Differential infestation of juvenile Pacific salmon by parasitic sea lice in British Columbia, Canada

Parasitism can influence fish recruitment and population growth via direct mortality and potentially through parasite-mediated sublethal effects on host behaviour, growth, predation risk, and reproductive success (Williams 1964; Barber et al. 2000; Longshaw et al. 2010; Krkošek et al. 2013b). Many fish parasites are generalists, infecting multiple host species, which can lead to apparent competition — indirect competition via some shared natural enemy (Hudson and Greenman 1998) — among host populations. Generalist parasites can persist even when the abundance of a focal host species is low by infesting a reservoir host species, leading to spill-over and spill-back dynamics that are relevant for management of farmed and wild stocks (Hedrick 1998; de Castro and Bolker 2005). Such is the case in the coastal waters of British Columbia (BC), Canada, where a specialist parasite, Lepeophtheirus salmonis (Johnson and Albright 1991), infects wild Pacific salmon (Oncorhynchus spp.) and farmed Atlantic salmon (Salmo salar), while these salmon along with Pacific herring (Clupea pallasii) share a generalist fish parasite, Caligus clemensi (Parker and Margolis 1964). Both of these parasites are ectoparasitic copepods broadly called “sea lice”. All of the host fish species are commercially important, and numerous populations of wild salmon and herring are also a focus for conservation. Prevalence of L. salmonis and C. clemensi on wild juvenile salmon is positively correlated with the presence of Atlantic salmon farms in BC (Marty et al. 2010; Price et al. 2011). How the dynamics of L. salmonis and C. clemensi vary among Pacific salmon species, however, is not well resolved, nor is the role of herring in this host–parasite system, which may serve as a natural reservoir host population for C. clemensi (Morton et al. 2008; Beamish et al. 2009).

Pacific salmon support some of the most important fisheries in Canada and are of ecological, cultural, and historical importance (Hilderbrand et al. 2004; Scheuerell et al. 2005; FAO 2015). Populations of Pacific salmon have experienced major declines in recent decades, for example, sockeye salmon (Oncorhynchus nerka) from the Fraser River, whose decline triggered a CAN$37 million federal judicial inquiry (Cohen 2012). This inquiry identified the early marine phase as a potentially critical life stage for overall survival and recruitment of Fraser River salmon populations and specifically called for investigation into the interactions between migrating wild juvenile salmon and sea lice (Peterman et al. 2010; Cohen 2012). Sockeye, pink (Oncorhynchus gorbuscha), and chum (Oncorhynchus keta) salmon from the Fraser River enter the marine environment in the Strait of Georgia and primarily migrate through the Discovery Islands and Johnstone Strait, before passing through Queen Charlotte Sound to the open ocean (Fig. 1). When juvenile salmon leave their natal freshwater systems for their early marine migration, they experience multiple stressors, including variable prey availability, predators, and parasites (Hunt et al. 2018).

The sea lice C. clemensi and L. salmonis are native to BC, and both feed on the surface tissues, musculature, and blood of their host fish (Costello 1993; Krkošek et al. 2009). Sea lice are unable to survive in freshwater environments (Bricknell et al. 2006), but naturally infest juvenile salmon at low intensities after the fish migrate into the marine environment in spring. The abundances of sea lice observed on juvenile salmon in spring are a result of transmission from other wild fish species and farmed salmon, with most migratory adult salmon not having returned yet to coastal waters (Groot and Margolis 1991; Krkošek et al. 2005a). Juvenile sockeye in the Discovery Islands and Johnstone Strait are infected primarily by C. clemensi (Price et al. 2011; Godwin et al. 2015), but there are no estimates comparing infestation by both C. clemensi and L. salmonis among co-migrating juveniles of sockeye, pink, and chum salmon in the Discovery Islands and Johnstone Strait — an area with high density of salmon farms and wild herring (Beamish et al. 2009) (Fig. 1).

In this paper we compare L. salmonis and C. clemensi abundance from co-migrating groups of juvenile pink, chum, and sockeye salmon in the Discovery Islands and Johnstone Strait, BC, over 5 years of field surveys. We investigate possible sources of variation between louse species in their specialization among Pacific salmon species by focusing on the relative abundances of the two louse species on the three salmon species in our study. We also characterize the dynamics of sea lice on wild salmon relative to other areas with salmon farming in BC and the North Atlantic. While many systems are typically dominated by L. salmonis associated with farmed salmon (Mustafa and MacKinnon 1999; Marty et al. 2010; Krkošek et al. 2013b), we explore the possibility of this particular region and species set being characterized more by Caligus from wild herring and farmed salmon reservoir host populations.

Motile-louse abundance was highly variable among individuals, with the majority of fish having no attached lice but several having more than 10. The overall predicted motile L. salmonis abundance across all years was 0.09 (95% CI = 0.06, 0.15) lice per fish for pink salmon, 0.04 (0.02, 0.06) for chum, and 0.01 (0.006, 0.02) for sockeye, while the mean motile C. clemensi abundance for the same salmon species was 0.45 (0.38, 0.55), 0.28 (0.23, 0.35), and 0.39 (0.33, 0.47), respectively. For all three salmon species, C. clemensi reached their highest abundance in 2019, and L. salmonis reached their highest abundance in 2015 (Fig. 2). The year-to-year trends in L. salmonis abundance were consistent for all three salmon species, though abundance on sockeye were low throughout our sampling period. Year-to-year trends were also consistent in C. clemensi abundance for both chum and sockeye salmon (Fig. 2); these were characterized by a decrease between 2015 and 2017 and an increase in 2018 and 2019. Pink salmon exhibited entirely different and highly variable temporal patterns of louse abundance for C. clemensi (Fig. 2), with a large spike in 2017. All three species of salmon were of comparable size in our study; of the fish for which we had measurements, the mean fork lengths (±SE) were 109.3 (±16.3), 111.3 (±15.8), and 107.1 (±14.3) mm for pink, chum, and sockeye, respectively.

The models that received the most support from the data differed between the two louse species (Tables 1 and 2, Supplementary Table S1¹). The highest ranking model for C. clemensi included fixed effects for year, sampling area, salmon species, the interaction between salmon species and sampling area, the interaction between sampling area and year, and the interaction between salmon species and year. The top model for L. salmonis was similar but did not include the interaction between sampling area and year, nor the interaction between salmon species and year. For both the C. clemensi and L. salmonis model sets, salmon species had the highest relative variable importance (RVI) value of 1.0, as it was present in all eight of the nonzero weighted models, indicating it was the most important explanatory variable for both louse species. RVI values for the other fixed effects differed between the two model sets (Tables 1 and 2). Despite the support for an effect of salmon species on louse abundance, there was no one “best” model for either louse species. Instead, there were eight models within 13 AIC units of the top L. salmonis model, and eight models within 12 AIC units for C. clemensi. To capture maximum variation, we performed model-averaging over all nonzero weight candidate models, rather than using a delta-AIC threshold to denote which models were considered.

Our model-averaged predictions for L. salmonis and C. clemensi were consistent with observed abundances and showed obvious differences among salmon species, years, and sampling areas (Figs. 3 and 4). Caligus clemensi were more than five times as abundant as L. salmonis, on average, and our mean predictions for C. clemensi were higher than L. salmonis for every combination of salmon species, year, and sampling area. Generally, pink salmon had the highest L. salmonis abundance of any salmon species (Fig. 3). For L. salmonis, by far the highest abundance occurred on pink salmon in the Discovery Islands in 2015 (0.59, 95% CI = (0.31, 0.73)). Sampling area patterns were not consistent across years for L. salmonis; in 2015, all salmon species experienced higher L. salmonis abundances in the Discovery Islands compared with Johnstone Strait, while the opposite pattern generally occurred during 2016–2019. Our model-averaged predictions indicated that pink and sockeye salmon experienced similar C. clemensi abundances. In terms of sampling area, the abundance of C. clemensi on sockeye salmon was higher in the Discovery Islands than in Johnstone Strait, and pink salmon experienced higher C. clemensi abundance in Johnstone Strait than in the Discovery Islands. Chum salmon harboured the fewest C. clemensi in both areas.

Most of the sockeye salmon in our study were from the Fraser River. Of the 673 sockeye salmon that were genetically identified to stock, 89% were from the Fraser River, just over half the fish originating from Chilko (26%), Lower Adams (12%), and Lower Shuswap (12%) stocks. In total, 38 separate stocks were represented in our subsample of sockeye from 2015 to 2017 (Table S2¹).

Our results indicate that C. clemensi and L. salmonis differ in their contribution to the total sea louse burden on juvenile Pacific salmon in the Discovery Islands and Johnstone Strait areas of BC. For a given salmon species, C. clemensi was generally more abundant than L. salmonis across years, and particularly so for sockeye. With respect to salmon species, our results indicate that pink salmon may be a more competent host for both species of louse than sockeye or chum salmon, in contrast with previous estimates of louse abundance on juvenile Pacific salmon (Beamish et al. 2009), which report higher abundances and prevalence of lice on chum salmon. While laboratory studies have shown that pink salmon are relatively resistant to infestation from L. salmonis after some initial growth in the marine environment (Jones et al. 2007; Braden et al. 2012; Sutherland et al. 2014), pink salmon nonetheless had the highest abundances of L. salmonis and C. clemensi. Pink salmon are therefore likely to host the majority of sea lice on wild juvenile salmon in this system; this is in contrast with findings from a nearby region, the Broughton Archipelago, where in 9 of the 10 years data were collected, juvenile chum salmon showed higher louse abundances than juvenile pink salmon (Patanasatienkul et al. 2013). Sockeye salmon also experienced the largest difference in parasite abundance between the two louse species (Figs. 3 and 4). This result corroborates previous, more anecdotal reports that C. clemensi is the primary louse infecting juvenile wild Pacific salmon in this area (Price et al. 2011; Godwin et al. 2018) and that C. clemensi is particularly more abundant on sockeye salmon than L. salmonis. Because these three species co-migrate, differences in infestation rates among species are unlikely to be confounded by environment–species correlations unless there are large differences in species-specific migration speeds.

Our results indicate that there are differences in specialization of C. clemensi and L. salmonis among pink, chum, and sockeye that could arise via the initial infection process, survival of attached parasites, or parasite-induced host mortality. During the initial infection process, free-swimming copepodites (juvenile-stage lice) use both physical and chemical cues to locate and pursue a potential host (MacKinnon 1998; Hevrøy et al. 2003). Although little is known about how these cues differ among salmon species, it is possible that host characteristics such as odour, swimming speed, body shape, and surface roughness, as well as swimming hydrodynamics (Bailey et al. 2006; Mordue and Birkett 2009), could influence the reception of these cues by lice and, ultimately, attachment rates. Once sea lice have attached, host fish mount an immune response to rid themselves of infestation, and these responses vary among salmon species (Jones et al. 2007; Sutherland et al. 2014; Vargas-Chacoff et al. 2016). Direct mortality from sea lice is unlikely at the host sizes we observed (Jones et al. 2008; Sutherland et al. 2011), and specifically for sockeye and C. clemensi, previous studies suggest direct morality is quite low (Jakob et al. 2013; Godwin et al. 2015). However, indirect or “sublethal” effects of sea lice (e.g., slower growth, reduced foraging success, and increased predation risk) may play an important role in reducing host survival, and these effects likely differ according to each species’ foraging strategies and predator interactions (Costello 2009; Peacock et al. 2015; Godwin et al. 2017). The stress response of the salmonids to sea louse infestation typically involves an increase in plasma cortisol levels for both Oncorhynchus and Salmo species (Fast et al. 2006; Jones et al. 2007), along with an inflammatory response resulting from elevated expression of proinflammatory genes (Johnson and Albright 1992; Fast 2014). However, there are likely differences in immune response within the Oncorhynchus genus, and species-specific immune responses likely work in concert with foraging strategies and predator interactions to mediate direct and indirect effects of infestation. If any of these effects on initial infection, attached-louse survival, or host mortality vary with host species, this could explain the differences we observed in C. clemensi and L. salmonis abundances among salmon species. Perhaps most notably, if any of these species have a higher propensity to experience mortality (indirect or direct) as a consequence of louse infection, there would be fewer infected fish of that species in the co-migrating school and therefore in our dataset as well.

Spatial and temporal variation in temperature and salinity, as well as the interaction between the two, could play a role in explaining the differences we see in parasite abundance among years and sampling areas. Lepeophtheirus salmonis has higher rates of development (Hayward et al. 2011), settlement (Tucker et al. 2000), and survival (McEwan et al. 2019) with increased water temperatures. Settlement and survival of L. salmonis also decreases with lowered salinity (Bricknell et al. 2006; Sutherland et al. 2014; Rittenhouse et al. 2016). As juveniles migrate into the Discovery Islands from the Strait of Georgia, they transition to a region of deep tidal mixing that is characterized by colder, more saline water than the stratified Strait of Georgia. These cold and saline tidally mixed conditions persist through Johnstone Strait, before warming again as the fish pass northward into Queen Charlotte Strait (Dosser et al. 2019). These temperature and salinity patterns also vary among years (Riche et al. 2014; Chandler 2018). Looking forward, with a warming climate and resulting increase in coastal water temperatures, sea louse abundance on migrating juvenile salmon is likely to increase, as has been seen in the Broughton Archipelago, BC (Bateman et al. 2016). Climate-driven changes in environmental conditions could also influence survival rates of host fish. However, it is unclear from our current data how environmental drivers interact with other relevant factors to shape infestation patterns as a whole. If salinity and temperature were the only factors influencing infestation, we would expect coherence of infestation patterns among salmon and louse species. The lack of this coherence suggests a more complex relationship between the various drivers of infestation. Further work is needed to gain a more complete understanding of this multi-host–parasite system not only as it currently stands, but how further environmental change will alter its dynamics in the future.

One reservoir host population for sea louse infection pressure on the fish in this study is domesticated Atlantic salmon from salmon farms along the wild salmon migration routes. The link between sea louse counts on salmon farms and sea louse abundance on wild juvenile salmon is well documented for L. salmonis (Krkošek et al. 2007; Morton et al. 2008; Bateman et al. 2016), but has been largely ignored for C. clemensi, the dominant louse species in this study. Management of sea lice on salmon farms is targeted at L. salmonis rather than C. clemensi and involves government-mandated harvest or a delousing treatment when louse abundance exceeds three motile L. salmonis per fish (Fisheries and Oceans Canada 2019). When treatments do occur, they are effective at removing both species of lice (Godwin et al. 2020), but high numbers of C. clemensi themselves do not trigger management action. Industry counts of sea lice on salmon farms show generally low levels of C. clemensi in BC, with occasional very high abundances (Di Cicco et al. 2017). However, recent work has indicated that the true C. clemensi abundance on Atlantic salmon farms is approximately 2.55 times the reported counts (cf. 1.17 for L. salmonis), due to a combination of louse detachment during counts and systematic underestimation when counts are not being audited by Fisheries and Oceans Canada (Godwin et al. 2020). In fact, the true C. clemensi abundance on salmon farms during the wild juvenile salmon migration is roughly equivalent to that of L. salmonis (Godwin et al. 2020). However, while salmon farms may well be a source of C. clemensi for juvenile Pacific salmon, they are unlikely to be the only source or even the dominant source given their generalist nature.

The other main source of C. clemensi in this region is likely Pacific herring, which had high abundances in our study region during the years of our study (2015–2019; DFO 2019) and have been known to carry large abundances of C. clemensi (Morton et al. 2008; Beamish et al. 2009). The abundance of motile-stage C. clemensi on fish in the Discovery Islands and the fast migration speed of sockeye salmon suggests that many of the lice may have been acquired in the Strait of Georgia — the area that supports the largest spawning biomass of Pacific herring in BC (DFO 2019) — before the fish arrived in the salmon farming area of the Discovery Islands. According to Welch et al. (2009), the average residence time of juvenile Fraser River sockeye in the Strait of Georgia is 26–34 days, and while there are no published development rate data for C. clemensi, the development timing of other sea louse species indicates that copepodid lice acquired in the Strait of Georgia would have time to mature into motiles by the time the fish reached the Discovery Islands (Hogans and Trudeau 1989; Piasecki and MacKinnon 1995; Hamre et al. 2019); in contrast, lice acquired in the Discovery Islands would not likely have moulted into motiles by the time of sampling.

The potential of herring to be a primary source of C. clemensi on juvenile salmon is further supported by our sampling area-level results. With the exception of 2015, C. clemensi was present at higher levels in Johnstone Strait relative to the Discovery Islands (Figs. 3 and 4), especially for pink salmon. This rise in abundance between the two sampling areas was not observed for L. salmonis, with the exception of pink salmon in 2017. Since most L. salmonis likely originate from farmed salmon (Krkošek et al. 2007; Marty et al. 2010) and C. clemensi are subject to the same parasiticide treatments on farms, the relative magnitude of the increase in abundance between Discovery Islands and Johnstone Strait should be the same for C. clemensi and L. salmonis in the absence of other wild reservoir hosts. That these sampling area patterns differ between louse species indicates the source pathway may also differ.

Pacific salmon from the Fraser River support some of the most important fisheries in Canada, but many populations are seeing declines and are the focus of considerable conservation concern. In 2019, Fraser River sockeye, which represented almost 90% of the genetically identified sockeye in our study, experienced the worst adult return on record, just 8 years after the conclusion of a CAN$37 million federal inquiry into their decades-long decline in productivity (Cohen 2012; Grant et al. 2019). For sockeye salmon and other threatened species, generalist parasites like C. clemensi — whose abundance on sockeye salmon was on average 39-fold higher than L. salmonis in our study — are of particular concern because their additional reservoir host populations can maintain high levels of parasite abundance in the environment even when focal host abundance is low (de Castro and Bolker 2005; Krkošek et al. 2013a). In our study area, the main reservoir host population for L. salmonis is likely farmed Atlantic salmon (Price et al. 2011; Godwin et al. 2015) and wild Pacific herring for C. clemensi (Morton et al. 2008; Beamish et al. 2009). Our results show that C. clemensi is the dominant louse species infesting out-migrating pink, chum, and sockeye salmon in the most important salmon migration corridor in BC, in contrast with other salmon-farming areas in BC and the North Atlantic where L. salmonis is the dominant species (Glover et al. 2005). Conservation science and management of salmon populations vulnerable to sea louse infestation, like those from the Fraser River, should therefore shift some focus to C. clemensi and its transmission dynamics among farmed salmon, wild herring, and wild juvenile salmon.

First and foremost, the authors thank the Hakai Institute for its tremendous support of the Juvenile Salmon Program. We are also grateful to Salmon Coast Field Station for its invaluable contributions to the Johnstone Strait portion of the field work. This work was funded by the Hakai Institute, an NSERC Post-Graduate Scholarship and a Liber Ero Postdoctoral Fellowship to SCG, a MITACS Accelerate Grant (No. IT09911) to BPVH, and an NSERC Discovery Grant and Canada Research Chair to MK. Thanks as well to Simon Fraser University, the University of Toronto, The University of British Columbia, and the many field and lab technicians that have assisted the Juvenile Salmon Program. We thank two anonymous reviewers for their feedback, which improved the paper.