Pathogens from Salmon Aquaculture in Relation to Conservation of Wild Pacific Salmon in Canada: An Alternative Perspective

Introduction

2.

In Clayoquot Sound on the west coast of Vancouver Island, estimates of the numbers of wild Chinook salmon (Oncorhynchus tshawytscha) spawners in three key rivers generally decreased during the 1960s and 1970s, with variable recovery since several salmon farms were established in Clayoquot Sound in the 1980s and 1990s (Table 2). Estimates for the annual average number of spawners in all three rivers combined did not decrease from the first 30 years of records (before salmon farms, 1953 – 1982, 757 fish per year) to the most recent 30 years of records (with salmon farms, 1993 – 2022, 964 fish per year). Salmon farms remain active in Clayoquot Sound.

3.

In the Broughton Archipelago of BC, estimates of the numbers of wild pink salmon (Oncorhynchus gorbuscha) adult returns (spawners plus catch) before salmon farms (1960 – 1989) and with salmon farms (1990 – 2014) were within the range of estimated returns to a nearby reference area during the same time (Table 3). Average annual return estimates to the nine Broughton Archipelago rivers increased 14% from the 30 years before salmon farms to the first 25 years with salmon farms; this estimate is between similar estimates based on all 55 reference-area rivers (40% decline) and a 5-river subset of reference-area rivers (43% increase, Table 3).

Presenting data from all 55 rivers and the 5-river subset identifies potential bias in the dataset – Available data from the 55 rivers changes from nearly complete during 1960 – 1989 (average = counts from 47 rivers per year) to less complete during 1990 – 2014 (average = counts from 35 rivers per year), with a decreasing trend within 1990 – 2014 (Table 3). The 24% decrease in the number of rivers with counts from 1960 – 1989 to 1990 – 2014 is nominally less than the 40% decrease in average annual returns over the two periods (Table 3). Therefore, at least some of the decrease might represent a true decrease in returns rather than just a decrease in efforts to count the returns. Data from the 5 selected rivers are nearly complete, but basing conclusions on these selected rivers risks biasing results away from decreasing returns.

1.

Cohen Commission (Cohen 2012): In 2009, the Canadian government established the Cohen Commission of Inquiry into the Decline of Sockeye Salmon in the Fraser River. The 2012 final report (Volume 3, page 24) concluded (emphasis added), “Data presented during this Inquiry did not show that salmon farms were having a significant negative impact on Fraser River sockeye.”

a.

Final Report Volume 2, page 164 – This conclusion was based, in part, on “a statistically significant declining trend in the number of high-risk diseases reported by salmon farms between 2003 and 2010.”

b.

This is a good example of the difference between risk and impact, because Justice Cohen’s assessment of the risk (Final Report Volume 3, page 22) was “I therefore conclude that the potential harm posed to Fraser River sockeye salmon from salmon farms is serious or irreversible.” Here, the evidence did not support a conclusion that a potential risk had manifested as an actual impact.

c.

Qualifier – Justice Cohen also stated (Final Report Volume 3, page 113), “Although the data available to this Inquiry do not suggest that salmon farms are having a significant negative impact on Fraser River sockeye, I am not prepared to conclude, based on that data, that there is a low risk to sockeye from salmon farms. It is simply too early to reach that conclusion.” Today, more than a decade of additional information since the Cohen Commission—including information in Table 1 and points 2, 3, and 4 below—supports a conclusion of low risk to sockeye salmon from salmon farms.

2.

Pacific Northwest Fish Health Protection Committee (Meyers 2017): “The ubiquitous nature of piscine orthoreovirus (PRV), its apparent historic presence in wild Pacific salmonid stocks in the Pacific Northwest and the lack of clear association with disease in Pacific salmonids suggest the virus poses a low risk to wild species of Pacific salmonids.” This committee is an American organization of technical, scientific, and policy representatives from conservation agencies, Indigenous tribes, and commercial fish producers from the Pacific Northwest.

3.

Independent scientists in the USA states of Alaska and Washington: From part of Reference 39 omitted by The Review (emphasis added), “The scientific information continues to support the conclusion that endemic PRV-1a in the PNW should be considered as posing a low risk (not zero) to Pacific salmon, thus requiring no significant changes to agency fish health policies.”

4.

Independent scientists: A 2012 paper reported that “recent decreases in abundance and productivity of Fraser River sockeye salmon occurred across a large geographic area” ranging from Washington to southeast Alaska (Peterman and Dorner 2012). Restated, this academic study found no differences between sockeye salmon populations regardless of whether they were exposed to salmon farms.

• With rare exceptions, the progression does not skip any stage. The progression can end at any stage; for example, fish can be infected but never develop lesions, or fish with disease can recover and eliminate the pathogen.
• qPCR tests can detect pathogen nucleic acid at any stage from exposure to death. However, qPCR tests also detect segments of nucleic acid that are not part of viable organisms or an active infection.
• qPCR tests can detect transcriptional changes (e.g., gene expression converting DNA to mRNA) at any stage from pathogen infection to death. However, qPCR tests also detect changes that occur as part of normal life in the absence of infection or disease.
• To demonstrate population-level impacts, the predictive value of information for making reliable estimates generally increases from early in this progression (e.g., exposure, as evidenced by PCR tests of gills with no other evidence of infection) to later in the progression (e.g., lesions as evidenced by ulcers on the skin or gills).

• Comment on “size and life-stage differences”: Among the three infectious agents highlighted in The Review, only sea lice has been shown to differentially impact smaller wild salmon compared to farmed salmon. However, as we have outlined in Main Point #1 above, these differences are not manifest at the population level after 40 years of salmon farming in BC.
• Comment on “differences in physiological infection susceptibility”: Twenty years ago, the understanding that Pacific salmon were more resistant to endemic diseases than Atlantic salmon farmed in BC was considered to be standard knowledge that did not require citation; for example, from the Introduction section of (Kim et al. 2004): “In recent years, production of Atlantic salmon has dominated the industry but the resistance of Pacific salmonids to endemic disease organisms is leading to increased interest in their culture.”
• We are not aware of any pathogens other than sea lice for which wild salmon are more susceptible to infection than farmed salmon. However, wild Pacific salmon are probably less susceptible to Tenacibaculum maritimum than farmed Atlantic salmon (Salmon salar). This hypothesis is based on greater frequency of disease due to T. maritimum in farmed Atlantic salmon vs. farmed Pacific salmon species (see Main Point #6, item 3 below).
• Comment on “inability to benefit from vaccines, antibiotics, and other treatments”: Most farmed Chinook salmon in BC are grown organically without antibiotics or sea lice treatments. No BC farmed Atlantic salmon or Pacific salmon species are vaccinated against any of the three infectious agents highlighted in The Review (i.e., PRV, sea lice, or T. maritimum). And yet, only about 3% die each year from infectious diseases (page 11-9 of BCSFA 2024). Where lack of treatments for wild salmon increased mortality of infected fish, the time that those fish were infectious to cohorts would also decrease.
• Comment on “susceptibility to mortality from multiple ecological processes that pathogens can modulate, such as predation, competition, migration, and environmental stress”: Where these variables increase mortality of infected wild salmon, the time that those fish were infectious to cohorts would also decrease.
• Important information omitted by The Review: Study of 652 samples from BC sockeye salmon (Thakur et al. 2019) collected “from before and during aquaculture expansion in BC (1985–94)” yielded a conclusion that, “In general, our data suggest that agent distributions may not have substantially changed because of the salmon aquaculture industry.” This supports the hypothesis that wild salmon populations have been living with the potential pathogens that affect farm salmon for as long as there have been wild salmon. A possible exception is PRV (Reference 8), but BC PRV has not been shown to cause significant disease to Pacific salmon species under controlled laboratory conditions (References 94 – 97).

1.

References 34 and 72 coauthor AM reported more than 25 lice per infested farm salmon in the Broughton Archipelago in 2000 (Morton and Volpe 2002).

2.

All early records of sea lice infestations on farmed BC Atlantic salmon better fit the hypothesis that lice have been common on these fish since Atlantic salmon farming began in BC during the 1980s:

A.

(Hicks 1989) – “Lice are commonly present on both wild and farmed stock.”

B.

(Brackett et al. 1991) – “Indeed, in this survey, only sea lice were nearly comparable to BKD as a cause of morbidity in Atlantic salmon.”

C.

Reference 169 (1992) – “In the Pacific Northwest, two species of sea lice commonly infect and cause disease in sea-farmed salmonids: Lepeophtheirus salmonis (the salmon louse) and Caligus clemensi (Figure 31).”

D.

(Stephen and Iwama 1997) – “Sea lice management in B.C. is accomplished largely through non-medicinal approaches such as fallowing and single-year class production and selection of species farmed, as well as by the presentation of ivermectin in feed.”

1.

The Review regarding the disease heart and skeletal muscle inflammation (HSMI; emphasis added): “Controlled laboratory challenge trials conducted in Norway have established that different isolates of PRV-1 vary in virulence (i.e., disease severity) and that a PRV-1a isolate from BC can cause lesions diagnostic of HSMI, but in a lower proportion of infected individuals than the most virulent PRV-1b isolate dominant in Norway (86).”

Problem: Incorrect reporting of a cited reference.

Comment: The statement that “a PRV-1a isolate from BC can cause lesions diagnostic of HSMI” is contrary to what Reference 86 concludes (emphasis added): “Following peak replication in blood, the two Norwegian 2018 isolates induced histopathological lesions in the heart consistent with HSMI, whereas all three historical Norwegian and the Canadian isolates induced only mild cardiac lesions.” Mild cardiac lesions are not diagnostic for HSMI. Neither regulatory nor judicial decisions should be based on incorrect summaries of the evidence.

2.

The Review: “Recent studies on wild Pacific salmon have indicated that the spread of T. maritimum from salmon farms is a risk to infection and survival of wild fish (9, 19).” Also, The Review’s critique of Reference 110 includes, “low impact was predicated on a low detection rate, an interpretation that subsequent work has shown to be invalid (9).” The Review cites Reference 9 four other times in similar context. The “low detection rate” is based on Reference 158, which reported 5 of 2,006 (0.25%) juvenile Fraser River sockeye salmon sampled in the spring and summer of 2012 and 2013 that were qPCR+ for T. maritimum with copy number greater than the limit of detection.

Problem: Overstating the significance of a reference.

Comment: Our efforts to obtain the datasets for References 9 and 158 from the authors were not successful. However, the data used for Reference 9 seem to be included in the Reference 37 dataset. Of the 2,280 sockeye samples in the Reference 37 dataset that seem to match the description of the data in Reference 9, only 1.4% have a copy number greater than the limit of detection (LOD = 1.9 copies, from Bass et al. 2024), which is not substantially different from the 0.25% reported by Reference 158 and used by Reference 110. Further, we believe that the analysis reported in Reference 9 is invalid because all but three of the detections are less than 200 copies and, therefore, might be false positives. The data in Reference 9 are from 2008 – 2018, but the three probable true positives are all from 2015, which was an unusually warm year (Reference 9). We agree with Reference 9 that this is evidence that T. maritimum is more likely to grow in BC during abnormally warm years. However, neither regulatory nor judicial decisions should be based on a dataset that includes only three fish.

3.

The Review: “T. maritimum is known to have caused substantial health issues for Pacific salmonids in California (104), Chile (105, 106), New Zealand (107), and Alaska (108).”

Problem: Important information omitted.

Comment: Omitted is (i) disease due to T. maritimum has never been reported in wild sockeye salmon, and (ii) disease due to T. maritimum is rare among farmed Chinook salmon and coho salmon in BC. From 2002 – 2018, government veterinarians in charge of health audits of BC salmon farms diagnosed farm-level mouthrot (which is caused by T. maritimum) for 106 of 1,446 Atlantic salmon farm audits but for 0 of 273 Pacific salmon farm audits (Wade and Weber 2020). Since its inception by the BC provincial government, this audit program samples only moribund and freshly dead fish because it “enhances the likelihood of detection of disease” (BC-MAL 2006). Among these 273 Pacific salmon farm audits, two audits included individual fish (i.e., not farm level) diagnosed with mouthrot: three Chinook salmon sampled in 2009 (Wade and Weber 2020) and one coho salmon sampled on 2014-03-20 (DFO 2024c). The DFO audit program has not diagnosed mouthrot among the 655 farmed Pacific salmon sampled as part of the program since 2014-03-20 and through 2022 (DFO 2024c).

4.

The Review: “While T. dicentrarchi is highly virulent in some hosts (Atlantic salmon, rainbow trout), including wild and farmed Chinook in BC (127), it may have little effect in others, such as coho (119).”

Problem: Incorrect reporting of a cited reference. Important information omitted.

Comment: Reference 127 does not report sampling or examining any farmed fish. Instead, Reference 127 is a study of Chinook salmon that developed lesions associated with T. dicentrarchi infection 4 days after they were captured from the wild and held in tanks. Also, Reference 127 reports no lesions at the time of capture; therefore, Reference 127 provides no information about the virulence of T. dicentrarchi among Chinook salmon in the wild. Finally, Reference 127 is a non-peer reviewed manuscript that was posted on BioRxiv on 2023-02-21, 16 months before The Review was accepted for publication; The Review omits reasons that Reference 127 has not passed peer review.

5.

The Review: “Wild BC Chinook salmon infected with PRV-1a in their first year of ocean life have … lesions that indicate the early signs of jaundice/anemia (16).” Also, The Review says that recent studies “indicate that PRV-1a is associated with jaundice/anemia in farmed (15) and wild Chinook salmon in BC (16) ….”

Problem: Incorrect reporting of a cited reference. Contrary to the statement in The Review, Reference 16 does not report that any sampled wild salmon had jaundice or anemia.

Comment: Reference 16 reported qPCR test results for 46 infectious agents, including PRV, in samples from 319 juvenile Chinook salmon. Histopathology was done on selected samples from 44 fish that tested strongly qPCR-positive for at least one of six infectious agents, including samples from eight fish with the greatest PRV copy numbers. The analysis included no fish that had no or low copy numbers for all six infectious agents (i.e., no reference fish). This analysis and interpretation have several limitations:

A.

Lesions that “indicate” the early signs of jaundice/anemia are hypothesized but unknown because BC PRV has never been shown to cause jaundice under controlled laboratory conditions (References 94 – 96).

B.

Lesions in the eight PRV+ fish are nonspecific. As evidence, all lesions that occurred among the eight selected PRV+ fish also occurred in at least one of the other 36 fish that were selected for copy load for one of six other infectious agents (Reference 16, Table S3).

• A nephrosis score = 1 is reported for two of eight fish selected for PRV copy number, one of four fish selected for P. theridion copy number, and one of six fish selected for C. shasta copy number.
• A renal interstitial hyperplasia score = 1 is reported for six of eight fish selected for PRV copy number and for 17 of the other 36 fish, including at least two fish in each of the six groups of infectious agents.

C.

Some information in the Reference 16 text does not match the results in its Table S3.

• Reference 16 describes “one [fish] with renal tubular vacuolar degeneration leading to necrosis of kidney tubules,” but its Table S3 does not include “renal tubular vacuolar degeneration,” and the score = 0 for all eight PRV+ fish in the kidney “necrosis” column.
• Reference 16 describes “some cases of mild necrosis in liver, spleen ellipsoids …,” but Table S3 lists score = 0 for all PRV-fish in the liver “necrosis” and spleen “ellipsoids necrosis” columns.

6.

The Review: “PRV infection of wild Pacific salmon has been correlated with exposure to salmon farms and impaired migration success (18, 57).”

Problem: Important information omitted.

Comment: Reference 57 hypothesized, “the decline in PRV infection between the low and high migration challenge groups suggests that PRV infection may reduce a host's capacity to complete a challenging upriver migration.” For the Fraser River, the pre-migration challenge and post-migration challenge samples were mostly different species. The 38 pre-challenge samples included no sockeye salmon (0%), but the 77 post-challenge samples included 74 sockeye salmon (96%). Samples were tested for three viruses (see the Pivot table in the S1 file of Morton et al. 2021), but only PRV was included in the analysis, despite similar trends in the decrease in prevalence pre- and post-migration challenge for all three viruses (Table 7).

A.

Reference 57 coauthor RR is also a coauthor on Reference 149, which is a critique of Reference 139. Reference 149 includes, “Selective reporting of analysis runs counter to basic statistical practice and scientific integrity ….”

B.

The two viruses not included in the analysis—infectious salmon anemia virus (ISAV) and salmonid alphavirus (SAV)—are reportable to the World Organization for Animal Health (WOAH). The WOAH’s list of susceptible species for ISAV (WOAH 2024) does not include any of the six species reported as positive for ISAV in the Reference 57 correction (Morton et al. 2021). Therefore, the WOAH does not recognize these ISAV test results as true positive results. Among the seven species listed as SAV+ by the Reference 57 correction (Morton et al. 2021), only steelhead (Oncorhynchus mykiss) are considered susceptible to SAV infection; these steelhead account for 6 of the 49 (12%) SAV+ results reported in the study. The WOAH-recognized competent authority for Canada is the Canadian Food Inspection Agency (CFIA); CFIA reports that Canada has “Pathogen freedom at the level of the country” for SAV (CFIA 2022), so CFIA does not recognize these SAV test results as true positive results.

C.

The Review does not explain the reason(s) that one coauthor (AM) is reporting sample prevalences of ISAV (21%) and SAV (24%) while another coauthor (KMM) reports sample prevalence of 0% for these viruses in wild salmon samples (e.g., Thakur et al. 2019).

D.

Of the 115 PRV Ct values reported by Reference 57, 110 (96%) have a Ct value >34.0. The five fish with a PRV Ct value < 34.0 include two fish classified as exposed to salmon farms and three fish classified as not exposed to salmon farms. These results do not support The Review’s citation of Reference 57 for “PRV infection of wild Pacific salmon has been correlated with exposure to salmon farms.”

7.

The Review: “PRV infection of wild Chinook likely also affects predation, competition, and migration outcomes, which could remove infected individuals earlier in the disease progression than the advanced stages of jaundice/anemia observed in farmed Chinook.”

Problem: Important information omitted.

Comment: The Review’s coauthor AM in 2019 reported several jaundiced wild salmon and wrote (Morton 2019), “I took samples, which I will have tested [for PRV].” This is evidence that jaundiced wild salmon do survive to be observed. Omitted from The Review are the results from those PRV tests. Also, if the Miller laboratory tested jaundiced wild salmon for PRV, those results are also omitted from The Review.

8.

The Review: Regarding the sea lice species Lepeophtheirus salmonis, “Controlled laboratory trials have shown that sockeye salmon infected with L. salmonis experience mortality, skin erosion, scale loss, and high levels of stress (145).”

Problem: Statement is not ecologically relevant.

Comment: Reference 145 reports mortality with a laboratory-induced lice load—50 preadult L. salmonis per 135 g fish—that is not ecologically relevant. Surveys of BC sockeye salmon report that 95% of juvenile BC sockeye salmon have no L. salmonis, and only 0.2% have more than five L. salmonis per fish (page 10-29 of BCSFA 2024). Reference 145 reports that for fish at average mass of 40 g or 80 g when exposed to L. salmonis, none died during the experiment that lasted 34 – 36 days postinfection; when skin abrasions and scale loss were first noted at 21 days postinfection, these fish were infested with about 14 preadult lice per fish. Reference 145 did not test the effect of ecologically relevant sea lice loads.

9.

A relatively new sea lice treatment, hydrolicing, involves transferring farm salmon from the net pen to a well-boat, using jets of water to remove the lice, and then returning the fish to the net pen; unlike some treatment alternatives, hydrolicing involves no chemicals. Regarding hydrolicing in BC, The Review reports the following:

A.

“… the implementation of hydrolicing is coincident with an increase in incidental bycatch mortality of herring reported from salmon aquaculture sites in BC from less than 100,000 fish annually in 2011 to 2020 to over 800,000 in 2023 (156).”

Problems: Incorrect and deceptive reporting of a cited reference. Important information omitted.

Comment: Reference 156 is incorrectly listed in The Review’s References and Notes section with a date of 2020, and the year with over 800,000 herring is 2022, not 2023. Reference 156 shows that in 2023, incidental catch of herring was 52,000 fish, which is about the same as in 2016. To put the 800,000 fish in perspective (page 1-16 of BCSFA 2024), “The total Pacific herring incidental catch mortality at all salmon farms combined for all areas was equivalent to 0.086% of the herring spawning biomass for West Coast Vancouver Island that year”. At that level of mortality, it would take more than 11 years to add up to 1%.

Hydrolicing alone cannot explain the high incidental catch in 2022. Hydrolicing is used throughout BC to control sea lice, but in 2022, 99.6% of the Pacific herring (Clupea pallasii) incidental catch was in a single area (Clayoquot Sound); 88% of that was during the first 6 months of the year (Reference 156).

Whatever the cause in 2022, incidental catch is now closer to historical lows. For the first nine months of 2024, incidental catch of Pacific herring in Clayoquot Sound was 17,779, which is on track to be among of the lowest annual totals since 2011 (updated dataset cited as Reference 156; accessed 2025-01-24).

Finally, to further put this number in perspective, humpback whales (Megaptera novaeangliae) in the eastern Pacific are estimated to eat about 1,000 tonnes of prey in a 100-day feeding season, or 10 tonnes per day (Savoca et al. 2021). In British Columbia, about 10% of this prey is estimated to be juvenile Pacific herring, or 1,000 Kg per day (Moreaux 2025). If the consumed juvenile Pacific herring are 20g each (= 50 per Kg), then a single humpback whale consumes about 50,000 Pacific herring per day. Therefore, the total incidental catch of Pacific herring by the entire BC salmon aquaculture sector in 2023 is what one humpback whale eats in a single day.

B.

“… these alternative treatment methods … can increase stress on treated salmon (153, 154) through loss of mucus and scales that normally help protect fish against infectious microbial agents. These host effects likely increase vulnerability to disease (154, 155) ….”

Problem: Omitting evidence communicates risk that is contrary to the evidence.

Comment: In BC, alternative treatments like hydrolicing have not been associated with a significant change in infectious disease Fish Health Events reported to regulators as a condition of licence (Figure 3 in Jyoti et al. 2024). Hydrolicing was first used in BC to control sea lice in 2018, followed by annual increases in the number of treatments through 2022 (DFO 2023).

C.

“Although hydrolicers and bath treatments may remove lice from farms, viable larval lice are released back into the nearby marine environment (A. Morton, personal observation).”

Problem: Omitting regulatory information communicates risk that is contrary to the evidence.

Comment: This quote could be interpreted to say that all viable larval lice removed from farm salmon are released back into the nearby environment, but this interpretation is not correct. Marine finfish B.C. aquaculture licence and conditions of licence (DFO 2024a) include (emphasis added), “6.13 The Licence Holder must ensure that all mechanical and bath treatments carried out on vessels and barges as Sea Lice Mitigation capture and retain removed sea lice, which must be collected and disposed of on land.”

10.

The Review: “CSAS concluded that there is a high likelihood of transmission of PRV-1 from farmed salmon to wild sockeye salmon, but with uncertainty ranging from low to high (162).” Also, regarding the Canadian Science Advisory Secretariat (CSAS) assessment of the risk of PRV to BC wild salmon, “The 2019 risk assessment concluded that PRV-1 has been associated with severe heart inflammation in farmed Atlantic salmon. Those conclusions unconventionally excluded research conducted outside of Canada, which has causally linked PRV-1, including a variant from western North America, to HSMI in Atlantic salmon (161).”

Problem: Incorrect and deceptive reporting of a cited reference.

Comment: Reference 162 is incorrectly linked to the CSAS report for viral hemorrhagic septicemia virus (VHSV), not PRV. Here is the correct reference for 162: DFO. 2019. Advice from the assessment of the risk to Fraser River Sockeye Salmon due to piscine orthoreovirus (PRV) transfer from Atlantic Salmon farms in the Discovery Islands area, British Columbia. DFO Can. Sci. Advis. Sec. Sci. Advis. Rep. 2019/022.

The 2019 PRV CSAS report’s listing that “PRV-1 has been associated with severe heart inflammation in farmed Atlantic salmon” in BC was a “characterization,” not a conclusion, and the listing was followed by important information omitted by The Review: “but a causal relationship has not been established.”

Reference 161 is a perspectives paper, not a laboratory report that could have determined whether BC PRV causes HSMI. Reference 161 cites a 2016 email from scientist Espen Rimstad that includes, “there is no doubt that the isolate [PRV from BC] … causes HSMI.” However, this email was not peer reviewed, and it does not mention whether controls were examined. Dr. Rimstad’s peer-reviewed description of the effects of BC PRV (“the Canadian isolates induced only mild cardiac lesions”; Reference 86) is consistent with the 2019 CSAS PRV report (i.e., not HSMI). Reference 86 was published in 2020, so it could not have been cited by the 2019 CSAS report. Neither regulatory nor judicial decisions should rely on a preliminary email statement that is contrary to later peer-reviewed interpretation from the same scientist.

11.

The Review: “Some challenge studies in BC and Washington (with PRV-1a in Pacific salmon species) have not observed mortality or clinical jaundice/anemia (94–96). The data and observations in some of those studies, however, did show early signs of disease progression toward jaundice/anemia, consistent with observations from PRV-infected farmed Chinook salmon in BC (15) ….”

Problem: Deceptive reporting of cited references.

Comment: This quote could be interpreted to say that some, but not all, challenge studies have not observed mortality or jaundice, but that interpretation is incorrect. It would be clearer to say, “No challenge studies have reported mortality or jaundice.” If the Miller laboratory has conducted a challenge study exposing Chinook salmon to PRV derived from jaundiced salmon, those results are omitted from The Review.

Reference 15 is an observational study of samples from moribund and freshly dead farm salmon in BC that were collected by government auditors, not by the study authors. The assignment of “early signs of disease progression toward jaundice/anemia” in fish that are all end-stage (i.e., moribund or dead) is a hypothesis that is contrary to laboratory study, which has never proceeded to jaundice/anemia. While we are confident that PRV causes minor lesions in some Pacific salmon (e.g., Reference 95), we do not know what role—if any—these lesions play in the development of jaundice, which has never occurred in controlled laboratory study with PRV.

12.

The Review: “The abundance and density of fish in salmon farms present ideal conditions for the growth of viruses, bacteria, and parasites (4–6) (collectively “pathogens”). This can create a new source of transmission to wild Pacific salmon that would not exist naturally (6), and the associated risks are likely to be elevated whether or not a pathogen is exotic.”

Problem: Omits important information.

Comment: For as long as wild salmon have existed, migrating salmon have probably been naturally exposed to millions of infected salmon. Farms add no more than a slight variation to this pattern.

The number of infectious agents per fish is similar for farm salmon and wild salmon (e.g., see References 37, 169, and 201). Based on data in The Review’s Figure 1B, annual salmon aquaculture production varied around 80,000 tonnes from 2010 – 2019; if harvested fish average 5 kg, then during that time about 16 million maturing farm salmon were spread among the BC farms each year. From 2010 – 2015, more than 20 years after salmon farms were established along the migration routes of Fraser River salmon, adult salmon populations returning to just the Fraser River equalled or exceeded 15 million on four occasions (Table G4 of Reference 63):

• sockeye salmon – 28 million (2010), 19 million (2014)
• pink salmon – 21 million (2011), 16 million (2013)

These maturing fish would have been exposed to infectious disease among their cohorts—probably for several weeks—as they concentrated towards the mouth of the Fraser River. The number of sockeye salmon juveniles outmigrating from the Fraser River from just Chilko Lake exceeded 50 million in 2010, 2014, and 2015 (page 36 of Hawkshaw et al. 2020); these fish were exposed to cohorts for several weeks as they migrated out of the Fraser River and into the Pacific Ocean.

The Review cites evidence that infectious agent environmental DNA (eDNA) is elevated in the marine environment near active salmon farms (Reference 38), but we are not aware of any studies that have demonstrated that this increase is any different from what would occur from natural exposure to millions of migrating cohorts.

13.

The Review: “Stock-recruit fisheries models that include covariates for sea lice on farms near spawning rivers, or on juvenile wild salmon themselves, have provided evidence that sea lice on salmon farms are correlated with reduced population productivity for pink and coho salmon (34, 73, 74). Seemingly contradictory studies (134) ….”

Problem: Omits contrary information.

Comment: In this context, Reference 134 is not the only “seemingly contradictory” study. Omitted from The Review, but two of The Review’s coauthors (AM and MK) conducted a study (Morton et al. 2011) that compared survival of wild pink salmon populations that outmigrated as juveniles in 2007 through either (i) a corridor within the Broughton Archipelago with active salmon farms, (ii) a nearby corridor in which salmon farms were fallowed that spring, or (iii) a reference region to the north with no salmon farms:

• “The survival of the pink salmon cohort [within the Broughton Archipelago] was not statistically different from a reference region without salmon farms.”
• “From the rivers assessed in the Broughton Archipelago, only the Embly River clearly corresponds to the fallow migration route. That population experienced very poor survival, with a 90% decline, although it was subject to fallow intervention.”

In retrospect, the record high adult pink salmon returns to some Broughton Archipelago rivers in 2013 and 2014 are more consistent with results from the omitted contrary study (Morton et al. 2011) than with Reference 34.

[Main point #7] Did Competing Interests minimize scrutiny on publications cited by The Review?

1.

“To ensure that science advice does not reflect ‘unwarranted claims, unacceptable interpretations, or personal views,’ it needs to be reviewed independently from the body seeking advice (Kelly et al. 2014).” Fisheries and Oceans Canada (DFO) is the body that licenses salmon farms. The Review does not meet this definition of independent review for use by DFO because two coauthors (ALB and KMM) are affiliated with DFO.

2.

“For peer review to reliably assess the quality of research … for government science advice, reviewers must be independent and external from any focal party that may wish to ‘tip the scales’ (Hames 2008).” The Review does not meet this definition of independent review because most of its coauthors advocate to “tip the scales” towards salmon farm removal either directly or through organizational affiliations:

a.

The Pacific Salmon Foundation (PSF) is an advocate that does not meet this definition of independence. The 18 Dec 2023 message from Michael Meneer, President and CEO, PSF (Meneer 2023), includes (emphasis added), “PSF will continue to communicate our science and advocate for the removal of open-net pen salmon farms by 2025.” Nine of The Review’s 16 coauthors are either affiliated with the PSF (AWB, WSB, CMD, EDC, SG, SP, and BR), or they received from the PSF research funding (KMM) or postdoctoral funding (SG, WSB, CMD, and GM).

b.

The David Suzuki Foundation is an advocate that does not meet this definition of independence.

i.

The 14 December 2018 press release (David Suzuki Foundation 2018) includes (emphasis added), “We’ll continue to bring forward the latest, most credible science on risks to wild Pacific salmon populations, urging governments to get these ocean-based farms out of the way of wild salmon ….”

ii.

The 24 March 2021 press release (David Suzuki Foundation 2021) includes (emphasis added), “The David Suzuki Foundation, Georgia Strait Alliance, Living Oceans Society, Watershed Watch and independent biologist Alexandra Morton say stocking farms in the [Discovery Islands area of BC] would put wild salmon at risk. They are in court today to argue against granting an injunction to two fish farm companies, which want to stock pens in the Discovery Islands over the coming months.” Alexandra Morton is a coauthor of The Review.

iii.

The acknowledgements section of Reference 38 says that it “was supported by funding from the David Suzuki Foundation.” The author list for Reference 38 includes six of The Review’s coauthors (DS, AWB, GM, BMC, KMM, and MK).

c.

The founder and director of the Raincoast Research Society (The Review’s coauthor AM) is an advocate that does not meet this definition of independence. For example, in a 10 February 2022 article (Lewis and Morton 2022), AM writes (emphasis added), “The DFO bureaucracy must align with its minister and the Prime Minister’s Mandate Letter to remove salmon farms by 2025.”

1.

Lead author MK has published three papers reporting results from research partly funded by the aquaculture industry and coauthored with employees of DFO (Patanasatienkul et al. 2013) and the aquaculture industry (Rees et al. 2015; Rogers et al. 2013).

2.

Senior author KMM has projects partly funded by the aquaculture industry:

a.

(https://www.dfo-mpo.gc.ca/aquaculture/rp-pr/acrdp-pcrda/projects-projets/P-11-02-007-eng.html) – A final report has not yet been submitted for this project. One of us (GDM) is a collaborator on this project. An earlier draft of a final report for this project was released to the public (Reference 76) without permission from GDM or three other coauthors; GDM and the three other coauthors last submitted comments on a draft final report to KMM on 2021-04-01, but KMM has not responded to these comments.

b.

(https://www.dfo-mpo.gc.ca/aquaculture/rp-pr/acrdp-pcrda/projects-projets/P-04-01-006-eng.html) – Report from this work has been published (Funk et al. 2007).

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