Pathogens from salmon aquaculture in relation to conservation of wild Pacific salmon in Canada.

The spread of pathogens from farmed salmon is a conservation concern for wild Pacific salmon in British Columbia (BC), Canada. Three pathogens are prevalent in farmed Atlantic salmon in BC, spill over to wild Pacific salmon, and are linked to negative impacts on wild salmon: Piscine orthoreovirus, Tenacibaculum spp., and sea lice (Lepeophtheirus salmonis). Molecular screening of infectious agents in farmed and wild salmon and environmental DNA highlights a further 4 agents that are likely elevated near salmon farms and 37 that co-occur in wild and farmed salmon. Pathogens likely affect wild salmon indirectly by mediating migration, competition, and predation. Current net-pen aquaculture practices pose these risks to numerous populations of all species of wild salmon in BC, most of which are not covered in Government of Canada science and advisory reports. Climate change, pathogen evolution, and changes to disease management and aquaculture regulations will influence future risks.

Novel application of two- and four-lobed noise-canceling passive integrated transponder antennas for tracking fish in areas of high ambient electromagnetic interference.

Passive integrated transponder (PIT) technology is a leading tool for tracking fish in freshwater systems. PIT is highly applicable for assessing fish passage at anthropogenic infrastructure (e.g., dams and floodgates); however, there are often complications in operating PIT antennas near these structures due to the ambient electromagnetic interference of metal and power-supply equipment. We designed a PIT antenna that is resistant to the effects of ambient electromagnetic interference (AEMI). This design uses lobes with balanced polarity within the antenna to neutralize AEMI within the vicinity of the antenna. This novel PIT antenna provides a more effective and cost-efficient option for researchers tracking fish in environments with high AEMI.

Infectious agents and their physiological correlates in early marine Chinook salmon (Oncorhynchus tshawytscha).

The early marine life of Pacific salmon is believed to be a critical period limiting population-level survival. Recent evidence suggests that some infectious agents are associated with survival but linkages with underlying physiological mechanisms are lacking. While challenge studies can demonstrate cause and effect relationships between infection and pathological change or mortality, in some cases pathological change may only manifest in the presence of environmental stressors; thus, it is important to gain context from field observations. Herein, we examined physiological correlates with infectious agent loads in Chinook salmon during their first ocean year. We measured physiology at the molecular (gene expression), metabolic (plasma chemistry) and cellular (histopathology) levels. Of 46 assayed infectious agents, 27 were detected, including viruses, bacteria and parasites. This exploratory study identified.a strong molecular response to viral disease and pathological change consistent with jaundice/anemia associated with Piscine orthoreovirus,strong molecular signals of gill inflammation and immune response associated with gill agents `Candidatus Branchiomonas cysticola' and Parvicapsula pseudobranchicola,a general downregulation of gill immune response associated with Parvicapsula minibicornis complementary to that of P. pseudobranchicola.Importantly, our study provides the first evidence that the molecular activation of viral disease response and the lesions observed during the development of the PRV-related disease jaundice/anemia in farmed Chinook salmon are also observed in wild juvenile Chinook salmon.

Assessing the role of Piscine orthoreovirus in disease and the associated risk for wild Pacific salmon.

This paper is a response to Polinski, M. P. et al. Innate antiviral defense demonstrates high energetic efficiency in a bony fish. BMC Biology 19, 138 (2021). https://doi.org/10.1186/s12915-021-01069-2.

The spatial distribution of infectious agents in wild Pacific salmon along the British Columbia coast.

Although infectious agents can act as strong population regulators, knowledge of their spatial distributions in wild Pacific salmon is limited, especially in the marine environment. Characterizing pathogen distributions during early marine residence, a period considered a survival bottleneck for Pacific salmon, may reveal where salmon populations are exposed to potentially detrimental pathogens. Using high-throughput qPCR, we determined the prevalence of 56 infectious agents in 5719 Chinook, 2032 Coho and 4062 Sockeye salmon, sampled between 2008 and 2018, in their first year of marine residence along coastal Western Canada. We identified high prevalence clusters, which often shifted geographically with season, for most of the 41 detected agents. A high density of infection clusters was found in the Salish Sea along the east coast of Vancouver Island, an important migration route and residence area for many salmon populations, some experiencing chronically poor marine survival. Maps for each infectious agent taxa showing clusters across all host species are provided. Our novel documentation of salmon pathogen distributions in the marine environment contributes to the ecological knowledge regarding some lesser known pathogens, identifies salmon populations potentially impacted by specific pathogens, and pinpoints priority locations for future research and remediation.

Host-pathogen-environment interactions predict survival outcomes of adult sockeye salmon (Oncorhynchus nerka) released from fisheries.

Incorporating host-pathogen(s)-environment axes into management and conservation planning is critical to preserving species in a warming climate. However, the role pathogens play in host stress resilience remains largely unexplored in wild animal populations. We experimentally characterized how independent and cumulative stressors (fisheries handling, high water temperature) and natural infections affected the health and longevity of released wild adult sockeye salmon (Oncorhynchus nerka) in British Columbia, Canada. Returning adults were collected before and after entering the Fraser River, yielding marine- and river-collected groups, respectively (N = 185). Fish were exposed to a mild (seine) or severe (gill net) fishery treatment at collection, and then held in flow-through freshwater tanks for up to four weeks at historical (14°C) or projected migration temperatures (18°C). Using weekly nonlethal gill biopsies and high-throughput qPCR, we quantified loads of up to 46 pathogens with host stress and immune gene expression. Marine-collected fish had less severe infections than river-collected fish, a short migration distance (100 km, 5-7 days) that produced profound infection differences. At 14°C, river-collected fish survived 1-2 weeks less than marine-collected fish. All fish held at 18°C died within 4 weeks unless they experienced minimal handling. Gene expression correlated with infections in river-collected fish, while marine-collected fish were more stressor-responsive. Cumulative stressors were detrimental regardless of infections or collection location, probably due to extreme physiological disturbance. Because river-derived infections correlated with single stressor responses, river entry probably decreases stressor resilience of adult salmon by altering both physiology and pathogen burdens, which redirect host responses toward disease resistance.

Infected juvenile salmon can experience increased predation during freshwater migration.

Predation risk for animal migrants can be impacted by physical condition. Although size- or condition-based selection is often observed, observing infection-based predation is rare due to the difficulties in assessing infectious agents in predated samples. We examined predation of outmigrating sockeye salmon (Oncorhynchus nerka) smolts by bull trout (Salvelinus confluentus) in south-central British Columbia, Canada. We used a high-throughput quantitative polymerase chain reaction (qPCR) platform to screen for the presence of 17 infectious agents found in salmon and assess 14 host genes associated with viral responses. In one (2014) of the two years assessed (2014 and 2015), the presence of infectious haematopoietic necrosis virus (IHNv) resulted in 15-26 times greater chance of predation; in 2015 IHNv was absent among all samples, predated or not. Thus, we provide further evidence that infection can impact predation risk in migrants. Some smolts with high IHNv loads also exhibited gene expression profiles consistent with a virus-induced disease state. Nine other infectious agents were observed between the two years, none of which were associated with increased selection by bull trout. In 2014, richness of infectious agents was also associated with greater predation risk. This is a rare demonstration of predator consumption resulting in selection for prey that carry infectious agents. The mechanism by which this selection occurs is not yet determined. By culling infectious agents from migrant populations, fish predators could provide an ecological benefit to prey.

Aquaculture mediates global transmission of a viral pathogen to wild salmon.

Global expansion of aquaculture and agriculture facilitates disease emergence and catalyzes transmission to sympatric wildlife populations. The health of wild salmon stocks critically concerns Indigenous peoples, commercial and recreational fishers, and the general public. Despite potential impact of viral pathogens such as Piscine orthoreovirus-1 (PRV-1) on endangered wild salmon populations, their epidemiology in wild fish populations remains obscure, as does the role of aquaculture in global and local spread. Our phylogeographic analyses of PRV-1 suggest that development of Atlantic salmon aquaculture facilitated spread from Europe to the North and South East Pacific. Phylogenetic analysis and reverse transcription polymerase chain reaction surveillance further illuminate the circumstances of emergence of PRV-1 in the North East Pacific and provide strong evidence for Atlantic salmon aquaculture as a source of infection in wild Pacific salmon. PRV-1 is now an important infectious agent in critically endangered wild Pacific salmon populations, fueled by aquacultural transmission.

Descriptive multi-agent epidemiology via molecular screening on Atlantic salmon farms in the northeast Pacific Ocean.

Rapid expansion of salmon aquaculture has resulted in high-density populations that host diverse infectious agents, for which surveillance and monitoring are critical to disease management. Screening can reveal infection diversity from which disease arises, differential patterns of infection in live and dead fish that are difficult to collect in wild populations, and potential risks associated with agent transmission between wild and farmed hosts. We report results from a multi-year infectious-agent screening program of farmed salmon in British Columbia, Canada, using quantitative PCR to assess presence and load of 58 infective agents (viruses, bacteria, and eukaryotes) in 2931 Atlantic salmon (Salmo salar). Our analysis reveals temporal trends, agent correlations within hosts, and agent-associated mortality signatures. Multiple agents, most notably Tenacibaculum maritimum, were elevated in dead and dying salmon. We also report detections of agents only recently shown to infect farmed salmon in BC (Atlantic salmon calicivirus, Cutthroat trout virus-2), detection in freshwater hatcheries of two marine agents (Kudoa thyrsites and Tenacibaculum maritimum), and detection in the ocean of a freshwater agent (Flavobacterium psychrophilum). Our results provide information for farm managers, regulators, and conservationists, and enable further work to explore patterns of multi-agent infection and farm/wild transmission risk.

Capture severity, infectious disease processes and sex influence post-release mortality of sockeye salmon bycatch.

Bycatch is a common occurrence in heavily fished areas such as the Fraser River, British Columbia, where fisheries target returning adult Pacific salmon (Oncorhynchus spp.) en route to spawning grounds. The extent to which these encounters reduce fish survival through injury and physiological impairment depends on multiple factors including capture severity, river temperature and infectious agents. In an effort to characterize the mechanisms of post-release mortality and address fishery and managerial concerns regarding specific regulations, wild-caught Early Stuart sockeye salmon (Oncorhynchus nerka) were exposed to either mild (20 s) or severe (20 min) gillnet entanglement and then held at ecologically relevant temperatures throughout their period of river migration (mid-late July) and spawning (early August). Individuals were biopsy sampled immediately after entanglement and at death to measure indicators of stress and immunity, and the infection intensity of 44 potential pathogens. Biopsy alone increased mortality (males: 33%, females: 60%) when compared with non-biopsied controls (males: 7%, females: 15%), indicating high sensitivity to any handling during river migration, especially among females. Mortality did not occur until 5-10 days after entanglement, with severe entanglement resulting in the greatest mortality (males: 62%, females: 90%), followed by mild entanglement (males: 44%, females: 70%). Infection intensities of Flavobacterium psychrophilum and Ceratonova shasta measured at death were greater in fish that died sooner. Physiological indicators of host stress and immunity also differed depending on longevity, and indicated anaerobic metabolism, osmoregulatory failure and altered immune gene regulation in premature mortalities. Together, these results implicate latent effects of entanglement, especially among females, resulting in mortality days or weeks after release. Although any entanglement is potentially detrimental, reducing entanglement durations can improve post-release survival.

Predator swamping reduces predation risk during nocturnal migration of juvenile salmon in a high-mortality landscape.

Animal migrations are costly and are often characterized by high predation risk for individuals. Three of the most oft-assumed mechanisms for reducing risk for migrants are swamping predators with high densities, specific timing of migrations and increased body size. Assessing the relative importance of these mechanisms in reducing predation risk particularly for migrants is generally lacking due to the difficulties in tracking the fate of individuals and population-level characteristics simultaneously. We used acoustic telemetry to track migration behaviour and survival of juvenile sockeye salmon (Oncorhynchus nerka) smolts released over a wide range of conspecific outmigration densities in a river associated with poor survival. The landscape was indeed high risk; smolt survival was poor (˜68%) over 13·5 km of river examined even though migration was rapid (generally <48 h). Our results demonstrate that smolts largely employ swamping of predators to reduce predation risk. Increased densities of co-migrant conspecifics dramatically improved survival of smolts. The strong propensity for nocturnal migration resulted in smolts pausing downstream movements until the next nightfall, greatly increasing relative migration durations for smolts that could not traverse the study area in a single night. Smolt size did not appear to impact predation risk, potentially due to unique characteristics of the system or our inability to tag the entire size range of outmigrants. Movement behaviours were important in traversing this high-risk landscape and provide rare evidence for swamping to effectively reduce individual predation risk.

Fishing for Effective Conservation: Context and Biotic Variation are Keys to Understanding the Survival of Pacific Salmon after Catch-and-Release.

Acute stressors are commonly experienced by wild animals but their effects on fitness rarely are studied in the natural environment. Billions of fish are captured and released annually around the globe across all fishing sectors (e.g., recreational, commercial, subsistence). Whatever the motivation, release often occurs under the assumption of post-release survival. Yet, capture by fisheries (hereafter "fisheries-capture") is likely the most severe acute stressor experienced in the animal's lifetime, which makes the problem of physiological recovery and survival of relevance to biology and conservation. Indeed, fisheries managers require accurate estimates of mortality to better account for total mortality from fishing, while fishers desire guidance on strategies for reducing mortality and maintaining the welfare of released fish, to maximize current and future opportunities for fishing. In partnership with stakeholders, our team has extensively studied the effects of catch-and-release on Pacific salmon in both marine and freshwater environments, using biotelemetry and physiological assessments in a combined laboratory-based and field-based approach. The emergent theme is that post-release rates of mortality are consistently context-specific and can be affected by a suite of interacting biotic and abiotic factors. The fishing gear used, location of a fishery, water temperature, and handling techniques employed by fishers each can dramatically affect survival of the salmon they release. Variation among individuals, co-migrating populations, and between sexes all seem to play a role in the response of fish to capture and in their subsequent survival, potentially driven by pre-capture pathogen-load, maturation states, and inter-individual variation in responsiveness to stress. Although some of these findings are fascinating from a biological perspective, they all create unresolved challenges for managers. We summarize our findings by highlighting the patterns that have emerged most consistently, and point to areas of uncertainty that require further research.