Potential distribution of the viral haemorrhagic septicaemia virus in the Great Lakes region

Journal of Fish Diseases

Volumn 40, Issue 1, 2017, Pages 11-28

  Escobar, L E ^a,b   Kurath, G ^c   Escobar Dodero, J ^d   Craft, M E ^a   Phelps, N B D ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c WESTERN FISHERIES RESEARCH CENTER   (United States)

^d UNIVERSIDAD ANDRÉS BELLO   (Chile)

Author keywords

Great Lakes; Maxent; niche modeling; remote sensing; viral haemorrhagic septicaemia

Indexed keywords

ANIMAL; BIOLOGICAL MODEL; ECOSYSTEM; HEMORRHAGIC SEPTICEMIA, VIRAL; NOVIRHABDOVIRUS; ONTARIO; PHYSIOLOGY; UNITED STATES; VIROLOGY;

ANIMALS; ECOSYSTEM; GREAT LAKES REGION; HEMORRHAGIC SEPTICEMIA, VIRAL; MODELS, BIOLOGICAL; NOVIRHABDOVIRUS; ONTARIO;

EID: 84970021427     PISSN: 01407775     EISSN: 13652761     Source Type: Journal    
DOI: 10.1111/jfd.12490     Document Type: Article

References (89)

1. Bain M.B., Cornwell E.R., Hope K.M., Eckerlin G.E., Casey R.N., Groocock G.H., Getchell R.G., Bowser P.R., Winton J.R., Batts W.N., Cangelosi A. & Casey J.W. (2010) Distribution of an invasive aquatic pathogen (Viral Hemorrhagic Septicemia virus) in the Great Lakes and its relationship to shipping. PLoS ONE 5, 13–15.
2. Barve N., Barve V., Jiménez-Valverde A., Lira-Noriega A., Maher S.P., Peterson A.T., Soberón J. & Villalobos F. (2011) The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling 222, 1810–1819.
3. Blehert D.S., Hicks A.C., Behr M., Meteyer C.U., Berlowski-Zier B.M., Buckles E.L., Coleman J.T.H., Darling S.R., Gargas A., Niver R., Okoniewski J.C., Rudd R.J. & Stone W.B. (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227–227.
4. Brockmann D. & Helbing D. (2013) The hidden geometry of complex, network-driven contagion phenomena. Science 342, 1337–1342.
5. Burnham K.P., Anderson D.R. & Huyvaert K.P. (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65, 23–35.
6. Carroll M.L., DiMiceli C.M., Sohlberg R.A. & Townshend J.R.G. (2005) 250m MODIS Normalized Difference Vegetation Index, 250ndvi28920033435, Collection 4. University of Maryland. Available at http://glcf.umd.edu/data/ndvi/ (Accessed 2 June 2015).
7. Cornwell E.R., Eckerlin G.E., Getchell R.G., Groocock G.H., Thompson T.M., Batts W.N., Casey R.N., Kurath G., Winton J.R., Bowser P.R., Bain M.B. & Casey J.W. (2011) Detection of Viral Hemorrhagic Septicemia virus by quantitative reverse transcription polymerase chain reaction from two fish species at two sites in Lake Superior. Journal of Aquatic Animal Health 23, 207–217.
8. Cornwell E.R., Eckerlin G.E., Thompson T.M., Batts W.N., Getchell R.G., Groocock G.H., Kurath G., Winton J.R., Casey R.N., Casey J.W., Bain M.B. & Bowser P.R. (2012a) Predictive factors and viral genetic diversity for Viral Hemorrhagic Septicemia virus infection in Lake Ontario and the St. Lawrence River. Journal of Great Lakes Research 38, 278–288.
9. Cornwell E.R., Getchell R.G., Groocock G.H., Walsh M.G. & Bowser P.R. (2012b) Low prevalence of VHSV detected in round goby collected in offshore regions of Lake Ontario. Journal of Great Lakes Research 38, 575–579.
10. Cornwell E.R., Primus A., Wong P.T., Anderson G.B., Thompson T.M., Kurath G., Groocock G.H., Bain M.B., Bowser P.R. & Getchell R.G. (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.
11. Dale O.B., Ørpetveit I., Lyngstad T.M., Kahns S., Skall H.F., Olesen N.J. & Dannevig B.H. (2009) Outbreak of Viral Hemorrhagic Septicemia (VHS) in seawater-farmed rainbow trout in Norway caused by VHS virus Genotype III. Diseases of Aquatic Organisms 85, 93–103.
12. Do Amaral K.B., Alvares D.J., Heinzelmann L., Borges-Martins M., Siciliano S. & Moreno I.B. (2015) Ecological niche modeling of Stenella dolphins (Cetartiodactyla: Delphinidae) in the southwestern Atlantic Ocean. Journal of Experimental Marine Biology and Ecology 472, 166–179.
13. Drake J.M. (2015) Range bagging: a new method for ecological niche modelling from presence-only data. Journal of the Royal Society Interface 12, 20150086.
14. Dudik M., Phillips S.J. & Schapire R.E. (2007) Maximum entropy density estimation with generalized regularization and an application to species distribution modeling. Journal of Machine Learning Research 8, 1217–1260.
15. Eckerlin G.E., Farrell J.M., Casey R.N., Hope K.M., Groocock G.H., Bowser P.R. & Casey J. (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.
16. Einer-Jensen K., Ahrens P., Forsberg R. & Lorenzen N. (2004) Evolution of the fish rhabdovirus viral haemorrhagic septicaemia virus. Journal of General Virology 85, 1167–1179.
17. Elith J., Phillips S.J., Hastie T., Dudík M., Chee Y.E. & Yates C.J. (2011) A statistical explanation of Maxent for ecologists. Diversity and Distributions 17, 43–57.
18. Elsayed E., Faisal M., Thomas M., Whelan G., Batts W. & Winton J.R. (2006) Isolation of Viral Hemorrhagic Septicemia 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.
19. Escobar L.E. & Peterson A.T. (2013) Spatial epidemiology of bat-borne rabies in Colombia. Pan American Journal of Public Health 34, 135–136.
20. Escobar L.E., Lira-Noriega A., Medina-Vogel G. & Peterson A.T. (2014) Potential for spread of White-nose fungus (Pseudogymnoascus destructans) in the Americas: using Maxent and NicheA to assure strict model transference. Geospatial Health 11, 221–229.
21. Escobar L.E., Peterson A.T., Papeş M., Favi M., Yung V., Restif O., Qiao H. & Medina-Vogel G. (2015a) Ecological approaches in veterinary epidemiology: mapping the risk of bat-borne rabies using vegetation indices and night-time light satellite imagery. Veterinary Research 46, 92.
22. Escobar L.E., Ryan S.J., Stewart-Ibarra A.M., Finkelstein J.L., King C.A., Qiao H. & Polhemus M.E. (2015b) A global map of suitability for coastal Vibrio cholerae under current and future climate conditions. Acta Tropica 149, 202–211.
23. ESRI (2015) ArcGIS Desktop: Release 10.2. Envrionmental Systems Research Institute, Redlands, CA.
24. Estrada-Peña A., Ostfeld R.S., Peterson A.T., Poulin R. & de la Fuente J. (2014) Effects of environmental change on zoonotic disease risk: an ecological primer. Trends in Parasitology 30, 205–214.
25. Faisal M. & Winters A.D. (2011) Detection of Viral Hemorrhagic Septicemia virus (VHSV) from Diporeia spp. (Pontoporeiidae, Amphipoda) in the Laurentian Great Lakes, USA. Parasites & Vectors 4, 2.
26. Faisal M., Shavalier M., Kim R.K., Millard E.V., Gunn M.R., Winters A.D., Schulz C.A., Eissa A., Thomas M.V., Wolgamood M., Whelan G.E. & Winton J.R. (2012) Spread of the emerging Viral Hemorrhagic Septicemia virus strain, genotype IVb, in Michigan, USA. Viruses 4, 734–760.
27. Fisher M.C., Garner T.W.J. & Walker S.F. (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology 63, 291–310.
28. Foreman M.G.G., Guo M., Garver K.A., Stucchi D., Chandler P., Wan D., Morrison J. & Tuele D. (2015) Modelling Infectious Hematopoietic Necrosis virus dispersion from marine salmon farms in the Discovery Islands, British Columbia, Canada. PLoS ONE 10, e0130951.
29. Frattini S.A., Groocock G.H., Getchell R.G., Wooster G.A., Casey R.N., Casey J.W. & Bowser P.R. (2011) A 2006 survey of Viral Hemorrhagic Septicemia (VHSV) virus type IVb in New York state waters. Journal of Great Lakes Research 37, 194–198.
30. Gallardo B., Zu Ermgassen P.S.E. & Aldridge D.C. (2013) Invasion ratcheting in the zebra mussel (Dreissena polymorpha) and the ability of native and invaded ranges to predict its global distribution. Journal of Biogeography 40, 2274–2284.
31. Garver K.A., Traxler G.S., Hawley L.M., Richard J., Ross J.P. & Lovy J. (2013) Molecular epidemiology of viral haemorrhagic septicaemia virus (VHSV) in British Columbia, Canada, reveals transmission from wild to farmed fish. Diseases of Aquatic Organisms 104, 93–104.
32. GEBCO (2014) GEBCO_2014 Grid — A global 30 arc-second interval grid. General Bathymetric Chart of the Oceans. Available at http://www.gebco.net/ (Accessed 01 January 2016).
33. Goodwin A.E. & Merry G.E. (2011) Mortality and carrier status of bluegills exposed to Viral Hemorrhagic Septicemia virus genotype IVb at different temperatures. Journal of Aquatic Animal Health 23, 85–91.
34. Groocock G.H., Getchell R.G., Wooster G.A., Britt K.L., Batts W.N., Winton J.R., Casey R.N., Casey J.W. & Bowser P.R. (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.
35. Guisan A. & Thuiller W. (2005) Predicting species distribution: offering more than simple habitat models. Ecology Letters 8, 993–1009.
36. Hawley L.M. & Garver K.A. (2008) Stability of Viral Hemorrhagic Septicemia virus (VHSV) in freshwater and seawater at various temperatures. Diseases of Aquatic Organisms 82, 171–178.
37. Hengl T., Kilibarda M., Carvalho-Ribeiro E.D. & Reuter H.I. (2015) Worldgrids — a public repository and a WPS for global environmental layers. WorldGrids. Available at http://worldgrids.org/doku.php?id=about&rev=1427534899 (Accessed 14 September 2015).
38. Herdendorf C.E. (1990) Great Lakes Estuaries. Estuaries 13, 493–503.
39. Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G. & Jarvis A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.
40. Holt R.D. (2009) Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives. Proceedings of the National Academy of Sciences of the United States of America 106(Suppl), 19659–19665.
41. Hondzo M. & Stefan H.G. (1993) Lake water temperature simulation model. Journal of Hydraulic Engineering Division of the American Society of Civil Engineers 119, 1251–1273.
42. Horlyck V., Mellergard S., Dalsgaard I. & Jorgensen P.E.V. (1984) Occurrence of VHS in Danish Maricultured Rainbow Trout. Bulletin of the European Association of Fish Pathologists 4, 11–13.
43. Horning N., Robinson J., Sterling E., Turner W. & Spector S. (2010) Remote Sensing for Ecology and Conservation. Oxford University Press, New York.
44. Hurlbert S.H. (1984) Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54, 187–211.
45. Kane-Sutton M., Kinter B., Dennis P.M. & Koonce J.F. (2010) Viral Hemorrhagic Septicemia virus infection in Yellow perch, Perca flavescens, in Lake Erie. Journal of Great Lakes Research 36, 37–43.
46. Kennedy C.R. (2009) The ecology of parasites of freshwater fishes: the search for patterns. Parasitology 136, 1653–1662.
47. Kim R. & Faisal M. (2011) Emergence and resurgence of the Viral Hemorrhagic Septicemia virus (Novirhabdovirus, Rhabdoviridae, Mononegavirales). Journal of Advanced Research 2, 9–23.
48. Kumar S., Spaulding S.A., Stohlgren T.J., Hermann K.A., Schmidt T.S. & Bahls L.L. (2009) Potential habitat distribution for the freshwater diatom Didymosphenia geminata in the continental US. Frontiers in Ecology and the Environment 7, 415–420.
49. LP DAAC (2009) Land Water Mask Derived from MODIS and SRTM L3 Global 250 m SIN Grid. MOD44W. Available at https://lpdaac.usgs.gov/dataset_discovery/modis/modis_products_table/mod44w (Accessed 16 November 2015).
50. Lumsden J.S., Morrison B., Yason C., Russell S., Young K., Yazdanpanah A., Huber P., Al-Hussinee L., Stone D.M. & Way K. (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.
51. MDNR (2010) Special notice: VHS found in Lake Superior. Minnesota Department of Natural Resources. Available at http://www.dnr.state.mn.us/fish_diseases/vhs.html (Accessed 06 September 2015).
52. Merow C., Smith M.J. & Silander J.A. (2013) A practical guide to Maxent for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36, 1–12.
53. Meyers T.R., Short S. & Lipson K. (1999) Isolation of the North American strain of viral hemorrhagic septicemia virus (VHSV) associated with epizootic mortality in two new host species of Alaskan marine fish. Diseases of Aquatic Organisms 38, 81–86.
54. Millard E.V. & Faisal M. (2012) Heterogeneity in levels of serum neutralizing antibodies against Viral Hemorrhagic Septicemia virus genotype IVb among fish species in Lake St. Clair, Michigan, USA. Journal of Wildlife Diseases 48, 405–415.
55. Mills E.L., Leach J.H., Carlton J.T. & Secor C.L. (1993) Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. Journal of Great Lakes Research 19, 1–54.
56. Munro E.S., McIntosh R.E., Weir S.J., Noguera P.A., Sandilands J.M., Matejusova I., Mayes A.S. & Smith R. (2015) A mortality event in wrasse species (Labridae) associated with the presence of Viral Hemorrhagic Septicemia virus. Journal of Fish Diseases 38, 335–341.
57. Nekouee N., Hamidi S.A., Roberts P.J.W. & Schwab D.J. (2015) Assessment of a 3D hydrostatic model (POM) in the near field of a Buoyant River plume in Lake Michigan. Water, Air, & Soil Pollution 226, 210.
58. NOAA (2000) National Oceanic and Atmospheric Administration. About our Great Lakes: Lake by lake profiles. Great Lakes Environmental Research Laboratory. Available at http://www.glerl.noaa.gov/pr/ourlakes/lakes.html (Accessed 07 November 2016).
59. Oliveira M.D., Hamilton S.K. & Jacobi C.M. (2010) Forecasting the expansion of the invasive golden mussel Limnoperna fortunei in Brazilian and North American rivers based on its occurrence in the Paraguay River and Pantanal wetland of Brazil. Aquatic Invasions 5, 59–73.
60. Peterson A.T. (2006) Ecologic niche modeling and spatial patterns of disease transmission. Emerging Infectious Diseases 12, 1822–1826.
61. Peterson A.T. (2014) Mapping Disease Transmission Risk: Enriching Models using Biology and Ecology. Johns Hopkins University Press, Baltimore.
62. Peterson A.T., Papes M. & Kluza D.A. (2003) Predicting the potential invasive distributions of four alien plant species in North America. Weed Science 51, 863–868.
63. Peterson A.T., Lash R.R., Carroll D.S. & Johnson K.M. (2006) Geographic potential for outbreaks of Marburg hemorrhagic fever. The American Journal of Tropical Medicine and Hygiene 75, 9–15.
64. Peterson A.T., Soberón J., Pearson R.G., Anderson R.P., Martínez-Meyer E., Nakamura M. & Bastos M. (2011) Ecological Niches and Geographic Distributions. Princeton University Press, Princeton, NJ.
65. Phelps N.B.D., Goodwin A.E., Marecaux E. & Goyal S.M. (2013) Comparison of treatments to inactivate Viral Hemorrhagic Septicemia virus (VHSV-IVb) in frozen baitfish. Diseases of Aquatic Organisms 102, 211–216.
66. Phelps N.B.D., Craft M.E., Travis D., Pelican K. & Goyal S.M. (2014) Risk-based management of Viral Hemorrhagic Septicemia virus in Minnesota. North American Journal of Fisheries Management 34, 373–379.
67. Phillips S.J., Dudik M. & Schapire R.E. (2004) A maximum entropy approach to species distribution modeling. Twenty-first international conference on Machine learning - ICML ‘04 21, 83.
68. Phillips S.J., Anderson R.P. & Schapire R.E. (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling 190, 231–259.
69. Qiao H., Soberón J. & Peterson A.T. (2015) No silver bullets in correlative ecological niche modelling: insights from testing among many potential algorithms for niche estimation. Methods in Ecology and Evolution 6, 1126–1136.
70. Qiao H., Peterson A.T., Campbell L.P., Soberón J., Ji L. & Escobar L.E. (2016) NicheA: creating virtual species and ecological niches in multivariate environmental scenarios. Ecography. doi:10.1111/ecog.01961 [Epub ahead of print].
71. R Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
72. Raja-Halli M., Vehmas T.K., Rimaila-Pärnänen E., Sainmaa S., Skall H.F., Olesen N.J. & Tapiovaara H. (2006) Viral Hemorrhagic Septicemia (VHS) outbreaks in Finnish rainbow trout farms. Diseases of Aquatic Organisms 72, 201–211.
73. Res C., Pettorelli N., Ryan S., Mueller T., Bunnefeld N., Jedrzejewska B., Lima M. & Kausrud K. (2011) The Normalized Difference Vegetation Index (NDVI): unforeseen successes in animal ecology. Climate Research 46, 15–27.
74. Ruby E.G., Greenberg E.P. & Hastings J.W. (1980) Planktonic marine luminous bacteria: species distribution in the water column. Applied and Environmental Microbiology 39, 302–306.
75. Schindler D.W. & Nighswander J.E. (1970) Nutrient supply and primary production in Clear Lake, eastern Ontario. Journal of the Fisheries Research Board of Canada 27, 2009–2036.
76. Skall H.F., Slierendrecht W.J., King J.A. & Olesen N.J. (2004) Experimental infection of rainbow trout Oncorhynchus mykiss with viral haemorrhagic septicaemia virus isolates from European marine and farmed fishes. Diseases of Aquatic Organisms 58, 99–110.
77. Soberón J. & Peterson A.T. (2005) Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiversity Informatics 2, 1–10.
78. Thompson T.M., Batts W.N., Faisal M., Bowser P., Casey J.W., Phillips K., Garver K.A., Winton J.R. & Kurath G. (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.
79. Throckmorton E., Peters A., Brenden T. & Faisal M. (2015) Direct and indirect evidence suggests continuous presence of Viral Hemorrhagic Septicemia virus (Genotype IVb) in Budd Lake, Michigan: management implications. North American Journal of Fisheries Management 35, 503–511.
80. Tyberghein L., Verbruggen H., Pauly K., Troupin C., Mineur F. & De Clerck O. (2012) Bio-ORACLE: a global environmental dataset for marine species distribution modelling. Global Ecology and Biogeography 21, 272–281.
81. U.S. Geological Survey (2013) Molecular epidemiology of aquatic pathogens -viral hemorrhagic septicemia virus (MEAP-VHSV) database. Available at http://gis.nacse.org/vhsv/ (Accessed 1 June 2015).
82. VHSV Expert Panel and Working Group (2010) Viral Hemorrhagic Septicemia virus (VHSV-IVb) risk factors and association measures derived by expert panel. Preventative Veterinary Medicine 94, 28–139.
83. Vo N.T.K., Bender A.W., Lee L.E.J., Lumsden J.S., Lorenzen N., Dixon B. & Bols N.C. (2015) Development of a walleye cell line and use to study the effects of temperature on infection by Viral Hemorrhagic Septicemia virus group IVb. Journal of Fish Diseases 38, 121–136.
84. Warren D.L. & Seifert S.N. (2011) Ecological niche modeling in Maxent: the importance of model complexity and the performance of model selection criteria. Ecological Applications 21, 335–342.
85. Warren D.L., Glor R.E. & Turelli M. (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33, 607–611.
86. Williams J.W. & Jackson S.T. (2007) Novel climates, no-analog communities, and ecological surprises. Frontiers in Ecology and the Environment 5, 475–482.
87. Winton J.R., Kurath G. & Batts W. (2007) Detection of Viral Hemorrhagic Septicemia Virus. USGS. Available at http://pubs.usgs.gov/fs/2007/3055/fs20073055.pdf (Accessed 10 September 2015).
88. Zambrano L., Martínez-Meyer E., Menezes N. & Peterson A.T. (2006) Invasive potential of common carp (Cyprinus carpio) and Nile tilapia (Oreochromis niloticus) in American freshwater systems. Canadian Journal of Fisheries and Aquatic Sciences 63, 1903–1910.
89. Zengeya T.A., Robertson M.P., Booth A.J. & Chimimba C.T. (2013) Ecological niche modeling of the invasive potential of Nile tilapia Oreochromis niloticus in African river systems: concerns and implications for the conservation of indigenous congenerics. Biological Invasions 15, 1507–1521.