Oust the louse: leaping behaviour removes sea lice from wild juvenile sockeye salmon Oncorhynchus nerka

We conducted a manipulative field experiment to determine whether the leaping behaviour of wild juvenile sockeye salmon Oncorhynchus nerka dislodges ectoparasitic sea lice Caligus clemensi and Lepeophtheirus salmonis by comparing sea‐lice abundances between O. nerka juveniles prevented from leaping and juveniles allowed to leap at a natural frequency. Juvenile O. nerka allowed to leap had consistently fewer sea lice after the experiment than fish that were prevented from leaping. Combined with past research, these results imply potential costs due to parasitism and indicate that the leaping behaviour of juvenile O. nerka does, in fact, dislodge sea lice.     

Reduced growth in wild juvenile sockeye salmon Oncorhynchus nerka infected with sea lice

Daily growth rings were examined in the otoliths of wild juvenile sockeye salmon Oncorhynchus nerka to determine whether infection by ectoparasitic sea lice Caligus clemensi and Lepeophtheirus salmonis was associated with reduced host body growth, an important determinant of survival. Over 98% of the sea lice proved to be C. clemensi and the fish that were highly infected grew more slowly than uninfected individuals. Larger fish also grew faster than smaller fish. Finally, there was evidence of an interaction between body size and infection status, indicating the potential for parasite‐mediated growth divergence.     

Sea lice and salmon population dynamics: effects of exposure time for migratory fish

The ecological impact of parasite transmission from fish farms is probably mediated by the migration of wild fishes, which determines the period of exposure to parasites. For Pacific salmon and the parasitic sea louse, Lepeophtheirus salmonis, analysis of the exposure period may resolve conflicting observations of epizootic mortality in field studies and parasite rejection in experiments. This is because exposure periods can differ by 2–3 orders of magnitude, ranging from months in the field to hours in experiments. We developed a mathematical model of salmon–louse population dynamics, parametrized by a study that monitored naturally infected juvenile salmon held in ocean enclosures. Analysis of replicated trials indicates that lice suffer high mortality, particularly during pre-adult stages. The model suggests louse populations rapidly decline following brief exposure of juvenile salmon, similar to laboratory study designs and data. However, when the exposure period lasts for several weeks, as occurs when juvenile salmon migrate past salmon farms, the model predicts that lice accumulate to abundances that can elevate salmon mortality and depress salmon populations. The duration of parasite exposure is probably critical to salmon–louse population dynamics, and should therefore be accommodated in coastal planning and management where fish farms are situated on wild fish migration routes.     

How sea lice from salmon farms may cause wild salmonid declines in Europe and North America and be a threat to fishes elsewhere

Fishes farmed in sea pens may become infested by parasites from wild fishes and in turn become point sources for parasites. Sea lice, copepods of the family Caligidae, are the best-studied example of this risk. Sea lice are the most significant parasitic pathogen in salmon farming in Europe and the Americas, are estimated to cost the world industry €300 million a year and may also be pathogenic to wild fishes under natural conditions.Epizootics, characteristically dominated by juvenile (copepodite and chalimus) stages, have repeatedly occurred on juvenile wild salmonids in areas where farms have sea lice infestations, but have not been recorded elsewhere. This paper synthesizes the literature, including modelling studies, to provide an understanding of how one species, the salmon louse, Lepeophtheirus salmonis, can infest wild salmonids from farm sources. Three-dimensional hydrographic models predicted the distribution of the planktonic salmon lice larvae best when they accounted for wind-driven surface currents and larval behaviour. Caligus species can also cause problems on farms and transfer from farms to wild fishes, and this genus is cosmopolitan. Sea lice thus threaten finfish farming worldwide, but with the possible exception of L. salmonis, their host relationships and transmission adaptations are unknown. The increasing evidence that lice from farms can be a significant cause of mortality on nearby wild fish populations provides an additional challenge to controlling lice on the farms and also raises conservation, economic and political issues about how to balance aquaculture and fisheries resource management.     

Modeling Parasite Dynamics on Farmed Salmon for Precautionary Conservation Management of Wild Salmon

Conservation management of wild fish may include fish health management in sympatric populations of domesticated fish in aquaculture. We developed a mathematical model for the population dynamics of parasitic sea lice (Lepeophtheirus salmonis) on domesticated populations of Atlantic salmon (Salmo salar) in the Broughton Archipelago region of British Columbia. The model was fit to a seven-year dataset of monthly sea louse counts on farms in the area to estimate population growth rates in relation to abiotic factors (temperature and salinity), local host density (measured as cohort surface area), and the use of a parasiticide, emamectin benzoate, on farms. We then used the model to evaluate management scenarios in relation to policy guidelines that seek to keep motile louse abundance below an average three per farmed salmon during the March–June juvenile wild Pacific salmon (Oncorhynchus spp.) migration. Abiotic factors mediated the duration of effectiveness of parasiticide treatments, and results suggest treatment of farmed salmon conducted in January or early February minimized average louse abundance per farmed salmon during the juvenile wild salmon migration. Adapting the management of parasites on farmed salmon according to migrations of wild salmon may therefore provide a precautionary approach to conserving wild salmon populations in salmon farming regions.     

Transmission dynamics of parasitic sea lice from farm to wild salmon

Marine salmon farming has been correlated with parasitic sea lice infestations and concurrent declines of wild salmonids. Here, we report a quantitative analysis of how a single salmon farm altered the natural transmission dynamics of sea lice to juvenile Pacific salmon. We studied infections of sea lice (Lepeophtheirus salmonis and Caligus clemensi) on juvenile pink salmon (Oncorhynchus gorbuscha) and chum salmon (Oncorhynchus keta) as they passed an isolated salmon farm during their seaward migration down two long and narrow corridors. Our calculations suggest the infection pressure imposed by the farm was four orders of magnitude greater than ambient levels, resulting in a maximum infection pressure near the farm that was 73 times greater than ambient levels and exceeded ambient levels for 30 km along the two wild salmon migration corridors. The farm-produced cohort of lice parasitizing the wild juvenile hosts reached reproductive maturity and produced a second generation of lice that re-infected the juvenile salmon. This raises the infection pressure from the farm by an additional order of magnitude, with a composite infection pressure that exceeds ambient levels for 75 km of the two migration routes. Amplified sea lice infestations due to salmon farms are a potential limiting factor to wild salmonid conservation.     

Aquaculture-induced changes to dynamics of a migratory host and specialist parasite: a case study of pink salmon and sea lice

Exchange of diseases between domesticated and wild animals is a rising concern for conservation. In the ocean, many species display life histories that separate juveniles from adults. For pink salmon (Oncorhynchus gorbuscha) and parasitic sea lice (Lepeophtheirus salmonis), infection of juvenile salmon in early marine life occurs near salmon sea-cage aquaculture sites and is associated with declining abundance of wild salmon. Here, we develop a theoretical model for the pink salmon/sea lice host–parasite system and use it to explore the effects of aquaculture hosts, acting as reservoirs, on dynamics. Because pink salmon have a 2-year lifespan, even- and odd-year lineages breed in alternate years in a given river. These lineages can have consistently different relative abundances, a phenomenon termed “line dominance”. These dominance relationships between host lineages serve as a useful probe for the dynamical effects of introducing aquaculture hosts into this host–parasite system. We demonstrate how parasite spillover (farm-to-wild transfer) and spillback (wild-to-farm transfer) with aquaculture hosts can either increase or decrease the line dominance in an affected wild population. The direction of the effect depends on the response of farms to wild-origin infection. If aquaculture parasites are managed to a constant abundance, independent of the intensity of infections from wild to farm, then line dominance increases. On the other hand, if wild-origin parasites on aquaculture hosts are proportionally controlled to their abundance then line dominance decreases.     

Evaluating Relationships between Wild Skeena River Sockeye Salmon Productivity and the Abundance of Spawning Channel Enhanced Sockeye Smolts

The enhancement of salmon populations has long been used to increase the abundance of salmon returning to spawn and/or to be captured in fisheries. However, in some instances enhancement can have adverse impacts on adjacent non-enhanced populations. In Canada''s Skeena watershed, smolt-to-adult survival of Babine Lake sockeye from 1962–2002 was inversely related to the abundance of sockeye smolts leaving Babine Lake. This relationship has led to the concern that Babine Lake smolt production, which is primarily enhanced by spawning channels, may depress wild Skeena (Babine and non-Babine) sockeye populations as a result of increased competition between wild and enhanced sockeye smolts as they leave their natal lakes and co-migrate to sea. To test this hypothesis we used data on Skeena sockeye populations and oceanographic conditions to statistically examine the relationship between Skeena sockeye productivity (adult salmon produced per spawner) and an index of Babine Lake enhanced smolt abundance while accounting for the potential influence of early marine conditions. While we had relatively high power to detect large effects, we did not find support for the hypothesis that the productivity of wild Skeena sockeye is inversely related to the abundance of enhanced sockeye smolts leaving Babine Lake in a given year. Importantly, life-time productivity of Skeena sockeye is only partially explained by marine survival, and likely is an unreliable measure of the influence of smolt abundance. Limitations to our analyses, which include: (1) the reliance upon adult salmon produced per spawner (rather than per smolt) as an index of marine survival, and (2) incomplete age structure for most of the populations considered, highlight uncertainties that should be addressed if understanding relationships between wild and enhanced sockeye is a priority in the Skeena.     

Genomic Resources for Sea Lice: Analysis of ESTs and Mitochondrial Genomes

Sea lice are common parasites of both farmed and wild salmon. Salmon farming constitutes an important economic market in North America, South America, and Northern Europe. Infections with sea lice can result in significant production losses. A compilation of genomic information on different genera of sea lice is an important resource for understanding their biology as well as for the study of population genetics and control strategies. We report on over 150,000 expressed sequence tags (ESTs) from five different species (Pacific Lepeophtheirus salmonis (49,672 new ESTs in addition to 14,994 previously reported ESTs), Atlantic L. salmonis (57,349 ESTs), Caligus clemensi (14,821 ESTs), Caligus rogercresseyi (32,135 ESTs), and Lernaeocera branchialis (16,441 ESTs)). For each species, ESTs were assembled into complete or partial genes and annotated by comparisons to known proteins in public databases. In addition, whole mitochondrial (mt) genome sequences of C. clemensi (13,440 bp) and C. rogercresseyi (13,468 bp) were determined and compared to L. salmonis. Both nuclear and mtDNA genes show very high levels of sequence divergence between these ectoparastic copepods suggesting that the different species of sea lice have been in existence for 37–113 million years and that parasitic association with salmonids is also quite ancient. Our ESTs and mtDNA data provide a novel resource for the study of sea louse biology, population genetics, and control strategies. This genomic information provides the material basis for the development of a 38K sea louse microarray that can be used in conjunction with our existing 44K salmon microarray to study host–parasite interactions at the molecular level. This report represents the largest genomic resource for any copepod species to date.     

The influence of aquaculture unit proximity on the pattern of Lepeophtheirus salmonis infection of anadromous Salmo trutta populations on the isle of Skye,Scotland

A total of 230 anadromous Salmo trutta (brown trout) were sampled in five sheltered coastal fjords (or sea lochs) on the Isle of Skye, Scotland, U.K., in 2016 at varying distances from active Atlantic salmon Salmo salar farms. Statistical models were developed to investigate potential correlations between salmon lice Lepeophtheirus salmonis burdens on S. trutta hosts and their proximity to S. salar farm cages. Significant correlations were found between lice burdens and fish fork length and proximity to the nearest S. salar farm. The probability of the presence of L. salmonis on fish hosts increased with fish host size and with distance from the nearest S. salar farm, but total lice burdens were highest in fish sampled near S. salar farms and decreased with distance. The proportion of different life‐cycle stages of L. salmonis were also dependent on S. salar farm proximity, with higher juvenile lice numbers recorded at sites near S. salar farm cages. These results highlight the complexity of the relationship between S. trutta and L. salmonis infections on wild fish and emphasize the requirement of further research to quantify these effects to better inform conservation and management strategies, particularly in areas of active S. salar farm facilities.     

Juvenile Salmon Usage of the Skeena River Estuary

Migratory salmon transit estuary habitats on their way out to the ocean but this phase of their life cycle is more poorly understood than other phases. The estuaries of large river systems in particular may support many populations and several species of salmon that originate from throughout the upstream river. The Skeena River of British Columbia, Canada, is a large river system with high salmon population- and species-level diversity. The estuary of the Skeena River is under pressure from industrial development, with two gas liquefaction terminals and a potash loading facility in various stages of environmental review processes, providing motivation for understanding the usage of the estuary by juvenile salmon. We conducted a juvenile salmonid sampling program throughout the Skeena River estuary in 2007 and 2013 to investigate the spatial and temporal distribution of different species and populations of salmon. We captured six species of juvenile anadromous salmonids throughout the estuary in both years, and found that areas proposed for development support some of the highest abundances of some species of salmon. Specifically, the highest abundances of sockeye (both years), Chinook in 2007, and coho salmon in 2013 were captured in areas proposed for development. For example, juvenile sockeye salmon were 2–8 times more abundant in the proposed development areas. Genetic stock assignment demonstrated that the Chinook salmon and most of the sockeye salmon that were captured originated from throughout the Skeena watershed, while some sockeye salmon came from the Nass, Stikine, Southeast Alaska, and coastal systems on the northern and central coasts of British Columbia. These fish support extensive commercial, recreational, and First Nations fisheries throughout the Skeena River and beyond. Our results demonstrate that estuary habitats integrate species and population diversity of salmon, and that if proposed development negatively affects the salmon populations that use the estuary, then numerous fisheries would also be negatively affected.     

Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations

Animal migrations can affect disease dynamics. One consequence of migration common to marine fish and invertebrates is migratory allopatry-a period of spatial separation between adult and juvenile hosts, which is caused by host migration and which prevents parasite transmission from adult to juvenile hosts. We studied this characteristic for sea lice (Lepeophtheirus salmonis and Caligus clemensi) and pink salmon (Oncorhynchus gorbuscha) from one of the Canada's largest salmon stocks. Migratory allopatry protects juvenile salmon from L. salmonis for two to three months of early marine life (2-3% prevalence). In contrast, host diversity facilitates access for C. clemensi to juvenile salmon (8-20% prevalence) but infections appear ephemeral. Aquaculture can augment host abundance and diversity and increase parasite exposure of wild juvenile fish. An empirically parametrized model shows high sensitivity of salmon populations to increased L. salmonis exposure, predicting population collapse at one to five motile L. salmonis per juvenile pink salmon. These results characterize parasite threats of salmon aquaculture to wild salmon populations and show how host migration and diversity are important factors affecting parasite transmission in the oceans.     

A three-species model explaining cyclic dominance of Pacific salmon

The four-year oscillations of the number of spawning sockeye salmon (Oncorhynchus nerka) that return to their native stream within the Fraser River basin in Canada are a striking example of population oscillations. The period of the oscillation corresponds to the dominant generation time of these fish. Various—not fully convincing—explanations for these oscillations have been proposed, including stochastic influences, depensatory fishing, or genetic effects. Here, we show that the oscillations can be explained as an attractor of the population dynamics, resulting from a strong resonance near a Neimark Sacker bifurcation. This explains not only the long-term persistence of these oscillations, but also reproduces correctly the empirical sequence of salmon abundance within one period of the oscillations. Furthermore, it explains the observation that these oscillations occur only in sockeye stocks originating from large oligotrophic lakes, and that they are usually not observed in salmon species that have a longer generation time.     

After 100 years: hydroelectric dam-induced life-history divergence and population genetic changes in sockeye salmon (<Emphasis Type="Italic">Oncorhynchus nerka</Emphasis>)

Understanding the impact of barriers and habitat fragmentation on the ecology and genetics of species is of broad interest to many biologists. In aquatic systems, hydroelectric dams often present an impenetrable barrier to migratory fish and can have negative effects on their persistence. Hydroelectric dams constructed in the Coquitlam and Alouette Rivers in the Fraser River drainage (British Columbia, Canada) in the early 1900s were thought to have led to complete loss of anadromous sockeye salmon from both rivers. For both reservoirs, recent water release programs resulted in the unexpected downstream migration of juvenile sockeye salmon and the subsequent upstream migration of adults towards the reservoir 2 years later. Here we investigate the evolutionary impact of dams on the sockeye salmon migration behavior by investigating the genetic distinction between migratory and non-migratory individuals within the Alouette and Coquitlam reservoirs. We also compare historical and contemporary genetic connectivity among 11 Lower Fraser River sockeye sites to infer recent population connectivity changes that might have been influenced by anthropogenic activities. Our molecular genetic analyses show a genetic distinction between the sea-run and resident individuals from the Coquitlam reservoir and population splitting time estimates suggest a very recent divergence between them. These results indicate a genetic component to migration behavior. For our broader survey from 11 sites, our comparisons suggest a general decline in gene flow, with a few interesting exceptions. In summary, our results suggest (i) early stage divergence between life history forms of sockeye salmon within one reservoir, and (ii) recent changes in genetic connectivity among Lower Fraser River populations; both of these results have potential recovery implications for historically migratory populations that were affected by anthropogenic barriers such as hydroelectric dams.     

Does increased abundance of sea lice influence survival of wild Atlantic salmon post‐smolt?

A synthesis of results from two projects was assessed to analyse possible influence of sea lice Lepeophtheirus salmonis on marine Atlantic salmon Salmo salar survival. During the years 1992–2004, trawling for wild migrating post-smolts was performed in Trondheimsfjord, a fjord in which no Atlantic salmon aquaculture activity is permitted. Prevalence and intensity of sea lice infections on migrating wild post-smolts differed between years. A correlation analysis between 1 sea-winter (SW) Atlantic salmon catch statistics from the River Orkla (a Trondheimsfjord river) and sea lice infections on the migrating smolts in the Trondheimsfjord was not significant. Up to 2% reduction in adult returns due to sea-lice infection was expected. In addition, experimental releases from 1996 to 1998 with individually tagged groups of hatchery-reared Atlantic salmon smolts given protection against sea-lice infection was performed. Higher recaptures of adult Atlantic salmon from 1998 treated smolts compared to the control group may correspond to high abundance of sea lice found on the wild smolt, and may indicate influence on post-smolt mortality. These studies indicate that post-smolt mortality in Trondheimsfjord is marginally influenced by sea lice infection; however, the methods for assessing wild smolt mortality might be insufficient. Higher infections of sea lice farther out in the fjord may indicate more loss in Atlantic salmon returns in some years.