TY - JOUR
AU - Miller, Kristina M
AB - Abstract Salmon farming has multiplied from a side business of coastal farmers to one of the world's major aquaculture species. This has dramatically altered the disease dynamics between farmed and wild salmonids. As salmon fish farming has increased, new restrictions have been enforced to combat emerging density-dependent impacts of pathogen spillover. In most northern and arctic regions, the effects of pathogens from fish farms on wild salmonids have been minimal for two key reasons: (i) relative low density of fish farms in the north and (ii) cold water temperatures. However, both factors are set to change dramatically. On one side, there is an increasing interest in utilizing northern areas for fish farming due to limited capacity for expansion in mid-latitude regions. On the other side, climate change is rapidly changing these northern ecosystems. High-latitude regions inhabit some of the largest remaining wild Atlantic salmon populations in the world along with sea trout and Arctic charr. Wild salmonids in the north have most likely seldom been exposed to high infection pressure, and we question how these populations will cope with changes that are coming. We identify 12 research questions emerging from these imminent changes and discuss methodologies for addressing them. We conclude that policies related to fish farming must consider uncertainties with respect to pathogen dynamics in the north until these research questions are fully addressed. Background Intensive marine finfish farming has been a hugely influential industry in many nations in recent decades (UN FAO, 2018). Farming of salmonids has particularly blossomed into a large international industry. Technological innovations (i.e. bacterial vaccines, means of production, fish feed development, genetic selection programmes) have now made it possible to produce salmon in quantities that nobody could have envisioned when the first salmon were introduced to net pens. Yet, fish farms are still mainly based on open net-pen production, which allow pathogens to freely spread through the surrounding water (Kent, 2000). Effects of these pathogens on wildlife are largely unknown but are generally recognized as a key threat to sustainability (Forseth et al., 2017). The conflict surrounding salmon aquaculture is often simplified into discussion of the effect of sea lice (Lepeophtheirus salmonis and Caligus spp.) from farmed fish on out-migrating wild salmon smolts. This has led to numerous studies on the impact of this parasitic copepod on marine survival of wild salmon (see Vollset et al., 2016). There is now little debate about whether salmon lice can have a negative impact on wild salmon, but it is still highly controversial how much of the declining marine survival of salmon observed in some regions can be attributed to the salmon lice originated from fish farming (Vollset, 2019). Traditional management of sea lice across salmon-producing countries has been to implement maximum allowable parasites per farmed fish (Jackson et al., 2018). A criticism of this system is that it does not account for the number of hosts, and therefore, infestation pressure arguably varies linearly with the number of farmed fish. Norway has recently implemented a new management protocol termed the Traffic Light System, which uses sustainability indicators in 13 delineated production regions to define whether biomass production will be allowed to increase or required to decrease (Olaussen, 2018). The intention of the Traffic Light System is to act as an environmental assessment that regulates the expansion of the fish farming industry based on ecological indicators. Despite myriad potential effects of aquaculture on the environment, assessments have so far focused solely on the effects of sea lice on wild fish. Southwestern Norway is consistently designated as an area of high impact due to high levels of sea lice infestation causing additive mortality >10% (Figure 1) whereas northern regions are designated as areas where aquaculture is allowed to increase production (Vollset et al., 2019). Lower densities of sea lice in the north can be attributable to less intense fish farming and colder annual temperatures that prolong generation time of the parasite and therefore a lower infestation pressure (Jansen et al., 2012). This has set the fish farming in Norway on a path to greatly expanding its production in northern regions, setting a course for rapid changes in disease dynamics. Figure 1. Open in new tabDownload slide Atlantic salmon (S. salar) farming production zones in Norway in 2017, divided into 13 districts coloured by their average salmon production calculated as the allowable biomass (tonne) divided by the sea surface area (hectar) inside the Norwegian baseline. The symbols indicate the evaluation of impacts of salmon lice on wild salmonids according to the new regulation system, the traffic light system (Vollset et al., 2019). Figure 1. Open in new tabDownload slide Atlantic salmon (S. salar) farming production zones in Norway in 2017, divided into 13 districts coloured by their average salmon production calculated as the allowable biomass (tonne) divided by the sea surface area (hectar) inside the Norwegian baseline. The symbols indicate the evaluation of impacts of salmon lice on wild salmonids according to the new regulation system, the traffic light system (Vollset et al., 2019). Atlantic salmon populations are threatened at the southern edge of their range and populations in the northern part of the Atlantic represent some of the largest remaining wild Atlantic salmon populations in the world (Forseth et al., 2017). These populations are increasingly overlapping with northward expansion of aquaculture towards polar regions in Norway; such poleward expansions are also occurring in Canada, Iceland, and Russia, as well as in the southern hemisphere (e.g. www.statice.is; Niklitschek et al., 2013). High latitudes that likely have had limited exposure to high infestation/infection pressure from pathogens are therefore about to encounter novel stressors. Both temperature (because of climate change) and fish farm production (because of restrictions in the south and increasing demand) are increasing. The future of wild salmon and salmon farming therefore depends on a critical question: how will wild fish in a higher latitude ecosystem respond to coming aquaculture expansion in the northern regions? Here, we argue that eco-epidemiological science is lagging behind aquaculture industry expansion in the north and that research is needed to understand and how wild salmonid populations will respond to new pathogen diversity that will inevitably come with fish farms and climate change. We exemplify this with 12 questions for research in the case of Norway, the largest farmed salmon-producing country in the world. Pathogens and epidemics Animals have co-evolved with a diversity of endemic viruses, bacteria, and parasites (collectively: pathogens) that form a complex host–pathogen trophic networks within ecosystems (Lafferty et al., 2008). Under natural conditions, pathogens pose little threat to populations as they fluctuate in a dynamic equilibrium with their host populations (Harvell, 2002). However, this balance can be disrupted when environmental conditions become stressful to populations, compromising immunity and thereby the capacity to cope with pathogens, resulting in epidemics (Miller et al., 2014). The balance can also be disturbed by the introduction of exotic pathogens or strains that trigger “virgin ground” epidemics, which spread quickly through previously unexposed and immunologically naive populations causing high host mortality and reduced abundance (Altizer et al., 2013). One important source of exotic pathogens is the transport of infected individuals into new regions (Krkošek, 2017). This transmission pathway has caused severe outbreaks of aquatic diseases in Norway such as the introduction of Gyrodactylus salaris via salmon smolts imported from Sweden (Johnsen and Jensen, 1986) and Aeromonas salmonicida subsp. salmonicida (the aetiological agent of furunculosis) in rainbow trout hosts transported from Denmark and salmon smolts from Scotland (Johnsen and Jensen, 1994). Similarly, the “ISA crisis”, wherein infectious salmon anaemia proliferated in salmonid farms in Chile, was most likely caused by import of the virus via infected salmon embryos from Norway (Vike et al., 2008). Pathogen interactions between wild and farmed fish Pathogens can spread quickly within an aquaculture facility, which can serve as a reservoir (Peeler and Murray, 2004) with potential “spillback” to wild populations (Krkošek, 2017). Consequently, high-density net-pen culture of farmed fish in areas inhabited by wild fish is viewed as one of the most pressing issues related to epidemiology in aquatic ecosystems (Lafferty et al., 2015). A wide variety of infectious disease agents are recognized among farmed Atlantic salmon in Norway, and there are spatial differences in the distribution of these pathogens (Lennox et al., 2020). Salmon lice infestations (L. salmonis), pancreas disease [salmonid alphavirus (SAV)], and amoebic gill disease (Paramoeba perurans) are among the most economically important diseases in the production of salmonids in Western Norway, whereas Parvicapsulosis (Parvicapsula pseudobranchicola), Tenacibaculosis (Tenacibaculum finnmarkense), and sea lice (C. elongatus) are more common and widespread diseases in salmon farms in Northern Norway (Hjeltnes et al., 2019). Some of these differences may reflect different environmental conditions (water temperature), host densities (salmonids, marine fish), and natural reservoirs of pathogens. In Norway, surveillance of pathogen in wild salmonids has largely been an ad hoc effort focused predominantly on a few fish pathogens (mainly viruses) such as piscine orthoreovirus-1 (PRV-1), SAV, and salmonid gill pox virus (SGPV). Monitoring has revealed generally low prevalence of viral infections in samples of wild salmonids, with only a few incidences of high prevalence. SAV is usually not detected, and PRV-1 is relatively uncommon (1–14%; Garseth et al., 2013; Taranger et al., 2015; Madhun et al., 2016, 2018; Kambestad, 2019). However, SGPV seems to be present in wild salmon spawners in many rivers, and with examples with high prevalence (Garseth et al., 2018). Phylogenetic studies of PRV-1 have revealed that exchange between wild and farmed salmon must occur relatively frequently and that PRV-1 is transported long distances (Garseth et al., 2013), perhaps even across the North Atlantic. One of the most comprehensive studies on relationships between viral and bacterial pathogens’ association on wild fish in the Atlantic and farmed salmon outside of Norway is by Wallace et al. (2017) who reviewed data on six key pathogens [Renibacterium salmoninarum, A. salmonicida, infectious pancreatic necrosis virus (IPNV), infectious salmon anaemia virus (ISAV), SAV and viral haemorrhagic septicaemia virus (VHSV)] in Scotland encompassing thousands of samples (among them salmon and trout). They found a small number of positives and only slightly elevated prevalence of IPNV in wild fish associated with fish farms, concluding that there was limited evidence for clinical disease in wild fish due to these pathogens. However, as with other sampling programmes, the fate of clinically sick fish is unknown, making it hard to disentangle the potential impact of virulent outbreaks. Whereas Atlantic salmon are well studied, pathogen dynamics among sea trout (Salmo) and Arctic charr (Salvelinus alpinus) are poorly understood. Urquhart et al. (2010) sampled and examined 300 sea trout from different coast sites in Scotland. All fish were screened for viruses and bacteria with the use of cell cultivation and bacterial-culture methods and for metazoan parasites by microscopy. No bacterial pathogens were detected, and only one fish was positive for IPNV. The most abundant parasites were sea lice (L. salmonis, C. elongatus) and various nematodes. A study on wild caught sea trout in Norway suggested that sea trout may be less susceptible to viral disease agents such as SAV (pancreas disease) and PRV-1 (heart and skeletal muscle inflammation) than Atlantic salmon (Madhun et al., 2016). A more recent study has examined infection levels of a wide range of pathogens in sea trout in Norway showed that sea trout can be infected with similar pathogens as Atlantic salmon (Kambestad, 2019). Lennox et al. (2020) screened sea trout that overwintered in freshwater for 46 pathogens in Tosenfjord and Skjerstadfjord and detected only 11, among them Ichthyobodo spp., Flavobacterium psychrophilum, and Candidatus Branchiomonas cysticola. Yet, we do not know whether such infections are benign or may cause disease outbreaks among sea trout under certain conditions (e.g. during spawning). Overall, the diversity and abundance of potential diseases impacting wild salmonids is poorly known, except perhaps for emerging research in western Canada where intensive efforts to identify pathogen-specific biomarkers have been undertaken (e.g. Miller et al., 2014; Bass et al., 2019; Mordecai et al., 2019; Teffer et al., 2019). These genomic tools reveal how pathogens are distributed spatially and how they affect different species, and how they are important contributors to performance, fitness, and fate of wild fish (Bass et al., 2019). The capacity to know which pathogens are affecting fish of different species, life stages, and life history types opens new opportunities to identify mechanisms for physiology, behaviour, and fate also in Atlantic populations of salmonids (Lennox et al., 2020). Theoretical framework Disease dynamics can be described theoretically using a variety of mathematical approaches. Strategies range from simple equations (Anderson and May, 1979), susceptible, infected, removed models, complex network analysis (Adams et al., 2012), population matrix models (Oli et al., 2006), or individual-based models with disease components (Willem et al., 2017). However, to develop a theoretical framework integrating the most important processes, disease dynamics are often explained by the pathogen reproduction number (Anderson and May, 1979). This can be represented mathematically as R0=β×N/(α+b+γ),(1) in which the rate of the pathogen reproduction number (R0) is a function of the transmission coefficient β, N is the number of hosts, α is virulence, b is the background mortality, and γ is the proportion of immune individuals. Theoretical frameworks have been applied to estimate the effect of introducing fish farms in areas with wild fish populations (Krkošek, 2010). An epidemic state emerges when the total number of hosts surpasses a threshold N0=β/(α+b+γ),(2) where N0 symbolizes the threshold number of hosts which leads to epidemic outbreaks. Perhaps the biggest challenges to relating these theoretical frameworks to applied scenarios is that (i) assumptions about the random distribution of individuals are not met, (ii) simplified allometric scaling is unrealistically coarse, and (iii) effects of stochasticity are difficult to predict. Host density will generally influence disease dynamics in salmonids. In fact, fish farms are a perfect example of an environment where infectious diseases thrive because of high host density (N) and contact rate among hosts (χ). Translating this framework to include wild fish is clearly invalid because contact rate (χ) will vary greatly between the inside and outside of the net-pen. Modelling contact rate (χ) between pathogens and wild fish is complicated, even though large progress has been made related to sea lice in recent years through the development of either complex hydrodynamic models (Sandvik et al., 2020) or spatially explicit statistical models (Kristoffersen et al., 2018). For other pathogens, χ is generally unknown, but thought to be relatively small for viral and bacterial diseases (Bakke and Harris, 1998), an argument that is often used to imply that such diseases have little impact on wild fish, even though outbreaks are frequently observed in fish farms. Perhaps the most important dynamic of disease spreading is the transmission network, in which fish farms represent nodes with edges connecting the farms to wild populations, or transfer of fish from other regions with diseases may link disease networks spreading novel diseases into new regions (Green et al., 2009). Presently, we know very little about how aquaculture affects the epidemiology of wild fish, but this knowledge must emerge to manage fish farming expansion. Another aspect that is often overlooked is that other parameters such as α (virulence) have been shown to be dramatically impacted by the presence of fish farms (Mennerat et al., 2012; McCallum et al., 2014). The maintenance of highly virulent pathogens in coastal waters throughout the year (Groner et al., 2016) may therefore have dramatic effects despite small contact rates χ. Climate change may impact disease dynamics Climate is a factor that can potentially have synergistic effects with pathogens (Harvell, 2002). Temperature is an important modulator of disease dynamics and is projected to alter pathogen diversity and the abundance of infectious disease agents (Harvell, 2002). The North Atlantic has been identified as the region of the world with the most rapid warming trends, with largely unknown effects of disease dynamics on wild fish. As an example, it is well documented that furunculosis outbreaks in wild salmon in Norwegian rivers were associated with increased temperature and low water discharge (Johnsen and Jensen, 1994). Further research on the relationship between climate and pathogenesis is needed for effective predictions about the future of disease propagation around salmon farms. Impact of temperature on disease spread can be difficult to quantify without isolating the mechanisms of disease transfer such as contact rate and infection rates (Miller et al., 2014), because these processes interact in various ways across different temperature ranges (Kirk et al., 2018). Perhaps the best example of attempting to disentangle the effect of temperature and pathogens on salmonids is the work done on the myxozoan parasite Ceratomyxa chasta on Pacific salmon in the Klamath river in Oregon (Ray et al., 2012). They demonstrated that parasite induced mortality generally increased with temperature, but that this varied a lot over time and among species, exemplifying that disease dynamics can be host, parasite, and system specific. In general, warmer temperature will increase the overall distribution and prevalence of infectious disease, although some pathogens with narrow niches may also thrive in colder water (Vike et al., 2008). Perhaps one of the few examples of the exacerbation disease load due to the spillback of parasites from farmed to wild fish in warming conditions is that of Shephard et al. (2016), who demonstrated that the link between lice infestations from farms was stronger in periods of warmer water. Similar patterns have also been observed by Vollset et al. (2018b). How will Northern populations cope with altered pathogen dynamics? Wild host populations exhibit “standing genetic variation” in immunocompetence, which is variance in immunocompetence adapted to local disease dynamics. In Canadian Atlantic salmon populations, there has been found a correlation between latitude and genetic diversity in the Major Histocompatibility Complex II (MHC II), a biomarker of immunocompetence (Dionne et al., 2007), where population more northern and colder rivers has lower genetic diversity at MHC II. Similar studies have not been conducted in Europe. On a different selection scale, northern populations have relatively brief and intense growing seasons followed by relatively harsh winter conditions during which resource acquisition and growth are poor. Selection for growing quickly during the short summer months is therefore intense. Selection on northern compared to southern populations is termed “counter gradient variation,” alluding to the phenotypic variation among populations being small owing to underlying genetic variation caused by stronger selective pressure towards rapid growth in the north (Conover and Schultz, 1995). From an eco-epidemiological perspective, we should therefore expect a trade-off in northern populations that facilitates rapid growth, which may be traded off against immunocompetence. Evidence of growth-immunocompetence trade-offs is not unequivocal from other species and immunocompetence can also be traded off against other traits (e.g. Soler et al., 2003) and should be investigated further in salmonids. Although few studies have been conducted to conclude, theory suggests that populations in the north are more susceptible to infectious diseases but less likely to contract them because cold water temperatures maintain relatively small epidemic potential for many pathogens. Fish farming is artificially enhancing the host population density, and climate change is increasing hospitability and reproductive potential of pathogenic species, a combination that we propose will lead to novel epidemic outbreaks in the north. The consequences for wild salmonids are unknown. Twelve emerging research questions In the following section, we describe specific research questions that need to be answered to tackle the imminent change that is occurring in the northernmost areas of the distribution of salmonids. The questions are arranged in order, beginning at individual scales and progressing to population and species scales. For each question, we present a testable hypothesis that should be investigated. For a quick overview, we have summarized key takeaways with our expert opinion about prioritization (1–3), the perceived knowledge level, and relevant publications for each question (Table 1). Table 1. Quick overview of pressing research questions with associated scale (individual, population, species), knowledge level (* = well studied, ** = well documented for case studies, *** = data exists for some case studies, **** = data generally lacking), and prioritization (1–3, based on expert opinion from the group. Number . Research question . Scale . Knowledge level . Prioritization . Relevance . Important publications . 1 Do pathogens prevalent in fish farming affect the growth, survival, and fitness of wild salmonids and is this impacted by temperature? Individual ** 1 Aquaculture management Miller et al. (2014,) andVollset et al. (2016) 2 Is individual fate linked to up- or down-regulation of stress and immune-related genes? Individual ** 3 Fisheries management Jeffries et al. (2014,) andMiller et al. (2017) 3 Is the richness and abundance of fish farms associated pathogens among wild salmonids associated with migration and behavioural strategies? Individual *** 2 Aquaculture management Birkeland and Jakobsen (1997) and Lennox et al. (2020) 4 Are transitions between freshwater and saltwater critical for disease development? Individual *** 3 Fisheries management Moles (1997) and Teffer et al. (2018) 5 Is the richness and abundance of pathogens found in wild salmonids associated with the density of farmed fish and latitude? Population *** 1 Aquaculture management Teffer et al. (2020) 6 Does a latitudinal gradient in immunocompetence exist and what are the consequences of fish farming? Population *** 1 Aquaculture management Dionne et al. (2007) 7 How susceptible are different salmonid species to infestation pressure from aquaculture? Population ** 2 Aquaculture management Jensen et al. (2018) 8 Do different predator communities in northern and southern regions affect the survival of diseased fish? Population **** 2 Fisheries management Schemske et al. (2009) and Friedland et al. (2017) 9 Can disease dynamics of wild salmonids be impacted by changes in recruitment and migratory behaviour of non-salmonid fish mediated through climate change? Population **** 3 Fisheries management Imsland et al. (2019) 10 Will invasive species interact with aquaculture and thereby spread disease to wild salmonids in the high north? Species *** 2 Invasive species management Sandlund et al. (2019) and Fjær (2019) 11 Does stocking affect prevalence or virulence of pathogens? Species *** 1 Fisheries management Garseth et al. (2013) 12 Does farmed fish act as pathogen vectors and does genetic introgression from farmed fish impact pathogen load? Species **** 1 Fisheries management Madhun et al. (2015) Number . Research question . Scale . Knowledge level . Prioritization . Relevance . Important publications . 1 Do pathogens prevalent in fish farming affect the growth, survival, and fitness of wild salmonids and is this impacted by temperature? Individual ** 1 Aquaculture management Miller et al. (2014,) andVollset et al. (2016) 2 Is individual fate linked to up- or down-regulation of stress and immune-related genes? Individual ** 3 Fisheries management Jeffries et al. (2014,) andMiller et al. (2017) 3 Is the richness and abundance of fish farms associated pathogens among wild salmonids associated with migration and behavioural strategies? Individual *** 2 Aquaculture management Birkeland and Jakobsen (1997) and Lennox et al. (2020) 4 Are transitions between freshwater and saltwater critical for disease development? Individual *** 3 Fisheries management Moles (1997) and Teffer et al. (2018) 5 Is the richness and abundance of pathogens found in wild salmonids associated with the density of farmed fish and latitude? Population *** 1 Aquaculture management Teffer et al. (2020) 6 Does a latitudinal gradient in immunocompetence exist and what are the consequences of fish farming? Population *** 1 Aquaculture management Dionne et al. (2007) 7 How susceptible are different salmonid species to infestation pressure from aquaculture? Population ** 2 Aquaculture management Jensen et al. (2018) 8 Do different predator communities in northern and southern regions affect the survival of diseased fish? Population **** 2 Fisheries management Schemske et al. (2009) and Friedland et al. (2017) 9 Can disease dynamics of wild salmonids be impacted by changes in recruitment and migratory behaviour of non-salmonid fish mediated through climate change? Population **** 3 Fisheries management Imsland et al. (2019) 10 Will invasive species interact with aquaculture and thereby spread disease to wild salmonids in the high north? Species *** 2 Invasive species management Sandlund et al. (2019) and Fjær (2019) 11 Does stocking affect prevalence or virulence of pathogens? Species *** 1 Fisheries management Garseth et al. (2013) 12 Does farmed fish act as pathogen vectors and does genetic introgression from farmed fish impact pathogen load? Species **** 1 Fisheries management Madhun et al. (2015) We emphasize that we have placed high prioritization on research question associated with anthropogenic activities that can be mitigated), relevance (defined as most relevant associated management organization), and important publications. Open in new tab Table 1. Quick overview of pressing research questions with associated scale (individual, population, species), knowledge level (* = well studied, ** = well documented for case studies, *** = data exists for some case studies, **** = data generally lacking), and prioritization (1–3, based on expert opinion from the group. Number . Research question . Scale . Knowledge level . Prioritization . Relevance . Important publications . 1 Do pathogens prevalent in fish farming affect the growth, survival, and fitness of wild salmonids and is this impacted by temperature? Individual ** 1 Aquaculture management Miller et al. (2014,) andVollset et al. (2016) 2 Is individual fate linked to up- or down-regulation of stress and immune-related genes? Individual ** 3 Fisheries management Jeffries et al. (2014,) andMiller et al. (2017) 3 Is the richness and abundance of fish farms associated pathogens among wild salmonids associated with migration and behavioural strategies? Individual *** 2 Aquaculture management Birkeland and Jakobsen (1997) and Lennox et al. (2020) 4 Are transitions between freshwater and saltwater critical for disease development? Individual *** 3 Fisheries management Moles (1997) and Teffer et al. (2018) 5 Is the richness and abundance of pathogens found in wild salmonids associated with the density of farmed fish and latitude? Population *** 1 Aquaculture management Teffer et al. (2020) 6 Does a latitudinal gradient in immunocompetence exist and what are the consequences of fish farming? Population *** 1 Aquaculture management Dionne et al. (2007) 7 How susceptible are different salmonid species to infestation pressure from aquaculture? Population ** 2 Aquaculture management Jensen et al. (2018) 8 Do different predator communities in northern and southern regions affect the survival of diseased fish? Population **** 2 Fisheries management Schemske et al. (2009) and Friedland et al. (2017) 9 Can disease dynamics of wild salmonids be impacted by changes in recruitment and migratory behaviour of non-salmonid fish mediated through climate change? Population **** 3 Fisheries management Imsland et al. (2019) 10 Will invasive species interact with aquaculture and thereby spread disease to wild salmonids in the high north? Species *** 2 Invasive species management Sandlund et al. (2019) and Fjær (2019) 11 Does stocking affect prevalence or virulence of pathogens? Species *** 1 Fisheries management Garseth et al. (2013) 12 Does farmed fish act as pathogen vectors and does genetic introgression from farmed fish impact pathogen load? Species **** 1 Fisheries management Madhun et al. (2015) Number . Research question . Scale . Knowledge level . Prioritization . Relevance . Important publications . 1 Do pathogens prevalent in fish farming affect the growth, survival, and fitness of wild salmonids and is this impacted by temperature? Individual ** 1 Aquaculture management Miller et al. (2014,) andVollset et al. (2016) 2 Is individual fate linked to up- or down-regulation of stress and immune-related genes? Individual ** 3 Fisheries management Jeffries et al. (2014,) andMiller et al. (2017) 3 Is the richness and abundance of fish farms associated pathogens among wild salmonids associated with migration and behavioural strategies? Individual *** 2 Aquaculture management Birkeland and Jakobsen (1997) and Lennox et al. (2020) 4 Are transitions between freshwater and saltwater critical for disease development? Individual *** 3 Fisheries management Moles (1997) and Teffer et al. (2018) 5 Is the richness and abundance of pathogens found in wild salmonids associated with the density of farmed fish and latitude? Population *** 1 Aquaculture management Teffer et al. (2020) 6 Does a latitudinal gradient in immunocompetence exist and what are the consequences of fish farming? Population *** 1 Aquaculture management Dionne et al. (2007) 7 How susceptible are different salmonid species to infestation pressure from aquaculture? Population ** 2 Aquaculture management Jensen et al. (2018) 8 Do different predator communities in northern and southern regions affect the survival of diseased fish? Population **** 2 Fisheries management Schemske et al. (2009) and Friedland et al. (2017) 9 Can disease dynamics of wild salmonids be impacted by changes in recruitment and migratory behaviour of non-salmonid fish mediated through climate change? Population **** 3 Fisheries management Imsland et al. (2019) 10 Will invasive species interact with aquaculture and thereby spread disease to wild salmonids in the high north? Species *** 2 Invasive species management Sandlund et al. (2019) and Fjær (2019) 11 Does stocking affect prevalence or virulence of pathogens? Species *** 1 Fisheries management Garseth et al. (2013) 12 Does farmed fish act as pathogen vectors and does genetic introgression from farmed fish impact pathogen load? Species **** 1 Fisheries management Madhun et al. (2015) We emphasize that we have placed high prioritization on research question associated with anthropogenic activities that can be mitigated), relevance (defined as most relevant associated management organization), and important publications. Open in new tab Do pathogens prevalent in fish farming affect the growth, survival, and fitness of wild salmonids and is this impacted by temperature? Studies regarding pathogen impacts on growth and survival of wild salmonids have been limited to a few key pathogens. Substantially more work has been done within the context of fish farming (Kibenge et al., 2004), but these are not generally applicable to wild fish settings. Studies on sea lice have spearheaded this research with randomized control trials using either treatment or infestation methods to disentangle how wild fish respond to infestations (Vollset et al., 2016). These methods are available and should be utilized to study a range of pathogens at both juvenile and adult stages of wild salmonids. Pathogens have variable lethal and sublethal impacts on host fitness, which are likely to vary to some extent with temperature. Negative effects can be estimated directly by measuring the energetic costs of pathogens using bioenergetics experiments (Hvas et al., 2017). An animal’s oxygen demand is regulated by controlling, limiting, masking, lethal, and directive factors (Fry, 1947), which includes temperature (controlling) and disease (masking). Pathogenicity for some agents can also be a function of temperature (reviewed in Miller et al., 2014). Disease is a natural ecological process and one that broadly regulates animal populations and communities (Dobson and Hudson, 1986), but the equilibrium can be affected by disturbances such as altered temperature or increased virulence or increased host densities (either naturally or by introducing farmed fish in the ecosystem). Research on Pacific salmonids has affirmed the predictive potential that pathogens have on the performance and fate of both smolt (Jeffries et al., 2014) and adult migrants (Teffer et al., 2018; Bass et al., 2019). We hypothesize that, as temperatures warm in the northern waters occupied by salmonids, stress responses may reduce immune capacities and enhance potential for the replication of pathogens and the likelihood of disease related to pathogens from farmed fish. Is individual fate linked to up- or down-regulation of stress and immune-related genes? Migratory salmon are exposed to a range of environmental and anthropogenic stressors that can interact in a cumulative or synergistic relationship with infection to affect disease outcomes (Crain et al., 2008; Altizer et al., 2011, 2013). These impacts may be especially pronounced in a warming climate (Crain et al., 2008). For salmon, environmental stressors can include ocean and freshwater warming, shifts in oxygen saturation, salinity, and harmful algal blooms, among others. We know that many of these factors can directly impact the survival of caged fish (Haigh and Esenkulova, 2014), and if exposed, these environmental stressors may be highly impactful on wild salmon; particularly in synergy with pathogens. The answers to these questions may now be tractable given the availability of new molecular technologies by directly studying stress and immune-related genes (Miller et al., 2017). We hypothesize that measurable gene expressions in individual fish can predict likelihood of survival and reproduction in various salmonids. If successful, this will form a robust tool to study the impacts of both climate and fish farming on wild fish in situ. Is the richness and abundance of fish farms associated pathogens among wild salmonids associated with migration and behavioural strategies? Life history and physiological traits can vary substantially within populations (Ricklefs and Wikelski, 2002). Such traits are often manifested in behavioural differences and dietary and habitat selections, which act to modify the encounter with pathogens in different habitats. Migrations of sea trout and anadromous Arctic charr are plastic and a threshold-dependent response to growth that may be modulated by genetics and environment (Klemetsen et al., 2003). Within sea trout, it has been observed that females and larger individuals in a poor pre-migratory nutritional state often are more exploratory and migrate further away from their home river during the marine feeding migration (S. Eldøy unpublished data). These migratory behaviours specifically modulate the exposure rate of animals to disease (Altizer et al., 2011). Migration is both phenotypically plastic (Olsson et al., 2006) and a partially genetic trait that may respond to selection (Ferguson et al., 2019). Among salmonid fishes, it has been repeatedly observed that parasitism from ectoparasitic sea lice affects the rate of migration by sea trout to exploit the marine environment (Birkeland and Jakobsen, 1997). There is clear potential for interaction between individual phenotypes and pathogens, with pathogens altering the migratory tendencies of some populations experiencing high burdens. Lennox et al. (2020) tracked sea trout in northern Norway and revealed that infection with freshwater pathogens was associated with prolonged freshwater residency by trout that had previously been to sea. However, no differences were observed with respect to marine area use. However, studies on impacts of several marine pathogens on sea trout and salmon remain to be explored. We hypothesize that pathogens other than salmon lice from fish farms impact migratory patterns of salmonids and that individuals with life-history and behavioural strategies that expose these individuals to fish farms will have high pathogen loads. Are anadromous salmonids particularly vulnerable to diseases during transitions between freshwater and saltwater? The transition between freshwater and saltwater environments is one of the most critical periods for anadromous salmonids. Saltwater yields an osmoregulatory challenge and changes to the gill and renal function are needed to maintain osmoregulation, which are necessary for transitioning to the ocean (described in Houde et al., 2019a). As they transition into the marine environment, salmon are exposed to a new array of pathogens, some that may infect the very tissues (gill and kidney) critical for saltwater adaptation (Miller et al., 2014). Research on Pacific salmon in North America has demonstrated that the early marine period for out-migrating smolts is the key determinant of year-class strength (Friedland et al., 2003). Both for smolts and for post-spawned veteran migrants, sea entry coincides with starvation. Survival of smolts released from enhancement hatcheries and fish cultured in salmon net pens can be associated with physiological condition at the smolt life stage during the transition from freshwater to seawater (Chittenden et al., 2008), findings supported by tracking studies of wild salmonids (Jeffries et al., 2014). Moles (1997) revealed that the transition can enhance susceptibility to disease; coho salmon (Oncorhynchus kisutch) with bacterial kidney disease (BKD) had greater mortality when transferred to sea water than controls, suggesting that the transition modulated the virulence of BKD. High infective burdens gained through exposure to new pathogens during transition from marine to freshwater have also been shown to reduce the resiliency of sockeye salmon thermal and handling stress (Teffer, 2018). We hypothesize that a stressful transition to saltwater is a general physiological bottleneck for all salmonids and that resilience to environmental stress during salinity transitions is highly impacted by the infective burden densities encountered within the new salinity environment. As a result, anthropogenic activities that increase concentrations of pathogens, such as open net farming, may be most detrimental to migratory salmon undergoing salinity transitions, especially when other environmental stressors are present. Is the richness and abundance of pathogens found in wild salmonids associated with the density of farmed fish and latitude? It is unknown how marine pathogens on wild salmonids are distributed along latitudinal gradients and how the presence of farmed fish affects this pattern. Surveillance of pathogens other than sea lice on wild salmonids in the North Atlantic has been scarce. In Norway, opportunistic sampling has suggested that viral pathogens and diseases are rarely observed in a few populations of migratory salmon and sea trout that have been surveyed (Madhun et al., 2015; Lennox et al., 2020). Limited viral and bacterial prevalence in migratory Pacific salmon compared to farmed salmon is also observed in North America (Tucker et al., 2018; Teffer et al., 2020; Laurin et al., 2019). It is important to recognize that low apparent prevalence of acute viral agents could be due to the rapid loss of fish suffering from acute disease, owing to predation, and an inability to locate and sample dying migratory salmon (i.e. survivor bias). We hypothesize that the low pathogen load observed in wild fish may be attributed to survivor bias because sick individuals are rapidly culled by predators and are not sampled. More extensive structured sampling is needed to fully understand how common such outbreaks are. Does a latitudinal gradient in immunocompetence of salmonids exist? Variation in the immunocompetence of salmonids along anthropogenic and climatic gradients is unknown. Earlier studies have shown that the standing genetic diversity in immunocompetence in wild Atlantic salmon populations is lower in northern compared to southern populations in the northwest Atlantic, most likely reflecting adaptation to local pathogen diversity, which are expected to be greater at warmer temperatures (Dionne et al., 2007). This raises the question of how tolerant northern salmonids populations are to changes in disease dynamics, and how they will respond to presence of aquaculture and subsequent increase in host density. We hypothesize that wild salmon populations at northern latitudes will have relaxed selection on the MHC. This can reduce their ability to immunologically respond to new infective pathogens which they will be exposed to as farming moves northwards and temperature continue to rise. How susceptible are different salmonid species to infestation pressure from aquaculture? Three of the anadromous salmonid species that are native to Europe, Atlantic salmon (Salmo salar), sea trout (Salmo trutta), and Arctic charr (S. alpinus) are all exposed to varying degrees of fish farming in Norwegian fjords. Sea trout and Arctic charr are considered to have the highest potential exposure because they only migrate into coastal areas and fjords during their sea sojourn, which is the same habitat exploited for fish farming (Jensen et al., 2018). Atlantic salmon, however, transit the fjords to the open ocean where their feeding habitats lie beyond the areas exploited for aquaculture. Consequently, salmon are exposed during the early marine migration of smolts and late marine migration of adults. Arctic charr are anadromous only in the north; therefore, their realized level of exposure is low compared to salmon and trout. As aquaculture pushes northwards, many populations of Arctic charr will become exposed to aquaculture for the first time and the species will in general be exposed to a previously unforeseen intensity of aquaculture. Studies of comparative behaviour and physiology among these species are therefore a necessary research avenue to determine which species are more and less susceptible to pathogens prevalent in fish farming. Comparative studies (e.g. Jensen et al., 2018) have advantages in terms of revealing how bacteria, viruses, and parasites infect the different species given that virulence can be expected to differ among species. Moreover, the three species have different water temperature preferences and warming in different parts of their distribution range can be predicted to affect cold water charr more than salmon and trout (Elliott and Elliott, 2010). Comparisons of habitat use, phenotypic plasticity, and immunological capabilities of the three species will yield new information about the risks imposed upon northern salmonids due to expanding fish farming in northern regions. We hypothesize that susceptibility of pathogens due to spill over from fish farms differ among salmonids species because of evolutionary history and life history strategy. Is the survival of infected fish affected by predators differently between Northern and Southern predator communities? Fish that are physiologically compromised due to pathogens will have an increased likelihood of being captured by animals either because of reduced locomotor capacity or because of impaired cognitive function (Mesa et al., 1994; Miller et al., 2014). Such mortality effects will not only depend on the physiological competence of the diseased fish, but also the predator community and functional and numerical responses of the predators. Biotic interactions shift along latitudinal gradients (Schemske et al., 2009). Predator communities that can prey on salmonids change dramatically along latitudinal gradients. Typical predators, such as mergansers (Mergus spp.), cod (Gadus morhua), and saithe (Pollachius virens) that predate young salmon and trout and grey seals (Halichoerus grypus) and orcas (Orcinus orca) that eat adults, have distributions along the North Atlantic that overlap with salmonids. Recruitment failure in populations of salmon in the Baltic has been linked to changes in spatial habitat use of potential predators (Friedland et al., 2017), and similar variation in predator fields along latitudinal gradients is also likely to occur. We hypothesize that predator communities during early life history for salmon can vary dramatically between salmon populations (both along latitudinal gradients and other gradients) and that this can influence mortality related to compromised physiology due to pathogens. Can disease dynamics of wild salmonids be impacted by changes in recruitment and migratory behaviour of non-salmonid fish mediated through climate change? Along the coast of Norway there are massive migrations of marine fish, e.g. the northeast Atlantic stock of cod spawning migrations from the Barents Sea down the coast of Norway, the massive migrations of herring (Clupea harengus) from its feeding grounds in the Norwegian Sea to spawning along the coast, and the northern mackerel (Scomber scombrus) summer feeding migration into the North Sea. These have been shown to be directly impacted by climate change (e.g. Sundby and Nakken, 2008). Non-salmonid-specific infections such as Ichtyophonus and Caligus spp. will be strongly impacted by the changes to such populations. In recent years, Caligus elongatus has become a more severe problem for salmon farms in northern counties (Troms and Finnmark) compared to the rest of Norway, most likely because of larger non-salmonid wild fish stocks in these regions (Imsland et al., 2019). We hypothesize that non-salmonid fish populations can alter and determine the epidemiological dynamic of non-salmonid-specific pathogens for both wild and farmed salmonids and serve as an important reservoir for pathogens during seasonal migrations. Moreover, interaction between high-density fish farms and large non-salmonid populations may be potential sources for horizontal interspecific transmissions, potentially creating novel future disease outbreaks, impacting both wild and farmed salmon. Will invasive species interact with aquaculture and thereby spread disease to wild salmonids in the high North? Warming climate will potentially make the freshwater habitats in the high north suitable for new species, which can bring new diseases. Fish communities in northern rivers are already shifting (Svenning et al., 2016) including arrival of new colonizers. Pink salmon (Oncorhynchus gorbuscha) was introduced to the Kola Peninsula in 1956 (Dushkina, 1994). Pink salmon catches of odd year-class populations have increased dramatically in recent years and might present a risk of transmitting pathogens into salmon rivers (Sandlund et al., 2019). The limited studies that have been conducted so far have demonstrated PRV-1 in Karpelva in pink salmon (Å. H. Garseth et al., pers. comm.), whereas no infectious diseases important to salmon farming were observed among pink salmon collected in southern Norway (Fjær, 2019). We hypothesize that invasive species such as pink salmon may be an important potential disease vector between fish farms, and between farmed to wild fish increasing the spread of pathogens through the aquatic ecosystem. Does stocking affect the prevalence of pathogens? About 60 populations of Atlantic salmon are stocked annually in Norway. In addition to concerns regarding the effect this might have on the genetic integrity and genetic variation of natural populations (Laikre et al., 2010; Christie et al., 2012b), there is also a concern for functional genetic changes from epigenetic changes and domestication selection (Christie et al., 2012a, 2016; Le Luyer et al., 2017). One study has demonstrated that salmon with a hatchery background has a higher PRV-1 prevalence than wild salmon (Garseth et al., 2013). Studies in the Pacific Northwest have shown that wild fish leaving freshwater often carry more myxozoan parasites with alternate invertebrate hosts than do hatchery fish, but infection patterns for marine agents are fairly similar and reflect the environments fish are sampled from (Thakur et al., 2018; Nekouei et al., 2019). However, differences in early marine habitat use may result in higher infective burdens in hatchery fish in the first month of ocean residence (Thakur et al., 2018), possibly contributing to lower observed survival rates. We hypothesize that stocking might lead to changes in the capability of the fish to fight pathogens because fish in hatcheries may go through very different bottleneck selection through the hatchery process. Does escaped farmed fish act as pathogen vectors and does genetic introgression from farmed fish impact pathogen load? Genetic introgression of escaped farmed Atlantic salmon in wild salmon populations is widespread in Norway and is quantified for >225 wild salmon populations (Diserud et al., 2019) using molecular genetic markers (Karlsson et al., 2011, 2014). Atlantic salmon and sea trout are subdivided into more or less genetically isolated populations, and there exist genotypic data from neutral markers (single-nucleotide polymorphisms) for both species that can be used as a contrast to explore a potential local genetic adaptation in genes subjected to contemporary selection relevant to the immune system. It is mandatory to conduct genetic tests of all brood-salmon used for stocking to exclude individuals with background from fish farms in Norway since 2014 (Karlsson et al., 2016). Consequently, all stocked salmon in Norway are genetically “tagged” by the existing genetic profile of their parents. A fish can thereby with nearly 100% certainty be assigned as either stocked or naturally produced, allowing inference of possible effects of domestication selection or epigenetic effects on pathogen resistance from being hatchery produced. Depending on the selection protocols in breeding programmes, farmed fish can be either more or less susceptible to pathogens changing the immunocompetence of the population when interbreeding, or having a selective advantage in some conditions. Furthermore, escaped farmed fish may serve directly as vectors for pathogens bringing pathogens into rivers where contact rate is high (Madhun et al., 2015), or through vertical transmission when successfully interbreeding with wild fish (Colquhoun et al., 2018). We hypothesize that populations affected by escaped farmed fish and genetic introgression have different immunocompetence, and pathogen diversity. Furthermore, the exposure to pathogens could drive selection for or against farmed genes as a function of the local pathogen diversity. How do we address these research questions? Epidemiological studies Epidemiological studies describe the risk and pattern of diseases within a population and include knowledge of hosts, pathogens, and environment (Snieszko, 1974). Aetiology and pathogenesis of infectious diseases in fish farms can easily be monitored by observations of behaviour, feed consumption, and clinical signs, measuring growth and condition factor or increased mortality rate. Samples of wild salmonids to describe the prevalence of infections should include both healthy fish and fish with disease. This is often difficult because sick fish are likely to die or to be rapidly predated due to reduced swimming ability or abnormal behaviour (McVicar, 1997). Detecting diseases among wild fish and measuring the impact of such diseases in situ are therefore difficult, and in most cases impossible due to survivor biases. In addition, lethal sampling of healthy individuals of high conservation value may be problematic, calling for non-lethal testing methods. Moreover, targeted surveillance may in some cases distort prevalence, making it hard to draw inferences based on the samples. Screening of wild caught fish can reveal health status based on levels of infections among healthy carrier fish that may be asymptomatic. However, it is important to acknowledge that screening of pathogens on individuals in the wild will not give the same insights into the pathogenesis of diseases as is possible in fish farms. A possible avenue for insight into the epidemiology of wild fish is therefore to better utilize molecular signatures of developing disease states (Miller et al., 2017), which may allow us to sample fish that do not necessarily exhibit symptoms of disease but are in the early stages of pathogenesis (See molecular techniques). Opportunity to gain insight into the effects of pathogens on wild fish usually stems from rare epidemics. For example, G. salaris infections followed by saprolegniasis in rivers, furunculosis outbreak in the spawning period, or heavy infections of sea lice in fjords (Heggberget et al., 1993; Bakke and Harris, 1998; Vollset et al., 2018a, b) can sometimes be observed if the samples are taken during the epidemic. A problem with studying such outbreaks is that secondary infection such as saprolegniasis may be more apparent than the primary cause, increasing the chance of making more wrong conclusions about causality between the pathogen and impacts. Also, it is difficult to know a priori when such outbreaks may occur, but they are generally associated with a combination of the pathogen being prevalent and the fish encountering suboptimal environmental conditions (McLeay and Gordon, 1977; Barton and Iwama, 1991; Pickering, 1992). In contrast to farmed salmonids, wild fish may avoid areas with suboptimal environment and pathogens by their behaviour. However, crowding among wild fish is common in river systems during spawning and severe outbreaks of infectious diseases may occur if high numbers of fish are trapped in shallow water in periods with reduced water flow in the river (Schisler et al., 1999). Therefore, taking samples of fish that we can follow using telemetry (see below) can reveal if such stressing periods will increase mortality or decrease measures of fitness. Telemetry Individual behaviour reflects the internal state of the animal; therefore, behaviour can be used as an indicator of physiological status (Cooke et al., 2014). Harrison et al. (2015) showed how movement of individual fish reflects their physiological phenotypes in a consistent and repeatable way. On shorter timescales, several papers have outlined how stress, such as that incurred after interactions with fisheries, affects movement patterns of salmonids (e.g. Raby et al., 2015; Twardek et al., 2019). In semelparous adult Pacific salmon, indices of stress and/or disease have also been related to faster movement towards spawning grounds (Drenner et al., 2018) but reduced reproductive success (Miller et al., 2011). The ecological consequences of pathogens on individual fish can therefore be illuminated by observing the movement and relating observed patterns of migration, dispersal, or station keeping to the pathogen load of the animal (e.g. Lennox et al., 2020). Observing movement of aquatic animals is challenging. Novel telemetry methods has improved our ability to gather positional data from individuals as they move across time and at different stages of their ontogenetic development (Hussey et al., 2015). Arrays of acoustic telemetry receivers can be arranged in areas expected to be occupied by the study species so that detections of tagged animals on the receivers can be used to reconstruct movement paths or calculate usage patterns of key areas. For example, observations of tagged fish on acoustic telemetry receivers can be used to calculate home range sizes, movement corridors, and migratory timing. Telemetry is increasingly used for hypothesis testing, using the capture event as an opportunity to take measurements and samples from the individual that can later be related to the movement observed following release (Lennox et al., 2017). Several studies have now taken the opportunity to use non-lethal gill biopsy samples to describe the individual’s pathogen community and apply this to test hypotheses about the movements observed after release. For example, pathogens hasten the rate of upriver migration by chinook salmon (Oncorhynchus tshy) returning to spawn (Teffer et al., 2018; Bass et al., 2019) and infections of sockeye salmon smolts leaving nursery habitats for the sea decrease probability of survival (Jeffries et al., 2014). Telemetry was also applied by Lennox et al. (2020) to characterize the marine behaviour and survival to spawn of sea trout in two northern Norwegian fjords as a function of the pathogen community. Together, these studies exhibit the potential for using electronic tagging as a tool to observe fish and test hypotheses regarding the impacts of the pathogen community on behaviour and survival. Molecular techniques Development of new high-throughput molecular techniques now permits efficient identification and quantification of 47 multiple pathogens at once from tissue samples (Miller et al., 2014, 2016). This approach has been broadly applied (to over 28 000 fish) to characterize profiles of infectious agents suspected or known to cause disease in salmon worldwide in both wild (e.g. Tucker et al., 2018; Nekouei et al., 2019) and farmed(Laurin et al., 2019) salmon. It has also been applied non-lethally in tracking and holding studies to identify pathogens associated with fate (e.g. Jeffries et al., 2014; Teffer et al., 2018, 2019) and to assess patterns of co-infection in disease outbreaks (Di Cicco et al., 2017, Di Cicco et al., 2018). Biomarkers are expressed genes that can objectively be identified with molecular tools and validated as indicators of clinical endpoints (Strimbu and Tavel, 2010). Identification of genetic markers that can identify viral disease development state of salmonids (Miller et al., 2017) has greatly improved our ability to identify which phase of the disease development individuals are in (e.g. Di Cicco et al., 2018), making it possible to identify living and seemingly healthy fish that may develop pathogenesis from infections. This method, originally developed based on the approaches used to resolve and apply molecular markers to differentiate respiratory viral versus bacterial diseases in humans (Andres-Terre et al., 2015), has also led to the discovery of several novel viruses in salmon (Mordecai et al., 2019, 2020). Using a similar curated biomarker approach, a new salmon “Fit-Chip” technology has recently been developed that contains a series of curated biomarker panels that, when co-expressed, can signal the presence of different stressor and disease states in individual fish (e.g. Houde et al., 2019b). Co-expressed biomarker panels have been developed to recognize specific environmental stressors (e.g. hypoxia, thermal, osmotic; see Akbarzadeh et al., 2018; Houde et al., 2019b) and disease states [viral disease (Miller et al., 2017), inflammation, humoral immunity, immunosuppression]. Biomarker panels have also been developed to identify pre-moribund fish with a high probability of imminent mortality [natural death within 72 hr; developed from Jeffries et al. (2012)], and a mortality-related signature that has repeatedly been associated with shifts in migratory behaviour (Drenner et al., 2018) and mortality across longer timeframes (Miller et al., 2011). This technology has been validated for application on cDNA from non-lethal gill biopsies, which can be taken from live fish. Scientists are starting to apply salmon these methods to identify the health and condition of individual fish, to identify correlations between environmental and animal health, to explore the complex synergies between stress and disease, to identify geographic regions along the coast where salmon are most compromised, and to test hypotheses about how salmon health will contribute to behaviour, reproduction, or survival. Significance Studies on pathogen dynamics of salmonid populations are emerging and revealing the complex role that these species have in the life cycle of salmon, trout, and charr. Much of the focus has been placed on ectoparasitic sea lice, but molecular techniques and epidemiological studies have begun to reveal the role of a broader suite of infectious agents. With increasing availability and capacity for the use of high-throughput PCR and telemetry techniques, there is great potential for new knowledge to be generated about the influence of pathogens on salmonids scaling from individuals to populations and entire ecological communities. Shifting political will to increase the production of fish farms in northern regions raises questions about what the future might hold for wild salmonid populations as the climate in these regions change more rapidly than that in other parts of the world. We emphasize the importance of considering uncertainties with respect to pathogen dynamics when considering new directives for aquaculture in poorly studied regions of the north until the key research questions are fully addressed and appropriate plans have been implemented to minimize the potential for harm to vulnerable wild salmonid populations. Acknowledgements The idea of this manuscript came from a round table dialogue with everyone working in the research group LFI at NORCE. The authors thank Erlend Mjelde Hanssen for commenting on the early version of the manuscript. This study was funded by the Norwegian Research Council through the programme MARINFORSK (Grant No. 303301). Data availability statement No new data were generated or analysed in support of this research. References Adams T. Black K. MacIntyre C. MacIntyre I. Dean R. 2012 . Connectivity modelling and network analysis of sea lice infection in Loch Fyne, west coast of Scotland . Aquaculture Environment Interactions , 3 : 51 – 63 . Google Scholar Crossref Search ADS WorldCat Akbarzadeh A. Günther O. P. Houde A. L. Li S. Ming T. J. Jeffries K. M. Hinch S. G. , et al. 2018 . Developing specific molecular biomarkers for thermal stress in salmonids . BMC Genomics , 19 : 749 . Google Scholar Crossref Search ADS PubMed WorldCat Altizer S. Bartel R. Han B. A. 2011 . Animal migration and infectious disease risk . Science , 331 : 296 – 302 . Google Scholar Crossref Search ADS PubMed WorldCat Altizer S. Ostfeld R. S. Johnson P. T. J. Kutz S. Harvell C. D. 2013 . Climate change and infectious diseases: from evidence to a predictive framework . Science , 341 : 514 – 519 . Google Scholar Crossref Search ADS PubMed WorldCat Anderson R. M. May R. M. 1979 . Population biology of infectious diseases: part I . Nature , 280 : 361 – 367 . Google Scholar Crossref Search ADS PubMed WorldCat Andres-Terre M. McGuire H. M. Pouliot Y. Bongen E. Sweeney T. E. Tato C. M. Khatri P. 2015 . Integrated, multi-cohort analysis identifies conserved transcriptional signatures across multiple respiratory viruses . Immunity , 43 : 1199 – 1211 . Google Scholar Crossref Search ADS PubMed WorldCat Bakke T. A. Harris P. D. 1998 . Diseases and parasites in wild Atlantic salmon (Salmo salar) populations . Canadian Journal of the Fisheries and Aquatic Sciences , 55 : 247 – 266 . Google Scholar Crossref Search ADS WorldCat Barton B. A. Iwama G. K. 1991 . Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids . Annual Review of Fish Diseases , 1 : 3 – 26 . Google Scholar Crossref Search ADS WorldCat Bass A. L. Hinch S. G. Teffer A. K. Patterson D. A. Miller K. M. 2019 . Fisheries capture and infectious agents are associated with travel rate and survival of Chinook salmon during spawning migration . Fisheries Research , 209 : 156 – 166 . Google Scholar Crossref Search ADS WorldCat Birkeland K. Jakobsen P. J. 1997 . Salmon lice, Lepeophtheirus salmonis, infestation as a causal agent of premature return to rivers and estuaries by sea trout, Salmo trutta, juveniles . Environmental Biology of Fishes , 49 : 129 – 137 . Google Scholar Crossref Search ADS WorldCat Chittenden C. M. Sura S. Butterworth K. G. Cubitt K. F. Plantalech Manel-la N. Balfry S. Økland F. , et al. 2008 . Riverine, estuarine and marine migratory behaviour and physiology of wild and hatchery‐reared coho salmon Oncorhynchus kisutch (Walbaum) smolts descending the Campbell River, BC, Canada . Journal of Fish Biology , 72 : 614 – 628 . Google Scholar Crossref Search ADS WorldCat Christie M. R. Marine M. L. Fox S. E. French R. A. Blouin M. S. 2016 . A single generation of domestication heritably alters the expression of hundreds of genes . Nature Communications , 7 : 1 – 6 . Google Scholar Crossref Search ADS WorldCat Christie M. R. Marine M. L. French R. A. Blouin M. S. 2012 a. Genetic adaptation to captivity can occur in a single generation . Proceedings of the National Academy of Sciences of the United States of America , 109 : 238 – 242 . Google Scholar Crossref Search ADS PubMed WorldCat Christie M. R. Marine M. L. French R. A. Waples R. S. Blouin M. S. 2012 b. Effective size of a wild salmonid population is greatly reduced by hatchery supplementation . Heredity , 109 : 254 – 260 . Google Scholar Crossref Search ADS PubMed WorldCat Colquhoun D. Garseth Å.-H. Gudding R. Helgesen K. Holst-Jensen A. Lillehaug A. Løkka G. Mo T. A. Qviller L. Skaar I. 2018 . Smitte mellom oppdrettsfisk og villfisk: Kunnskapsstatus og risikovurdering. Veterinærinstituttet, Rapport-12-2018. Norwegian with English Abstract. Conover D. O. Schultz E. T. 1995 . Phenotypic similarity and the evolutionary significance of countergradient variation . Trends in Ecology & Evolution , 10 : 248 – 252 . Google Scholar Crossref Search ADS PubMed WorldCat Cooke S. J. Blumstein D. T. Buchholz R. Caro T. Fernández-Juricic E. Franklin C. E. Metcalfe J. , et al. 2014 . Physiology, behavior, and conservation . Physiological and Biochemical Zoology , 87 : 1 – 14 . Google Scholar Crossref Search ADS PubMed WorldCat Crain C. M. Kroeker K. Halpern B. S. 2008 . Interactive and cumulative effects of multiple human stressors in marine systems . Ecology Letters , 11 : 1304 – 1315 . Google Scholar Crossref Search ADS PubMed WorldCat Di Cicco E. , Ferguson H. W. , Kaukinen K. H. , Schulze A. D. , Li S. , Tabata A. , Günther O. P. , et al. . 2018 . The same strain of Piscine orthoreovirus (PRV-1) is involved in the development of different, but related, diseases in Atlantic and Pacific Salmon in British Columbia . FACETS , 3 : 599 – 641 . Google Scholar Crossref Search ADS WorldCat Di Cicco E. , Ferguson H. W. , Schulze A. D., Kaukinen K. H.S., TVanderstichel R., GWessel Ø., et al. . 2018 . Heart and skeletal muscle inflammation (HSMI) disease diagnosed on a British Columbia salmon farm through a longitudinal farm study. PLoS One, 12: e0171471 . Dionne M. Miller K. M. Dodson J. J. Caron F. Bernatchez L. 2007 . Clinal variation in MHC diversity with temperature: evidence for the role of host–pathogen interaction on local adaptation in Atlantic salmon . Evolution , 61 : 2154 – 2164 . Google Scholar Crossref Search ADS PubMed WorldCat Diserud O. H. Fiske P. Sægrov H. Urdal K. Aronsen T. Lo H. Barlaup B. T. , et al. 2019 . Escaped farmed Atlantic salmon in Norwegian rivers during 1989–2013 . ICES Journal of Marine Science , 76 : 1140 – 1150 . Google Scholar Crossref Search ADS WorldCat Dobson A. P. Hudson P. J. 1986 . Parasites, disease and the structure of ecological communities . Trends in Ecology & Evolution , 1 : 11 – 15 . Google Scholar Crossref Search ADS PubMed WorldCat Drenner S. M. Hinch S. G. Furey N. B. Clark T. D. Li S. Ming T. Jeffries K. M. , et al. 2018 . Transcriptome patterns and blood physiology associated with homing success of sockeye salmon during their final stage of marine migration . Canadian Journal of Fisheries and Aquatic Sciences , 75 : 1511 – 1524 . Google Scholar Crossref Search ADS WorldCat Dushkina L. A. 1994 . Farming of salmonids in Russia . Aquaculture Research , 25 : 121 – 126 . Google Scholar Crossref Search ADS WorldCat Elliott J. Elliott J. A. 2010 . Temperature requirements of Atlantic salmon Salmo salar, brown trout Salmo trutta and Arctic charr Salvelinus alpinus: predicting the effects of climate change . Journal of Fish Biology , 77 : 1793 – 1817 . Google Scholar Crossref Search ADS PubMed WorldCat Ferguson A. Reed T. E. Cross T. F. McGinnity P. Prodöhl P. A. 2019 . Anadromy, potamodromy and residency in brown trout Salmo trutta: the role of genes and the environment . Journal of Fish Biology , 95 : 692 – 718 . Google Scholar PubMed OpenURL Placeholder Text WorldCat Fjær M. A. D. 2019 . Pukkellaks (Oncorhynchus gorbuscha) tatt på Vestlandet.-Hvilke parasitter og infeksjoner bærer de på? Master thesis, The University of Bergen. Forseth T. , Barlaup B. T. , Finstad B. , Fiske P. , Gjøsæter H. , Falkegård M. , Hindar A. , et al. . 2017 . The major threats to Atlantic salmon in Norway . ICES Journal of Marine Science , 74 : 1496 – 1513 . Google Scholar Crossref Search ADS WorldCat Friedland K. D. Dannewitz J. Romakkaniemi A. Palm S. Pulkkinen H. Pakarinen T. Oeberst R. 2017 . Post-smolt survival of Baltic salmon in context to changing environmental conditions and predators . ICES Journal of Marine Science , 74 : 1344 – 1355 . Google Scholar Crossref Search ADS WorldCat Friedland K. D. Reddin D. G. Castonguay M. 2003 . Ocean thermal conditions in the post-smolt nursery of North American Atlantic salmon . ICES Journal of Marine Science , 60 : 343 – 355 . Google Scholar Crossref Search ADS WorldCat Fry F. E. J. 1947 . Effect of the Environment on Animal Activity. University of Toronto Studies Biological Series 55, pp. 1 – 62 . Garseth Å. H. Biering E. Aunsmo A. 2013 . Associations between piscine reovirus infection and life history traits in wild-caught Atlantic salmon Salmo salar L. in Norway . Preventive Veterinary Medicine , 112 : 138 – 146 . Google Scholar Crossref Search ADS PubMed WorldCat Garseth Å. H. Ekrem T. Biering E. 2013 . Phylogenetic evidence of long distance dispersal and transmission of piscine reovirus (PRV) between farmed and wild Atlantic salmon . PLoS One , 8 : e82202 . Google Scholar Crossref Search ADS PubMed WorldCat Garseth Å. H. Fritsvold C. Opheim M. Skjerve E. Biering E. 2013 . Piscine reovirus (PRV) in wild Atlantic salmon, Salmo salar L., and sea‐trout, Salmo trutta L., in Norway . Journal of Fish Diseases , 36 : 483 – 493 . Google Scholar Crossref Search ADS PubMed WorldCat Garseth Å. H. Gjessing M. C. Moldal T. Gjevre A. G. 2018 . A survey of salmon gill poxvirus (SGPV) in wild salmonids in Norway . Journal of Fish Diseases , 41 : 139 – 145 . Google Scholar Crossref Search ADS PubMed WorldCat Green D. M. Gregory A. Munro L. A. 2009 . Small- and large-scale network structure of live fish movements in Scotland . Preventive Veterinary Medicine , 91 : 261 – 269 . Google Scholar Crossref Search ADS PubMed WorldCat Groner M. L. Rogers L. A. Bateman A. W. Connors B. M. Frazer L. N. Godwin S. C. Krkošek M. , et al. 2016 . Lessons from sea louse and salmon epidemiology . Philosophical Transactions of the Royal Society B: Biological Sciences , 371 : 20150203 . Google Scholar Crossref Search ADS WorldCat Haigh N. Esenkulova S. 2014 . Economic losses to the British Columbia salmon aquaculture industry due to harmful algal blooms, 2009-2012. PICES Scientific Report 2. Harrison P. M. Gutowsky L. F. G. Martins E. G. Patterson D. A. Cooke S. J. Power M. 2015 . Personality-dependent spatial ecology occurs independently from dispersal in wild burbot (Lota lota) . Behavioral Ecology , 26 : 483 – 492 . Google Scholar Crossref Search ADS WorldCat Harvell C. D. 2002 . Climate warming and disease risks for terrestrial and marine biota . Science , 296 : 2158 – 2162 . Google Scholar Crossref Search ADS PubMed WorldCat Heggberget T. G. Johnsen B. O. Hindar K. Jonsson B. Hansen L. P. Hvidsten N. A. Jensen A. J. 1993 . Interactions between wild and cultured Atlantic salmon—a review of the Norwegian experience . Fisheries Research , 18 : 123 – 146 . Google Scholar Crossref Search ADS WorldCat Hjeltnes B. Bang-Jensen B. Bornø G. Haukaas A. Walde CSr. 2019 The Health Situation in Norwegian Aquaculture 2018. Norwegian Veterinary Institute, Oslo. 132 pp. Houde A. L. S. Akbarzadeh A. Günther O. P. Li S. Patterson D. A. Farrell A. P. Hinch S. G. , et al. 2019 a. Salmonid gene expression biomarkers indicative of physiological responses to changes in salinity, temperature, but not dissolved oxygen . Journal of Experimental Biology , 222 : 198036 . Google Scholar Crossref Search ADS WorldCat Houde A. L. S. Günther O. P. Strohm J. Ming T. J. Li S. Kaukinen K. H. Patterson D. A. , et al. 2019 b. Discovery and validation of candidate smoltification gene expression biomarkers across multiple species and ecotypes of Pacific salmonids . Conservation Physiology , 7 : coz051 . Google Scholar Crossref Search ADS PubMed WorldCat Hussey N. E. Kessel S. T. Aarestrup K. Cooke S. J. Cowley P. D. Fisk A. T. Harcourt R. G. , et al. 2015 . Aquatic animal telemetry: a panoramic window into the underwater world . Science , 348 : 1255642 – 1255642 . Google Scholar Crossref Search ADS PubMed WorldCat Hvas M. Karlsbakk E. Mæhle S. Wright D. W. Oppedal F. 2017 . The gill parasite Paramoeba perurans compromises aerobic scope, swimming capacity and ion balance in Atlantic salmon . Conservation Physiology , 5 : cox066 . Google Scholar Crossref Search ADS PubMed WorldCat Imsland A. K. D. Sagerup K. Remen M., K. B.-H. Hemmingsen W. Myklebust E. A. 2019 Kunnskaps- og erfaringskartlegging av skottelus. Akvaplan-niva rapport: APN-60795. 96 pp. Jackson D. Moberg O. Stenevik Djupevåg E. M. Kane F. Hareide H. 2018 . The drivers of sea lice management policies and how best to integrate them into a risk management strategy: an ecosystem approach to sea lice management . Journal of Fish Diseases , 41 : 927 – 933 . Google Scholar Crossref Search ADS PubMed WorldCat Jansen P. A. Kristoffersen A. B. Viljugrein H. Jimenez D. Aldrin M. Stien A. 2012 . Sea lice as a density-dependent constraint to salmonid farming . Proceedings of the Royal Society B: Biological Sciences , 279 : 2330 – 2338 . Google Scholar Crossref Search ADS WorldCat Jeffries K. M. Hinch S. G. Gale M. K. Clark T. D. Lotto A. G. Casselman M. T. Li S. , et al. 2014 . Immune response genes and pathogen presence predict migration survival in wild salmon smolts . Molecular Ecology , 23 : 5803 – 5815 . Google Scholar Crossref Search ADS PubMed WorldCat Jeffries K. M. Hinch S. G. Sierocinski T. Clark T. D. Eliason E. J. Donaldson M. R. Li S. , et al. 2012 . Consequences of high temperatures and premature mortality on the transcriptome and blood physiology of wild adult sockeye salmon (Oncorhynchus nerka) . Ecology and Evolution , 2 : 1747 – 1764 . Google Scholar Crossref Search ADS PubMed WorldCat Jensen A. J. Finstad B. Fiske P. Forseth T. Rikardsen A. H. Ugedal O. 2018 . Relationship between marine growth and sea survival of two anadromous salmonid fish species . Canadian Journal of Fisheries and Aquatic Sciences , 75 : 621 – 628 . Google Scholar Crossref Search ADS WorldCat Johnsen B. O. Jensen A. J. 1986 . Infestations of Atlantic salmon, Salmo salar, by Gyrodactylus salaris in Norwegian rivers . Journal of Fish Biology , 29 : 233 – 241 . Google Scholar Crossref Search ADS WorldCat Johnsen B. O. Jensen A. J. 1994 . The spread of furunculosis in salmonids in Norwegian rivers . Journal of Fish Biology , 45 : 47 – 55 . Google Scholar Crossref Search ADS WorldCat Kambestad M. A. 2019 Microparasites in selected populations of wild Atlantic salmon (Salmo salar) in Norway—prevalence, density and diversity. Master thesis, Department of Biological Sciences, University of Bergen. 107 pp. Karlsson S. , Diserud O. H. , Fiske P. , Hindar K. , and editor. W. Stewart Grant. ( 2016 ). Widespread Genetic Introgression of Escaped Farmed Atlantic Salmon in Wild Salmon Populations . ICES Journal of Marine Science , 73 : 2488 – 2498 . Google Scholar Crossref Search ADS WorldCat Karlsson S. , Diserud O. H. , Moen T. , and Hindar K. 2014 . A standardized method for quantifying unidirectional genetic introgression . Ecology and Evolution , 4 : 3256 – 3263 . Google Scholar Crossref Search ADS PubMed WorldCat Karlsson S. , Moen T. , Lien S. , Glover K. A. , and Hindar K. 2011 . Generic genetic differences between farmed and wild Atlantic salmon identified from a 7K SNP‐chip . Molecular Ecology Resources , 11 : 247 – 253 . Google Scholar Crossref Search ADS PubMed WorldCat Kent M. L. 2000 . Marine netpen farming leads to infections with some unusual parasites . International Journal for Parasitology , 30 : 321 – 326 . Google Scholar Crossref Search ADS PubMed WorldCat Kibenge F. S. B. Kibenge F. S. B. Munir K. Kibenge† M. J. T. Joseph T. Moneke E. 2004 . Infectious salmon anemia virus: causative agent, pathogenesis and immunity . Animal Health Research Reviews , 5 : 65 – 78 . Google Scholar Crossref Search ADS PubMed WorldCat Kirk D. Jones N. Peacock S. Phillips J. Molnár P. K. Krkošek M. Luijckx P. 2018 . Empirical evidence that metabolic theory describes the temperature dependency of within-host parasite dynamics . PLoS Biology , 16 : e2004608 . Google Scholar Crossref Search ADS PubMed WorldCat Klemetsen A. Amundsen P. A. Dempson J. B. Jonsson B. Jonsson N. O'connell M. F. Mortensen E. 2003 . Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.): a review of aspects of their life histories . Ecology of Freshwater Fish , 12 : 1 – 59 . Google Scholar Crossref Search ADS WorldCat Kristoffersen A. B. , Qviller L. , Helgesen K. O. , Vollset K. W. , Viljugrein H. , and Jansen P. A. 2018 . Quantitative risk assessment of salmon louse-induced mortality of seaward-migrating post-smolt Atlantic salmon . Epidemics , 23 : 19 – 33 . Google Scholar Crossref Search ADS PubMed WorldCat Krkošek M. 2010 . Host density thresholds and disease control for fisheries and aquaculture . Aquaculture Environment Interactions , 1 : 21 – 32 . Google Scholar Crossref Search ADS WorldCat Krkošek M. 2017 . Population biology of infectious diseases shared by wild and farmed fish . Canadian Journal of Fisheries and Aquatic Sciences , 74 : 620 – 628 . Google Scholar Crossref Search ADS WorldCat Lafferty K. D. Allesina S. Arim M. Briggs C. J. De Leo G. Dobson A. P. Dunne J. A. , et al. 2008 . Parasites in food webs: the ultimate missing links . Ecology Letters , 11 : 533 – 546 . Google Scholar Crossref Search ADS PubMed WorldCat Lafferty K. D. Harvell C. D. Conrad J. M. Friedman C. S. Kent M. L. Kuris A. M. Powell E. N. , et al. 2015 . Infectious diseases affect marine fisheries and aquaculture economics . Annual Review of Marine Science , 7 : 471 – 496 ., Google Scholar Crossref Search ADS PubMed WorldCat Laikre L. Schwartz M. K. Waples R. S. Ryman N. ; GeM Working Group . 2010 . Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals . Trends in Ecology & Evolution , 25 : 520 – 529 . Google Scholar Crossref Search ADS PubMed WorldCat Laurin E. , Jaramillo D. , Vanderstichel R. , Ferguson H. , Kaukinen K. H. , Schulze A. D. , Keith I. R. , et al. . 2019 . Histopathological and novel high-throughput molecular monitoring data from farmed salmon (Salmo salar and Oncorhynchus spp.) in British Columbia, Canada, from 2011–2013 . Aquaculture , 499 : 220 – 234 . Google Scholar Crossref Search ADS WorldCat Le Luyer J. Laporte M. Beacham T. D. Kaukinen K. H. Withler R. E. Leong J. S. Rondeau E. B. , et al. 2017 . Parallel epigenetic modifications induced by hatchery rearing in a Pacific salmon . Proceedings of the National Academy of Sciences of the United States of America , 114 : 12964 – 12969 . Google Scholar Crossref Search ADS PubMed WorldCat Lennox R. J. Aarestrup K. Cooke S. J. Cowley P. D. Deng Z. D. Fisk A. T. Harcourt R. G. , et al. 2017 . Envisioning the future of aquatic animal tracking: technology, science, and application . BioScience , 67 : 884 – 896 . Google Scholar Crossref Search ADS WorldCat Lennox R. J. Eldøy S. H. Vollset K. W. Miller K. M. Li S. Kaukinen K. H. Isaksen T. E. , et al. 2020 . How pathogens affect the marine habitat use and migration of sea trout (Salmo trutta) in two Norwegian fjord systems . Journal of Fish Diseases , 43 : 729 – 746 . Google Scholar Crossref Search ADS PubMed WorldCat Madhun A. S. Isachsen C. H. Omdal L. M. Einen A. C. B. Bjørn P. A. Nilsen R. Karlsbakk E. 2016 . Occurrence of salmonid alphavirus (SAV) and piscine orthoreovirus (PRV) infections in wild sea trout Salmo trutta in Norway . Diseases of Aquatic Organisms , 120 : 109 – 113 . Google Scholar Crossref Search ADS PubMed WorldCat Madhun A. S. Isachsen C. H. Omdal L. M. Einen A. C. B. Maehle S. Wennevik V. Niemelä E. , et al. 2018 . Prevalence of piscine orthoreovirus and salmonid alphavirus in sea‐caught returning adult Atlantic salmon (Salmo salar L.) in northern Norway . Journal of Fish Diseases , 41 : 797 – 803 . Google Scholar Crossref Search ADS PubMed WorldCat Madhun A. S. Karlsbakk E. Isachsen C. H. Omdal L. M. Eide Sørvik A. G. Skaala Ø. Barlaup B. T. , et al. 2015 . Potential disease interaction reinforced: double‐virus‐infected escaped farmed Atlantic salmon, Salmo salar L., recaptured in a nearby river . Journal of Fish Diseases , 38 : 209 – 219 . Google Scholar Crossref Search ADS PubMed WorldCat McCallum H. I. Kuris A. Harvell C. D. Lafferty K. D. Smith G. W. Porter J. 2004 . Does terrestrial epidemiology apply to marine systems? Trends in Ecology & Evolution , 19 : 585 – 591 . Google Scholar Crossref Search ADS WorldCat McLeay D. J. Gordon M. R. 1977 . Leucocrit: a simple hematological technique for measuring acute stress in salmonid fish, including stressful concentrations of pulpmill effluent . Journal of the Fisheries Research Board of Canada , 34 : 2156 – 2175 . Google Scholar Crossref Search ADS WorldCat McVicar A. 1997 . Disease and parasite implications of the coexistence of wild and cultured Atlantic salmon populations . ICES Journal of Marine Science , 54 : 1093 – 1103 . Google Scholar OpenURL Placeholder Text WorldCat Mennerat A. Hamre L. Ebert D. Nilsen F. Davidova M. Skorping A. 2012 . Life history and virulence are linked in the ectoparasitic salmon louse Lepeophtheirus salmonis . Journal of Evolutionary Biology , 25 : 856 – 861 . Google Scholar Crossref Search ADS PubMed WorldCat Mesa M. G. Poe T. P. Gadomski D. M. Petersen J. H. 1994 . Are all prey created equal? A review and synthesis of differential predation on prey in substandard condition . Journal of Fish Biology , 45 : 81 – 96 . Google Scholar Crossref Search ADS WorldCat Miller K. M. Gardner I. A. Vanderstichel R. Burnley T. Angela D. Li S. Ginther N. G. 2016 . Report on the Performance Evaluation of the Fluidigm BioMark Platform for High-Throughput Microbe Monitoring in Salmon. Fisheries and Oceans Canada, Ecosystems and Oceans Science. British Columbia. 282 pp. Miller K. M. Günther O. P. Li S. Kaukinen K. H. Ming T. J. 2017 . Molecular indices of viral disease development in wild migrating salmon . Conservation Physiology , 5 : cox036. Google Scholar OpenURL Placeholder Text WorldCat Miller K. M. Li S. Kaukinen K. H. Ginther N. Hammill E. Curtis J. M. R. Patterson D. A. , et al. 2011 . Genomic signatures predict migration and spawning failure in wild Canadian salmon . Science , 331 : 214 – 217 . Google Scholar Crossref Search ADS PubMed WorldCat Miller K. M. Teffer A. Tucker S. Li S. Schulze A. D. Trudel M. Juanes F. , et al. 2014 . Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines . Evolutionary Applications , 7 : 812 – 855 . Google Scholar Crossref Search ADS PubMed WorldCat Moles A. 1997 . Effect of bacterial kidney disease on saltwater adaptation of coho salmon smolts . Journal of Aquatic Animal Health , 9 : 230 – 233 . Google Scholar Crossref Search ADS WorldCat Mordecai G. J. Miller K. M. Di Cicco E. Schulze A. D. Kaukinen K. H. Ming T. J. Li S. , et al. 2019 . Endangered wild salmon infected by newly discovered viruses . eLife , 8 : Google Scholar OpenURL Placeholder Text WorldCat Mordecai G. J. , Di Cicco E. Gunther O. P. Schulze A. D. Kaukinen K. H. Li S. , et al. ( 2020 ). Emerging viruses in British Columbia salmon discovered via a viral immune response biomarker panel and metatranscriptomic sequencing. bioRxiv. Nekouei O. , Vanderstichel R. , Kaukinen K. H. , Thakur K. , Ming T. , Patterson D. A. , Trudel M. , et al. . 2019 . Comparison of infectious agents detected from hatchery and wild juvenile Coho salmon in British Columbia, 2008-2018 . PLOS ONE , 14 : e0221956 . Google Scholar Crossref Search ADS PubMed WorldCat Niklitschek E. J. Soto D. Lafon A. Molinet C. Toledo P. 2013 . Southward expansion of the Chilean salmon industry in the Patagonian Fjords: main environmental challenges . Reviews in Aquaculture , 5 : 172 – 195 . Google Scholar Crossref Search ADS WorldCat Olaussen J. O. 2018 . Environmental problems and regulation in the aquaculture industry. Insights from Norway . Marine Policy , 98 : 158 – 163 . Google Scholar Crossref Search ADS WorldCat Oli M. K. Venkataraman M. Klein P. A. Wendland L. D. Brown M. B. 2006 . Population dynamics of infectious diseases: a discrete time model . Ecological Modelling , 198 : 183 – 194 . Google Scholar Crossref Search ADS WorldCat Olsson I. C. Greenberg L. A. Bergman E. Wysujack K. 2006 . Environmentally induced migration: the importance of food . Ecology Letters , 9 : 645 – 651 . Google Scholar Crossref Search ADS PubMed WorldCat Peeler E. Murray A. 2004 . Disease interaction between farmed and wild fish populations . Journal of Fish Biology , 65 : 321 – 322 . Google Scholar Crossref Search ADS WorldCat Pickering A. D. 1992 . Rainbow trout husbandry—management of the stress response . Aquaculture , 100 : 125 – 139 . Google Scholar Crossref Search ADS WorldCat Raby G. D. Clark T. D. Farrell A. P. Patterson D. A. Bett N. N. Wilson S. M. Willmore W. G. , et al. 2015 . Facing the river gauntlet: understanding the effects of fisheries capture and water temperature on the physiology of coho salmon . PLoS One , 10 : e0124023., Google Scholar Crossref Search ADS WorldCat Ray R. A. Holt R. A. Bartholomew J. L. 2012 . Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath River salmonids . Journal of Parasitology , 98 : 520 – 526 . Google Scholar Crossref Search ADS PubMed WorldCat Ricklefs R. E. Wikelski M. 2002 . The physiology/life-history nexus . Trends in Ecology & Evolution , 17 : 462 – 468 . Google Scholar Crossref Search ADS WorldCat Sandlund O. T. Berntsen H. H. Fiske P. Kuusela J. Muladal R. Niemelä E. Uglem I. , et al. 2019 . Pink salmon in Norway: the reluctant invader . Biological Invasions , 21 : 1033 – 1054 . Google Scholar Crossref Search ADS WorldCat Sandvik A. D. Johnsen I. A. Myksvoll M. S. Sævik P. N. Skogen M. D. 2020 . Prediction of the salmon lice infestation pressure in a Norwegian fjord . ICES Journal of Marine Science , 77 : 746 – 756 . Google Scholar Crossref Search ADS WorldCat Schemske D. W. Mittelbach G. G. Cornell H. V. Sobel J. M. Roy K. 2009 . Is there a latitudinal gradient in the importance of biotic interactions? Annual Review of Ecology, Evolution, and Systematics , 40 : 245 – 269 . Google Scholar Crossref Search ADS WorldCat Schisler G. J. Walker P. G. Chittum L. A. Bergersen E. P. 1999 . Gill ectoparasites of juvenile rainbow trout and brown trout in the upper Colorado River . Journal of Aquatic Animal Health , 11 : 170 – 174 . Google Scholar Crossref Search ADS WorldCat Shephard S. MacIntyre C. Gargan P. 2016 . Aquaculture and environmental drivers of salmon lice infestation and body condition in sea trout . Aquaculture Environment Interactions , 8 : 597 – 610 . Google Scholar Crossref Search ADS WorldCat Snieszko S. F. 1974 . The effects of environmental stress on outbreaks of infectious diseases of fishes . Journal of Fish Biology , 6 : 197 – 208 . Google Scholar Crossref Search ADS WorldCat Soler J. J. , Neve L. d Pérez–Contreras T Soler M. , and Sorci G. 2003 . Trade-off between immunocompetence and growth in magpies: an experimental study . Proceedings of the Royal Society of London. Series B: Biological Sciences , 270 : 241 – 248 . Google Scholar Crossref Search ADS WorldCat Strimbu K. Tavel J. A. 2010 . What are biomarkers? Current Opinion in HIV and AIDS , 5 : 463 – 466 . Google Scholar Crossref Search ADS PubMed WorldCat Sundby S. Nakken O. 2008 . Spatial shifts in spawning habitats of Arcto-Norwegian cod related to multidecadal climate oscillations and climate change . ICES Journal of Marine Science , 65 : 953 – 962 . Google Scholar Crossref Search ADS WorldCat Svenning M. A. Sandem K. Halvorsen M. Kanstad-Hanssen Ø. Falkegård M. Borgstrøm R. 2016 . Change in relative abundance of Atlantic salmon and Arctic charr in Veidnes River, Northern Norway: a possible effect of climate change? Hydrobiologia , 783 : 145 – 158 . Google Scholar Crossref Search ADS WorldCat Taranger G. L. Karlsen Ø. Bannister R. J. Glover K. A. Husa V. Karlsbakk E. Kvamme B. O. , et al. 2015 . Risk assessment of the environmental impact of Norwegian Atlantic salmon farming . ICES Journal of Marine Science , 72 : 997 – 1021 . Google Scholar Crossref Search ADS WorldCat Teffer A. K. , Carr J. , Tabata A. , Schulze A. , Bradbury I. , Deschamps D. , Gillis C.-A. , et al. . 2020 . A molecular assessment of infectious agents carried by Atlantic salmon at sea and in three eastern Canadian rivers, including aquaculture escapees and North American and European origin wild stocks . FACETS , 5 : 234 – 263 . Google Scholar Crossref Search ADS WorldCat Teffer A. K. Bass A. L. Miller K. M. Patterson D. A. Juanes F. Hinch S. G. 2018 . Infections, fisheries capture, temperature, and host responses: multistressor influences on survival and behaviour of adult Chinook salmon . Canadian Journal of Fisheries and Aquatic Sciences , 75 : 2069 – 2083 . Google Scholar Crossref Search ADS WorldCat Teffer A. K. Hinch S. Miller K. Jeffries K. Patterson D. Cooke S. Farrell A. , et al. 2019 . Cumulative effects of thermal and fisheries stressors reveal sex-specific effects on infection development and early mortality of adult coho salmon (Oncorhynchus kisutch) . Physiological and Biochemical Zoology , 92 : 505 – 529 . Google Scholar Crossref Search ADS PubMed WorldCat Thakur K. K. Vanderstichel R. Li S. Laurin E. Tucker S. Neville C. Tabata A. , et al. 2018 . A comparison of infectious agents between hatchery-enhanced and wild out-migrating juvenile chinook salmon (Oncorhynchus tshawytscha) from Cowichan River, British Columbia . Facets , 3 : 695 – 721 . Google Scholar Crossref Search ADS WorldCat Tucker S. , Li S. , Kaukinen K. H., Patterson D. A. , and Miller K. M. 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 : e0195472 . Google Scholar Crossref Search ADS PubMed WorldCat Twardek W. M. Chapman J. M. Miller K. M. Beere M. C. Li S. Kaukinen K. H. Danylchuk A. J. , et al. 2019 . Evidence of a hydraulically challenging reach serving as a barrier for the upstream migration of infection-burdened adult steelhead . Conservation Physiology , 7 : coz023 . Google Scholar PubMed OpenURL Placeholder Text WorldCat UN FAO . 2018 . The State of World Fisheries and Aquaculture (SOFIA): Contributing to Food Security and Nutrition for All. Food and Agriculture Organization, Rome. 227 pp. http://www.fao.org/3/I9540EN/i9540en.pdf. Urquhart K. Pert C. C. Fryer R. J. Cook P. Weir S. Kilburn R. McCarthy U. , et al. 2010 . A survey of pathogens and metazoan parasites on wild sea trout (Salmo trutta) in Scottish waters . ICES Journal of Marine Science , 67 : 444 – 453 . Google Scholar Crossref Search ADS WorldCat Vike S. Nylund S. Nylund A. 2008 . ISA virus in Chile: evidence of vertical transmission . Archives of Virology , 154 : 1 – 8 . Google Scholar Crossref Search ADS PubMed WorldCat Vollset K. W. 2019 . Parasite induced mortality is context dependent in Atlantic salmon: insights from an individual-based model . Scientific Reports , 9 : 1 – 15 . Google Scholar Crossref Search ADS PubMed WorldCat Vollset K. W. Dohoo I. Karlsen Ø. Halttunen E. Kvamme B. O. Finstad B. Wennevik V. , et al. 2018 a. Disentangling the role of sea lice on the marine survival of Atlantic salmon . ICES Journal of Marine Science , 75 : 50 – 60 . Google Scholar Crossref Search ADS WorldCat Vollset K. W. Krontveit R. I. Jansen P. A. Finstad B. Barlaup B. T. Skilbrei O. T. Krkošek M. , et al. 2016 . Impacts of parasites on marine survival of Atlantic salmon: a meta‐analysis . Fish and Fisheries , 17 : 714 – 730 . Google Scholar Crossref Search ADS WorldCat Vollset K. W. Nilsen F. Ellingsen I. Finstad B. Helgesen K. O. Karlsen Ø. Sandvik A. D. , et al. 2019 . Vurdering av lakselusindusert villfiskdødelighet per produksjonsområde i 2019. Rapport fra ekspertgruppe for vurdering av lusepåvirkning. Norwegian report. https://www.regjeringen.no/globalassets/departementene/nfd/dokumenter/rapporter/ekspertgruppe-rapport_2019.pdf. Vollset K. W. Qviller L. Skår B. Barlaup B. T. Dohoo I. 2018 b. Parasitic sea louse infestations on wild sea trout: separating the roles of fish farms and temperature . Parasites & Vectors , 11 : 609 . Google Scholar Crossref Search ADS PubMed WorldCat Wallace I. S. McKay P. Murray A. G. 2017 . A historical review of the key bacterial and viral pathogens of Scottish wild fish . Journal of Fish Diseases , 40 : 1741 – 1756 . Google Scholar Crossref Search ADS PubMed WorldCat Willem L. Verelst F. Bilcke J. Hens N. Beutels P. 2017 . Lessons from a decade of individual-based models for infectious disease transmission: a systematic review (2006–2015 ). BMC Infectious Diseases , 17 : 612 . Google Scholar Crossref Search ADS PubMed WorldCat © International Council for the Exploration of the Sea 2020. All rights reserved. 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TI - Wild salmonids are running the gauntlet of pathogens and climate as fish farms expand northwards
JO - ICES Journal of Marine Science
DO - 10.1093/icesjms/fsaa138
DA - 2020-10-10
UR - https://www.deepdyve.com/lp/oxford-university-press/wild-salmonids-are-running-the-gauntlet-of-pathogens-and-climate-as-VL1eGrF5Pt
SP - 1
EP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -