.
   Google Scholar
• Wommack, K. E., K. E. Williamson, R. R. Helton, S. R. Bench, and D. M. Winget. 2009. Methods for the isolation of viruses from environmental samples. Pages 3–14 in M. R. Clokie and A. M. Kropinski, editors. Bacteriophages: methods and protocols, volume 1: isolation, characterization, and interaction. Springer-Verlag, New York.
   Google Scholar