Abstract
The effects of invasive pathogens on wild fish and fish communities generally are not well documented. We compiled information on the impacts of mass mortality events due to Cyprinid Herpesvirus-3 (CyHV-3), otherwise known as Koi Herpesvirus, on wild North American populations of the invasive cyprinid, Cyprinus carpio (common carp), based on our personal experiences, discussions with North American fish ecologists and virologists, a detailed survey of technical and popular publications and a web search. We found evidence of 17 mass die-offs of carp due to CyHV-3 in North America since 2004, for 7 of which we were able to obtain information about carp before and after the events. For 6 of the events, effects of the die-offs on carp population indices appeared to be slight. Carp size-frequency distributions before and after the well-documented 2007/08 event in Ontario were also not conspicuously different. The exceptional event was at Blue Springs Lake, Missouri, in 2012, at which we estimate 65% of the carp present died as a result of CyHV-3 infections and carp abundance continues to decline. Why Blue Springs Lake differs from other events in North America is not clear. Overall, carp die-offs due to CyHV-3 in North America (1) confirm laboratory studies that only common carp are affected, (2) are of brief duration (3–6 weeks), (3) are not repeated in subsequent years and (4) cause much lower mortality (with the exception of Blue Springs Lake) than previously reported for carp in aquaculture facilities or in the laboratory. In terms of both wild carp and their effects on aquatic communities, the short and long-term effects of most die-offs appear to be slight. These features could have implications for the effectiveness of the proposed use of CyHV-3 to reduce feral carp populations in Australia.
Similar content being viewed by others
References
Adamek M, Steinhagen D, Irnazarow I, Hikima J-I, Jung T-S, Aoki T (2014) Biology and host response of Cyprinid herpesvirus 3 infection in common carp. Dev Comp Immunol 43:151–159
Adkinson MA, Gilad O, Hedrick RP (2005) An enzyme linked immunosorbent essay (ELISA) for detection of antibodies to the koi herpesvirus (KHV) in the serum of koi Cyprinus carpio. Fish Pathol 40:53–62
Ahne W (1994) Viral infections of aquatic animals with special reference to Asian aquaculture. Annu Rev Fish Dis 4:375–388
Allman J (2014) The cause and effects of a massive common carp kill. In: 74th Midwest fish and wildlife conference, Kansas City, MO
Anderson G (2015) Hundreds of fish dying in Clear Lake. The Press Democrat. June 9, 2015. www.pressdemocrat.com/news/4045674-181/hundreds-of-fish-dying-in?artslide=0
Aoki T, Hirono I, Kurokawa K, Fukuda H, Nahary R, Eldar A, Davison AJ, Waltzek TB, Bercovier H, Hedrick RP (2017) Genome sequences of three koi herpesvirus isolates representing the expanding distribution of an emerging disease threatening koi and common carp worldwide. J Virol 81:5058–5065
Arizona Game and Fish Department (2009a) An update on Koi Herpes virus (KHV) outbreak. Arizona Game and Fish Dept. Fishing Blog. www.azgfd.net/fish/southwestern-arizona/southwestern-arizona-80/2009/08/06/
Arizona Game and Fish Department (2009b) Lab confirms Havasu carp died from virus. Arizona Game and Fish Dept. Fishing Blog. www.azgfd.net/fish/fishing-news/lab-confirms-havasu-carp-died-from-virus/2009/07/13/
Bajer PG, Sorensen PW (2012) Using boat electrofishing to estimate the abundance of invasive common carp in small Midwestern lakes. North Am J Fish Manag 32:817–822
Bajer PG, Sullivan G, Sorensen PW (2009) Effects of a rapidly increasing population of common carp on vegetative cover and waterfowl in a recently restored Midwestern shallow lake. Hydrobiologia 632:235–245
Bajer PG, Chizinski CJ, Silbernagel JJ, Sorensen PW (2012) Variation in native micro-predator abundance explains recruitment of a motile invasive fish, the common carp, in a naturally unstable environment. Biol Invasions 14:1919–1929
Barclay P (2017) Scientists fight to make invasive pest control palatable to the public. ABC News 13 June 2017. www.abc.net.au/news/2017-06-13/should-invasive-pest-control-be-acceptable-to-the-public/8613070)
Bax NJ, Thresher RE (2009) Ecological, behavioral and genetic factors influencing the recombinant control of invasive pests. Ecol Appl 19:873–888
Bretzinger A, Fischer-Scherl T, Oumouna M, Hoffmann R, Truyen U (1999) Mass mortalities in koi carp, Cyprinus carpio, associated with gill and skin disease. Bull Eur Assoc Fish Pathol 19:182–199
Brown P, Gilligan D (2014) Optimising an integrated pest-management strategy for a spatially structured population of common carp (Cyprinus carpio) using meta-population modelling. Mar Freshw Res 65:538–550
Cipriano RC, Bowser PR, Dove A, Goodwin A, Puzach C (2006) Prominent emerging diseases within the United States. http://www.lsc.usgs.gov/files/Ciprianoetal2011.pdf
Cipriano RC, Bowser PR, Dove A, Goodwin A, Puzach C (2011) Prominent emerging diseases within the United States. http://www.lsc.usgs.gov/files/Ciprianoetal2011.pdf
Cornwell ER, Anderson GB, Wooster GA, Getchell RG, Groocock GH, Casey JW, Bain MB, Bowser PR (2012) Low prevalence of cyprinid herpesvirus 3 found in common carp (Cyprinus carpio carpio) collected from nine locations in the Great Lakes. J Wildl Dis 48:1092–1096
Costes B, Stalin Raj V, Michel B, Fournier G, Thirion M, Gillet L, Mast J, Lieffrig F, Bremont M, Vanderplasschen A (2009) The major portal of entry of koi herpesvirus in Cyprinus carpio is the skin. J Virol 83:2819–2830
Eide KE, Miler-Morgan T, Heidel JR, Kent ML, Bildfell RJ, LaPatra S, Watson G, Jin L (2011) Investigation of koi herpesvirus latency in koi. J Virol 85:4954–4962
Engelsma MY, Way K, Dodge MJ, Voorbergen-Laarman M, Panzarin V, Abbadi M, El-Matbouli M, Skall HF, Kahns S, Stone DM (2013) Detection of novel strains of cyprinid herpesvirus closely related to koi herpesvirus. Dis Aquat Org 107:113–120
Farnham G (2014) Koi herpes virus found in carp on Rock River. Rock Koshkonong Lake District Blog. http://rkld.org/koi-herpes-virus-found-carp-rock-river/
Fuller PL, Nico LG, Williams JD (1999) Nonindigenous Fishes introduced into inland waters of the United States. Am Fish Soc Spec Pub 27, Bethesda, Md. 613 p
Garver KA, Dwilow AG, Richard J, Booth TF, Beniac DR, Souter BW (2010) Mass mortality associated with koi herpesvirus in wild common carp in Canada. J Wildl Dis 46:1242–1251
Gibson-Reinemer DK, Chick JH, VanMiddlesworth TD, VanMiddlesworth M, Casper AF (2017) Widespread and enduring demographic collapse of invasive common carp (Cyprinus carpio) in the Upper Mississippi River system. Biol Invasions 19:1905–1916
Gilad O, Yun S, Zagmutt-Vergara FJ, Leutenegger CM, Bervovier H, Hedrick RP (2003) Molecular comparison of isolates of an emerging fish pathogen, koi herpesvirus, and the effect of water temperature on mortality of experimentally infected koi. J Gen Virol 84:2661–2668
Gozlan RE, Peeler EJ, Longshaw M, St-Hilaire S, Feist SW (2006) Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe. Microbes Infect 8:1358–1364
Great Lakes Fish Health Committee (2012) Annual Agencies Reports. 42 p
Grimmett SG, Warg JV, Gethchell RG, Johnson DJ, Bowser PR (2006) An unusual Koi Herpesvirus associated with a mortality event of common carp Cyprinus carpio in New York State, USA. J Wildl Dis 42:658–662
Haenen OLM, Way K, Bergmann SM, Ariel E (2004) The emergence of koi herpesvirus and its significance to European aquaculture. Bull Eur Assoc Fish Pathol 24:293–307
Haynes GD, Gilligan DM, Grewe P, Moran C, Nicholas FW (2010) Population genetics of invasive common carp Cyrpinus carpio in coastal drainages in eastern Australia. J Fish Biol 77:1150–1157
Hedrick RP, Gilad O, Yun S, Spangenberg JV, Marty GD, Nordhausen RW, Kebus MJ, Bercovier H, Eldar A (2000) A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. J Aquat Anim Health 12:44–57
Ito T, Kurita J, Yuasa K (2014) Differences in the susceptibility of Japanese indigenous and domesticated Eurasian common carp (Cyprinus carpio), identified by mitochondrial DNA typing, to cyprinid herpesvirus 3 (CyHV-3). Veter Microbiol 171:31–40
Jackson ZJ, Quist MC, Larscheid JG (2008) Growth standards for nine North America Fish species. Fish Manag Ecol 15:107–118
Koehn J, Brumley A, Gehrke P (2000) Managing the impact of carp. Technical report, Bureau of Rural Sciences, Canberra, Australia. http://www.daff.gov.au/__data/assets/pdf_file/0010/1193167/Impacts_of_Carpv1.pdf
Kurita J, Yuasa K, Ito T et al (2009) Molecular epidemiology of Koi Herpesvirus. Fish Pathol 44:59–66
Matsui Y, Honjo M, Kohmatsu Y, Uchii K, Yonekura R, Kawabata Z (2008) Detection and significance of koi herpesvirus (KHV) in freshwater environments. Freshw Biol 53:1262–1272
McColl KA (compiler) (2016) Recommendations for long-term strategic carp control: consultation draft. Report to the Invasive Plants and Animals Committee. Invasive Animals CRC, Canberra
McColl KA, Cooke BD, Sunarto A (2014) Viral biocontrol of invasive vertebrates: lessons from the past applied to cyprinid herpesvirus-3 and carp (Cyprinus carpio) control in Australia. Biol Control 72:109–117
McKoll KA, Sunarto A, Holmes EC (2016) Cyprinid herpesvirus 3 and its evolutionary future as a biological control agent for carp in Australia. Virol J 13:206
Minnesota DNR Reports (2017) www.outdoornews.com/2017/07/27/dnr-virus-affects-carp-responsible-lake-elysian-fish-kill/
National Park Service (2009) Lab results identify primary cause of Lake Mohave carp die-off. www.nps.gov/lake/learn/news/lab-results-identify-primary-cause-of-lake-mohave-carp-die-off.htm
O’Hearn R, Martin (2014) Missouri pollution and fish kill investigations 2012 and 2013. www.lmvp.org/Waterline/volume17num1/fishkills.html
Perelberg A, Smirnov M, Hutoran M, Diamant A, Bejerano Y, Kotler M (2003) Epidemiological description of a new viral disease afflicting cultured Cyprinus carpio in Israel. Isr J Aquac Bamidgeh 55:5–12
Piackova V, Flajshans M, Pokorova D, Reschova S, Gela D, Cizek A, Vesely T (2013) Sensitivity of common carp, Cyprinus carpio L., strains and crossbreeds reared in the Czech Republic to infection by cyprinid herpesvirus 3 (CyHV-3; KHV). J Fish Dis 36:75–80
Pikarsky E, Ronen A, Abramowitz J, LevaviSivan B, Hutoran M, Shapira Y, Steinitz M, Perelberg A, Soffer D, Kotlar M (2004) Pathogenesis of acute viral disease induced in fish by carp interstitial nephritis and gill necrosis virus. J Virol 78:9544–9551
Pollick S (2011) Koi herepesvirus suspected in death of carp. The Blade, 9 Aug. 2011. www.toledoblade.com/StevePollick/…/Koi-herpesvirus-suspected-in-death-of-carp-2
Rakus KL, Irnazarow I, Ademek M et al (2012) Gene expression analysis of common carp (Cyprinus carpio L.) lines during Cyprinid herpesvirus 3 infection yields insights into differential immune responses. Dev Comp Immunol 37:65–76
Rakus K, Ouyang P, Boutier M, Ronsmans M, Reschner A, Vancsok C, Jazowiecka-Rakus J, Vanderplasschen A (2013) Cyprinid herpesvirus 3: an interesting virus for applied and fundamental research. Veterinary Res. 4485: 16 p
Read P, Landos M, Rowland SJ, Mifsud C (2007) Diagnosis, treatment and prevention of the diseases of the Australian freshwater fish silver perch (Bidyanus bidyanus). NSW Dept. Primary Ind., Sydney, NSW, Aust. http://www.dpi.nsw.gov.au/__data/assets/pdf_file/0010/638416/Silver-Perch-Diseases-Manual.pdf
Ricker RA (1954) Stock and recruitment. J Fish Res Board Canada 11:559–623
Roberts J, Chick A, Oswald L, Thompson P (1995) Effect of carp, Cyprinus carpio L., an exotic benthivorous fish, on aquatic plants and water quality in experimental ponds. Mar Freshw Res 46:1171–1180
Ronen A, Perelberg A, Abramowitz J, Hutoran M, Tinman S, Bejerano I, Steinitz M, Kotler M (2003) Efficient vaccine against the virus causing a lethal disease in cultured Cyprinus carpio. Vaccine 21:4677–4684
Sano M, Ito T, Kurita J, Yuasa K, Miwa S ,Iida T (2004) Experience of common carp mass mortality in Japan. In: Lavilla-Pitogo, CR, Nagasawa K (eds) Proceedings of the meeting on current status of transboundary fish diseases in Southeast Asia: occurrence, surveillance, research and training, Manila, Philippines, 23–24 June 2004 (pp 13–19). Tigbauan, Iloilo, Philippines: SEAFDEC Aquaculture Department. www.seafdec.org.ph
Scott MK, Farooqi M (2008) 2007 Survey Report Twin Buttes Reservoir. Texas Parks and Wildlife
Scott MK, Farooqi M (2012) 2011 Survey Report Twin Buttes Reservoir. Texas Parks and Wildlife
Scott MK, Van Zee BE (2004) 2003 Survey Report Twin Buttes Reservoir. Texas Parks and Wildlife
Simberloff D, Stilling P (1996) How risky is biological control. Ecology 77:1965–1974
Skinner V (2011) Koi herpes virus blamed for die-off of carp in Michigan. The Grand Rapids Press. www.mlive.com/outdoors/index.ssf/2011/11/koi_virus_blamed_for_die-off_o.html
Skinner A, Ball H (2004) Manual of instructions; end of spring trap netting. Ontario Ministry of Natural Resources, Peterborough, Ontario
Smith BB (2005) The state of the art: a synopsis of information on common carp (Cyprinus carpio) in Australia. Final Tech. Rpt, SARDI Aquatic Sci. Res. Rpt. Ser. (77)
Southard GM, Fries LT (2006) First report of koi herpesvirus in Texas. Am Fish Soc Fish Health Newsl 34:6
Sunarto A, Rukyani A, Itami T (2005) Indonesian experience on the outbreak of koi herpesvirus in koi and carp (Cyprinus carpio). Bull Fish Res Agency 2(395):15–21
Sunarto A, McKoll KA, Crane M, Sumiai T, Hyatt AD, Barnes AC, Walker PJ (2011) Isolation and characterization of koi herpesvirus (KHV) from Indonesia: identification of a new genetic lineage. J Fish Dis 34:87–101
Terhune JS, Grizzle JM, Hayden K, McClenahan SD, Lamprecht SD, White MG (2004) First report of Koi Herpesvirus in wild common carp in the Western Hemisphere. Am Fish Soc Fish Health Newsl 32(3):8–10
Thistleton J (2016) Millions of Lake Burley Griffin carp face swift death from cyprinid herpesevirus disease. Sydney Morning Herald. www.smh.com.au/environment/animals/millions-of-lake-burley-griffin-carp-face-swift-death-from-cyprinid-herpesvirus-release-20160606-gpcs3e.html
Thresher RE, Van de Kamp J, Campbell G, Grewe P, Canning M, Barney M, Bax NJ, Dunham R, Su B, Fulton W (2014) Sex-ratio-biasing constructs for the control of invasive lower vertebrates. Nat Biotechnol 32:424–427
Uchii K, Matsui K, Iida T, Kawabata Z (2009) Distribution of the introduced cyprinid herpesvirus 3 in a wild population of common carp, Cyprinus carpio L. J Fish Dis 32:857–864
United States Geological Survey. (2016) Cyprinid herpes virus-3 (CyHV3) ineffective as a control of Asian carp in the U.S. Unpublished summary
Urban M (2014) Lake Mohave Annual Sport Fish Surveys and Habitat Enhancement Project. www.lcrmscp.gov/crab/presentations/2014/crab14_12.pdf
VanMiddlesworth TD, Casper AF (2014) The Nature Conservancy’s Emiquon Preserve Fish and Aquatic Vegetation Monitoring Annual Report. Illinois Natural History Survey Tech. Report 2014(11)
Waggoner T (2009) Virus killing of carp in lake. www.havasunews.com/news/virus-killing-off-carp-in-lake/article_b5237fe1-0f39-5ea4-811f-a1dbe21f26f3.html
Walquist C (2017) Australia’s carp herpes plan dubbed ‘serious risk to global food security’. The Guardian, 24 February 2017, www.theguardian.com/environment/2017/feb/24/australias-carp-herpes-plan-dubbed-serious-risk-to-global-food-security
Xu J-R, Bentley J, Beck L, Reed L, Miller-Morgan T, Heidel JR, Kent ML, Rockey DD, Jin L (2013) Analysis of koi herpesvirus latency in wild common carp and ornamental koi in Oregon. J Virol Methods 187:372–379
Zeekoevlei (2015) Carp fish dying. www.zeekoevlei.co.za/2015/01/carp-fish-dying/
Acknowledgements
We sincerely appreciate the personal communications input from individuals familiar with CyHV-3 die-offs in North America and those who helped us contact such individuals. We thank A. Branson (Missouri Dept. of Conservation), E. Brown, M. Garvin, S. Gibson and D. Taillon (Ontario Ministry of Natural Resources and Forestry), M. Clancy (New York Dept. of Environment and Conservation), S. Clouthier, A. Drake and D. Watkinson (Dept. of Fisheries and Oceans, Canada), R. Dunham (Auburn Univ.), L. Gamble, J. Guinotte and L. Hopper (U.S. Fish and Wildlife Service), G. Garnett (Lower Colorado Multi-species Conservation Program), J. Lumsden (Univ. of Guelph), M. Jones (Michigan State Univ.), V. Millano (Colorado Parks and Wildlife), N. Phelps and P. Sorensen (Univ. of Minnesota), G. Southward (Texas Parks and Wildlife) and G. Whelan (Michigan Dept. of Natural Resources). This compilation was stimulated by discussions and correspondence with M. Barwick, D. Gilligan and K. McColl. The manuscript benefited from comments by D. Gibson-Reinemer and two anonymous referees, who are also thanked.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Thresher, R.E., Allman, J. & Stremick-Thompson, L. Impacts of an invasive virus (CyHV-3) on established invasive populations of common carp (Cyprinus carpio) in North America. Biol Invasions 20, 1703–1718 (2018). https://doi.org/10.1007/s10530-017-1655-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-017-1655-2