The science is clear: Fish farms put wild Pacific salmon at risk

Piscine orthoreovirus (PRV) research

2004 Kongtorp et al. (a[1],b[2]): First case definition of HSMI and demonstration that it is infectious.

2006 Watanabe et al. [3]: Early evidence on potential viral cause of HSMI.

2009 Kongtorp and Taksdal [4]: Risks of spreading HSMI by transferring apparently healthy fish.

2010 Palacios et al. [5]: PRV discovered – reported as viral precursor of HSMI.

2012 Finstad et al. [6]: Further evidence that PRV causes HSMI.
Løvoll et al. [7]: Elevated PRV loads associated with presence of HSMI. No evidence of differences in virulence between PRV strains.
Kristoffersen et al. [8]: Risk of long-distance dispersal of PRV over 50-100 km.
Garseth et al. (a[9], b[10], c[11]): PRV widely dispersed (without HSMI) in wild Atlantic salmon, can spread from farm to wild salmon, sea-trout could play role in pathogen exchange with wild Atlantic salmon.

2013 Kibenge et al. [12]: BC PRV sequences closely related to a Norwegian sub-genotype.

2014 Finstad et al. [13]: Discovery that PRV first proliferates in red blood cells with potential effects on fish health.
Miller et al. [14]: Shortened survival for PRV-infected sockeye salmon returning to Chilko Lake.

2015 Wessel et al. [15]: Technical progress on molecular-level functioning of PRV.
Wessel et al. [16]: More definitive evidence that PRV can replicate in red blood cells.
Olsen et al. [17]: HSMI-like disease and anemia along with PRV-like virus in rainbow trout.
Dahle et al. [18]: Found major phenotypic changes in PRV-infected red blood cells in Atlantic salmon. Functional consequences unexplored.
Bjørgen et al. [19]: Elevated PRV levels in damaged versus undamaged muscle cells. Further evidence that PRV causes HSMI.

2016 Siah et al. [20], [21]: HSMI not in BC. PRV widespread, long-present in BC.
Madhun et al. [22]: Low prevalence and intensity of PRV in wild sea trout.
Haatveit et al. [23]: Molecular-level evidence related to PRV replication in red blood cells.
Godoy et al. [24]: HSMI in Chilean farmed Atlantic salmon. Heart lesions with PRV-like virus found in Chilean farmed coho salmon.
Takano et al.[25]: PRV-like virus causes blood disease, EIBS, in coho salmon.
Lund et al. [26]: PRV can help Atlantic salmon fight an SAV infection.
Wiik-Nielsen et al. [27]: Evidence that PRV is higher when HSMI symptoms observed in farmed Atlantic salmon. Evidence also of complex co-infection dynamics.
Morton and Routledge [28]: Review of aquaculture-related risk factors (including PRV) for wild Pacific salmon.

2017 Di Cicco et al. [29]: HSMI in BC. Strengthened connection between PRV and HSMI.  Suggestion that DFO’s Fish Health and Surveillance Program is not adequate to consistently diagnose HSMI.
Haatveit et al. [30]: Initial acute PRV infection in red blood cells lasts only 1-2 weeks before subsiding.
Wessel et al. [31]: Confirmation that PRV can cause HSMI on its own.
Miller et al. [32]: Correlational evidence that PRV may cause jaundice in farmed chinook salmon.
Kibenge et al. [33]: Critique of Siah et al. (2016).
Morton et al. [34]: Correlational evidence linking both (i) salmon aquaculture to PRV dynamics in wild Pacific salmon, and (ii) PRV to weakened ability for Pacific salmon to return to higher-elevation spawning grounds.
Hauge et al. [35]: Further insight on the initial acute phase in the red blood cells of a PRV infection in Atlantic salmon.

2018 Madhun et al. [36]: PRV prevalence in wild Atlantic salmon in northern Norway: ambivalent evidence on salmon farm exposure
Cartagena et al. [37]: Evidence of two strains of PRV in Chilean farmed rainbow trout mortalities.
Tucker et al. [38]: Demonstration of value of molecular screening technique for detecting viral disease development. Low prevalence of PRV in juvenile Fraser River chinook not exposed to fish farms.
Di Cicco et al. [39]: PRV causes jaundice/anaemia in farmed chinook salmon in BC.
Dhamotharan et al. [40]: Molecular characterization of PRV in rainbow trout.
Khuen et al. [41]: PRV-like virus in brown trout with proliferative darkening syndrome (PDS).
Wang [42]: Evidence of potential impacts of PRV on wild, juvenile chinook salmon.

2019 Wessel et al. [43] Review of published findings on PRV infection, replication and effects on salmonid red blood cells.
Kibenge et al. [44]: 72 of 73 tissue samples from escaped farmed Atlantic salmon tested PRV-positive.

[1] Kongtorp, RT, Kjerstad, A, Taksdal T, Guttvik, A, and Falk, K. 2004a. Heart and skeletal muscle inflammation in Atlantic salmon, Salmo salar L.: a new infectious disease. J. Fish Dis. 27: 351-358.

[2] Kongtorp RT, Taksdal T, and Lyngøy A. 2004b. Pathology of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon Salmo salar. 2004b. Dis Aquat Org 59: 217–224.

[3] Watanabe K, Karlsen M, Devold M, Isdal E, Litlabø A, and Nylund A. 2006. Virus-like particles associated with heart and skeletal muscle inflammation (HSMI) Dis Aquat Org 70: 183-192.

[4] Kongtorp RT, and Taksdal T. 2009. Studies with experimental transmission of heart and skeletal muscle inflammation in Atlantic salmon, Salmo salar, L. J. Fish Dis 32: 253-262

[5] Palacios G, Lovoll M, Tengs T, Hornig M, Hutchison S, Hui J, Kongtorp R, Savji N, Bussettii AV, Solovyov A, Kristoffersen AB, Celone C, Street C, Trifonov V, Hirschberg DL, Rabadan R, Egholm M, Rimstad E, and Lipkin WI. 2010. Heart and skeletal muscle inflammation of farmed salmon is associated with infection with a novel reovirus. PLoS ONE 5(7): e11487. doi:10.1371/journal.pone.0011487

[6] Finstad ØW, Falk K, Løvoll M, Evensen Ø, and Rimstad E. 2012. “Immunohistochemical detection of piscine reovirus (PRV) in hearts of Atlantic salmon coincide with the course of heart and skeletal inflammation (HSMI).” Veterinary Research 43:27, 11 pp. DOI: 10.1186/1297-9716-42-27.

[7] Løvoll M, Alarcón M, Jenson BB, Taksdal T, Kristoffersen AB, and Tengs T. 2012. Quantification of piscine reovirus (PRV) at different stages of Atlantic salmon Salmo salar production.  Dis. Aquat. Org. 99: 7-12.

[8] Kristoffersen AB, Bang Jensen B, Jansen PA. 2013. Risk mapping of heart and skeletal muscle inflammation in salmon farming. Prev Vet Med. 2013 Apr 1;109(1-2):136-43. doi: 10.1016/j.prevetmed.2012.08.012. Epub 2012 Sep 5. PubMed  PMID: 22959429.

[9] Garseth AH, Biering E, Aunsmo A. 2013a. Associations between piscine reovirus infection and life history traits in wild-caught Atlantic salmon Salmo salar L. in Norway. Prev Vet Med. 2013 Oct 1;112(1-2):138-46. doi: 10.1016/j.prevetmed.2013.06.007. Epub 2013 Jul 29. PubMed PMID: 23906390.

[10] Garseth ÅH, Ekrem T, Biering E. 2013b. Phylogenetic evidence of long distance dispersal and transmission of piscine reovirus (PRV) between farmed and wild Atlantic salmon. PLoS One. 2013 Dec 11;8(12):e82202. doi: 10.1371/journal.pone.0082202. eCollection 2013. PubMed PMID: 24349221; PubMed Central PMCID: PMC3859594.

[11] Garseth ÅH, Fritsvold C, Opheim M, Skjerve E, and Biering E. 2013c. Piscine reovirus (PRV) in wild Atlantic salmon, Salmo salar L., and sea-trout, Salmo trutta Norway. J Fish Dis.. 36: 483-493.

[12] Kibenge MJT, Iwamoto T, Wang Y, Morton A, Godov MG, and Kibenge FSB. 2013. Whole-genome analysis of piscine reovirus (PRV) shows PRV represents a new genus in family Reoviridae and its genome segment S1 sequences group into two separate sub-genotypes. Virol J 10:230-250.

[13] Finstad OW, Dahle MK, Lindholm TH, Nyman IB, Løvoll M, Wallace C, Olsen CM, Storset AK, Rimstad E. Piscine orthoreovirus (PRV) infects Atlantic salmon erythrocytes. Vet Res. 2014 Apr 3;45:35. doi: 10.1186/1297-9716-45-35. PubMed PMID: 24694042; PubMed Central PMCID: PMC4234517.

[14] Miller KM, Teffer A, Tucker S, Li S, Schulze AD, Trudel M, Janes F, Tabata A, Kaukinen KH, Ginther NG, Ming TJ, Cooke SJ, Hipfner JM, Patterson DA, Hinch SG. 2014. Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines. Evol App  2014 7:812 855.

[15]  Wessel Ø, Nyman IB, Markussen T, Dahle MK, Rimstad E. Piscine orthoreovirus (PRV) ơ3 protein binds dsRNA. Virus Res. 2015 Feb 16;198:22-9. doi:10.1016/j.virusres.2015.01.001. Epub 2015 Jan 14. PubMed PMID: 25596495.

[16]  Wessel Ø, Olsen CM, Rimstad E, Dahle MK. Piscine orthoreovirus (PRV) replicates in Atlantic salmon (Salmo salar L.) erythrocytes ex vivo. Vet Res. 2015 Mar 6;46:26. doi: 10.1186/s13567-015-0154-7. PubMed PMID: 25888832; PubMed Central PMCID: PMC4350956.

[17]  Olsen AB, Hjortaas M, Tengs T, Hellberg H, Johansen R. First Description of a New Disease in Rainbow Trout (Oncorhynchus mykiss (Walbaum)) Similar to Heart and Skeletal Muscle Inflammation (HSMI) and Detection of a Gene Sequence Related to Piscine Orthoreovirus (PRV). PLoS One. 2015 Jul 15;10(7):e0131638. doi: 10.1371/journal.pone.0131638. eCollection 2015. PubMed PMID: 26176955; PubMed Central PMCID: PMC4503464.

[18]  Dahle MK, Wessel Ø, Timmerhaus G, Nyman IB, Jørgensen SM, Rimstad E, Krasnov  A. Transcriptome analyses of Atlantic salmon (Salmo salar L.) erythrocytes infected with piscine orthoreovirus (PRV). Fish Shellfish Immunol. 2015 Aug;45(2):780-90. doi: 10.1016/j.fsi.2015.05.049. Epub 2015 Jun 6. PubMed PMID: 26057463.

[19]  Bjørgen H, Wessel Ø, Fjelldal PG, Hansen T, Sveier H, Sæbø HR, Enger KB, Monsen E, Kvellestad A, Rimstad E, Koppang EO. Piscine orthoreovirus (PRV) in red and melanised foci in white muscle of Atlantic salmon (Salmo salar). Vet Res. 2015 Sep 8;46:89. doi: 10.1186/s13567-015-0244-6. PubMed PMID: 26346256; PubMed Central PMCID: PMC4562189.

[20] Siah A, Morrison DB, Fringuelli E, Savage P, Richmond Z, Johns R, et al. (2016) “Piscine Reovirus: Genomic and Molecular Phylogenetic Analysis from Farmed and Wild Salmonids Collected on the Canada/US Pacific Coast” PLoS ONE 11(10): e0164926.

[21] Erratum in above publication: PLoS One. 2016 Oct 12;11(10 ):e0164926. PubMed PMID: 26536673; PubMed Central PMCID: PMC4633109.

[22] Madhun AS, Isachsen CH, Omdal LM, Bårdsgjære Einen AC, Bjørn PA, Nilsen R, Karlsbakk E. 2016. Occurrence of salmonid alphavirus (SAV) and piscine orthoreovirus (PRV) infections in wild sea trout Salmo trutta in Norway. Dis Aquat Organ. 120(2):109-13. doi: 10.3354/dao03009. PubMed PMID: 27409234.

[23]  Haatveit HM, Nyman IB, Markussen T, Wessel Ø, Dahle MK, Rimstad E. 2016. The non-structural protein μNS of piscine orthoreovirus (PRV) forms viral factory-like structures. Vet Res. 2016 Jan 8;47:5. doi: 10.1186/s13567-015-0302-0. PubMed PMID: 26743679; PubMed Central PMCID: PMC4705589.

[24] Godoy MG, Kibenge MJT, Wang Y, Suarez R, Leiva C, Vallejos F, and Kibenge FSB. 2016. First description of clinical presentation of piscine orthoreovirus (PRV) infections in salmonid aquaculture in Chile and identification of a second genotype (Genotype II) of PRV. Virology Journal 201613: 98-112.

[25] Takano T, Nawata A, Sakai T, Matsuyama T, Ito T, Kurita J, et al.. Full-genome sequencing and confirmation of the causative agent of erythrocytic inclusion body syndrome in coho salmon identifies a new type of piscine orthoreovirus. PLoS ONE 2016 11(10): e0165424.

[26] Lund M, Røsæg MV, Krasnov A, Timmerhaus G, Nyman IB, Aspehaug V, Rimstad E, Dahle MK. 2016. Experimental piscine orthoreovirus infection mediates protection against pancreas disease in Atlantic salmon (Salmo salar). Vet Res. 2016 Oct 21;47(1):107. PubMed PMID: 27769313; PubMed Central PMCID: PMC5075195.

[27] Wiik-Nielsen J, Alarcón M, Jensen BB, Haugland Ø, Mikalsen AB. Viral co-infections in farmed Atlantic salmon, Salmo salar L., displaying myocarditis.  J Fish Dis. 2016 Dec;39(12):1495-1507. doi: 10.1111/jfd.12487. Epub 2016 May 5. PubMed PMID: 27146423.

[28] Morton A, Routledge R. 2016. Risk and precaution: salmon farming. Marine Policy 74: 206-212.

[29] Di Cicco E, Ferguson HW, Schulze AD, Kaukinen KH, Li S, Vanderstichel R, Wessel Ø, Rimstad E, Gardner IA, Hammell KL, and Miller KM. 2017. Heart and skeletal muscle inflammation (HSMI) disease diagnosed on a British Columbia salmon farm through a longitudinal farm study. PLoS ONE 12(2): e0171471. doi:10.1371/journal. pone.0171471

[30] Haatveit HM, Wessel Ø, Markussen T, Lund M, Thiede B, Nyman IB, Dahle MK, Rimstad E. 2017. Viral Protein Kinetics of Piscine Orthoreovirus Infection in Atlantic Salmon Blood Cells. Viruses 2017, 9, 49; doi:10.3390/v9030049

[31] Wessel Ø, Braaen S, Alarcon M, Haatveit, H, Roos N, Markussen T, Tengs T, Maria K. Dahle MK, Rimstad E. (2017) Infection with purified Piscine orthoreovirus demonstrates a causal relationship with heart and skeletal muscle inflammation in Atlantic salmon. PLoS ONE 12(8): e0183781.

[32] Miller KM, Günther OP, Li S, Kaukinen KH, Ming TJ (2017) Molecular indices of viral disease development in wild migrating salmon. Conserv Physiol 5(1): cox036; doi:10.1093/conphys/cox036.

[33] Kibenge MJT, Wang Y, Morton A, Routledge R, Kibenge FSB (2017) Formal comment on: Piscine reovirus: Genomic and molecular phylogenetic analysis from farmed and wild salmonids collected on the Canada/US Pacific Coast. PLoS ONE 12(11): e0188690.

[34] Morton A, Routledge R, Hrushowy S, Kibenge M, Kibenge F (2017) The effect of exposure to farmed salmon on piscine orthoreovirus infection and fitness in wild Pacific salmon in British Columbia, Canada. PLoS ONE 12(12): e0188793.

[35] Hauge H, Vendramin N, Taksdal T, Olsen AB, Wessel Ø, Mikkelsen SS, Alencar ALF, Olesen NJ, Dahle MK. (2017). Infection experiments with novel Piscine orthoreovirus from rainbow trout (Oncorhynchus mykiss) in salmonids. PLoS ONE 12(7): e0180293.

[36] Madhun AS, Isachsen CH, Omdal LM, Einen ACB, Mæhle S, Wennevik V, Neimel E, Svåsand T, Karlsbakk E. (2018). Prevalence of piscine orthoreovirus and salmonid alphavirus in sea-caught returning adult Atlantic salmon (Salmo salar L.) in northern Norway. J Fish Dis. 2018;41:797–803.

[37] Cartagena, J., Tambley, C., Sandino, A. M., Tello, M., Sandino Garcia, A. M., Sandino Garcia, A. M., … Tello Reyes, M. C. (2018). Detection of piscine orthoreovirus in farmed rainbow trout from Chile. Aquaculture, 493, 79-84.

[38] Tucker S, Li S, Kaukinen KH, Patterson DA, Miller KM (2018) Distinct seasonal infectious agent profiles in life-history variants of juvenile Fraser River Chinook salmon: An application of high-throughput genomic screening. PLoS ONE 13(4): e0195472.

[39] Di Cicco E, Ferguson H, Kaukinen K, Shulze A, Li S, Tabata A,  Günther O, Mordecai G, Suttle C, Miller K. (2018). The same strain of Piscine orthoreovirus (PRV) is involved with the development of different, but related, diseases in Atlantic and Pacific Salmon in British Columbia. FACETS (Accepted for publication, April, 2018).

[40] Dhamotharan, K., Vendramin, N., Markussen, T., Wessel, Ø., Cuenca, A., Nyman, I. B., Olsen, A. B., Tengs, T., Krudtaa Dahle, M. and Rimstad, E. 2018. Molecular and antigenic characterization of Piscine orthoreovirus (PRV) from Rainbow Trout (Oncorhynchus mykiss). Viruses 10(4): 1-16.

[41] Kuehn, R., Stoeckle, B. C., Young, M., Popp, L., Taeubert, J. E., Pfaffl, M. W. and Geist, J. 2018. Identification of a piscine reovirus-related pathogen in proliferative darkening syndrome (PDS) infected brown trout (Salmo trutta fario) using a next-generation technology detection pipeline. PLoS One 13(10): e0206164.

[42] Wang Y. (2018). The physiological associations between infectious agents and migrating juvenile chinook salmon (Oncorhynchus tshawytscha). MSc thesis, University of British Columbia

[43] Wessel Ø, Krasnov A, Timmerhaus G, Rimstad E, Dahle M. (2019). Antiviral responses and biological consequences of piscine orthoreovirus infection in salmonid erythrocytes.

[44] Kibenge MJT, Wang, Gayeski N, Morton A, Beardslee K, McMillan B, Kibenge, FSB. (2019). Piscine orthoreovirus sequences in escaped farmed Atlantic salmon in Washington and British Columbia. Virology Journal 16:41

Sea lice research

2000 Mustafa et al. [1]: Evidence salmon with sea lice are more susceptible to other viruses.

2006 Costello. [2]: Evidence sea lice can kill wild and farmed fish

2007 Krkošek et al. [3]: Evidence open-fish farms are the primary source of heavy Leps infestations on wild juvenile salmon

2008 Morton et al. [4]: Evidence open-fish farms contribute to sea lice infestations in wild salmon

2010 Mages and Dill. [5]: Evidence sea lice is detrimental to the swimming ability of salmon.

2010 Marty et al [6]: Link between farm salmon, sea lice and wild salmon populations

2010 Price et al. [7]. Evidence of farm-induced parasite infestations on nearby wild juvenile salmon in coastal British Columbia

2011 Jakob et al. [8]: Sea lice shown to act as a vector to other viruses.

2011 Price et al. [9]. Further evidence sea louse infection of juvenile salmon in relation to salmon farms in British Columbia

2011 Nendick et al. [10]: Further evidence sea lice is detrimental to swimming ability of salmon

2012 Connors et al. [11]: Open-fish farms impact wild salmon migration ability

2013 Barker. [12]: Salmon with sea lice are more susceptible to the ISA virus.

2014 Jeffries et al. [13]: Discovery that pathogen presence predicts migration survival in wild salmon

2015 Thorstad et al. [14]. Effects of salmon lice Lepeophtheirus salmonis on wild sea trout

2016 Bateman et al. [15]: Sea lice levels have increased in the Broughton Archipelago

2017 Shephard and Gargan. [16]: Further evidence of link between sea lice from aquaculture and declining annual returns in a wild Atlantic salmon population

[1] Mustafa, A et al. 2000. Enhanced susceptibility of seawater cultured rainbow trout, Oncorhynchus mykiss (Walbaum), to the microsporidian Loma salmonae during a primary infection with the sea louse, Lepeophtheirus salmonis. J Fish Dis 23: 337- 341.

[2] Costello, MJ. 2006. Ecology of sea lice parasitic on farmed and wild fish. Trends Parasitol 22: 475-483.

[3] Krkošek, M et al. 2007a. Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations. Proc R Soc B 274: 3141-3149.

[4] Morton, A et al. 2008. Sea louse infestation in wild juvenile salmon and Pacific herring associated with fish farms off the east-central coast of Vancouver Island, British Columbia. NA J Fish Manag 28: 523–532.

[5] Mages, PA & Dill, LM. 2010. The effect of sea lice (Lepeophtheirus salmonis) on juvenile pink salmon (Oncorhynchus gorbuscha) swimming endurance. Can J Fish Aquat Sci 67: 2045-2051.

[6] Marty, GD et al. 2010. Relationship of farm salmon, sea lice, and wild salmon populations. Proc Natl Acad Sci USA 107: 22599-22604.

[7] Price, MHH et al. 2010. Evidence of farm-induced parasite infestations on wild juvenile salmon in multiple regions of coastal British Columbia, Canada. Can J Fish Aquat Sci 67: 1925–1932.

[8] Jakob, E et al. 2011. Vector potential of the salmon louse Lepeophtheirus salmonis in the transmission of infectious haematopoietic necrosis virus (IHNV). Dis Aquat Org 97: 155-165.

[9] Price, MHH et al. 2011. Sea louse infection of juvenile sockeye salmon in relation to marine salmon farms on Canada’s west coast. PLoS ONE 6(2): e16851.

[10] Nendick, L et al. 2011. Sea lice infection of juvenile pink salmon (Oncorhynchus gorbuscha): effects on swimming performance and postexercise ion balance. Can J Fish Aquat Sci 68: 241-249.

[11] Connors, BM et al. 2012. Migration links ocean-scale competition and local ocean conditions with exposure to farmed salmon to shape wild salmon dynamics. Conserv Letts 5: 304-312.

[12] Barker, S. 2013. Lice and isav: Are ‘lousy’ salmon more susceptible? Fish Shellfish Immunol 34: 1637-1638.

[13] Jeffries, KM et al. 2014. Immune response genes and pathogen presence predict migration survival in wild salmon smolts. Molec Ecol 23: 5803-5815.

[14] Thorstad, EB et al. 2015. Effects of salmon lice Lepeophtheirus salmonis on wild sea trout Salmo trutta – a literature review. Aquacult Environ Interact 7: 91- 113.

[15] Bateman, AW et al. 2016. Recent failure to control sea louse outbreaks on salmon in the Broughton Archipelago, British Columbia. Can J Fish Aquat Sci 73: 1-9.

[16] Shephard, S & P Gargan. 2017. Quantifying the contribution of sea lice from aquaculture to declining annual returns in a wild Atlantic salmon population. Aquacult Environ Interact 9: 181-192.

Fish farm waste research

1996 Kibria et al. [1]: Fish farms are found to produce dangerous quantities of phosphorus pollution

1998 Kibria et al. [2]: Nitrogen from fish farms is found to be polluting surrounding areas

2003 Miranda et al. [3]: An extensive list of chemicals are found to be caused by fish farms

2010 Burridge et al. [4]: A review unveiled the ocean pollution caused by chemical use in salmon aquaculture.

[1] Kibria, G et al.1996: Aspects of phosphorus pollution from aquaculture. Naga, the ICLARM Quarterly, 19(3), pp. 20-24.

[2] Kibria, G et al.1998: Can nitrogen pollution from aquaculture be reduced? Naga, the ICLARM Quarterly, 21(1), pp. 17-25.

[3] Miranda, C.D., et al. 2003. Diversity of tetracycline resistance genes in bacteria from Chilean salmon farms. Antimicrobial Agents and Chemotherapy 47 (2003). Pp 883-888.

[4] Burridge, L et al. 2010. Chemical use in salmon aquaculture: A review of current practices and possible environmental effects. Aquacult 306: 7-23.