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.     

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 model of salmon louse production in Norway: effects of increasing salmon production and public management measures.

Salmon lice Lepeophtheirus salmonis Kr?yer have caused disease problems in farmed Atlantic salmon Salmo salar L. since the mid-1970s in Norway. High infection intensities and premature return of wild sea trout Salmo trutta L. were first reported in 1992. Later emaciated wild Atlantic salmon smolts carrying large amounts of lice have been observed both in fjords and offshore. The Norwegian Animal Health Authority regulations to control the problem, which came into operation in 1998, included compulsory louse level monitoring in farms and maximum legal numbers of lice per fish. Here, we present a model of salmon louse egg production in Norway and show that the effect of the current public management strategy is critically dependent on the yearly increase in salmon production. This is because the infection pressure is the product of the number of fish in the system, and the number of lice per fish. Due to the much larger number of farmed than wild salmonids, it is highly likely that lice originating from farmed salmon infect wild stock. Estimated tolerance limits for wild salmonids vary widely, and the level of louse egg production in farms which would be needed to decimate wild populations is not known. Two possible thresholds for total lice egg production are investigated: (1) 1986 to 1987 level (i.e. before adverse effects on sea trout were recorded), and (2) a level corresponding to a doubling of the estimated natural infection pressure. The farm lice per fish limits that would have to be observed to keep louse production within the 2 thresholds are calculated for the period 1986 to 2005. A steady decrease in the permitted number of lice per fish may keep the total louse production stable, but the number of salmon required for verification of lice numbers will increase as the prevalence to be verified is decreased. At threshold (2), the model estimated that lice limits should have been 0.05 louse per fish in 1999. This would require 60 fish from each pen to be collected, anaesthetised and examined for a good estimate at a confidence level of 95%. Such sample numbers are likely to be opposed by farmers. The use of national delousing programs to solve the problem is discussed.     

Using Agent-Based Modelling to Predict the Role of Wild Refugia in the Evolution of Resistance of Sea Lice to Chemotherapeutants

A major challenge for Atlantic salmon farming in the northern hemisphere is infestation by the sea louse parasite Lepeophtheirus salmonis. The most frequent method of controlling these sea louse infestations is through the use of chemical treatments. However, most major salmon farming areas have observed resistance to common chemotherapeutants. In terrestrial environments, many strategies employed to manage the evolution of resistance involve the use of refugia, where a portion of the population is left untreated to maintain susceptibility. While refugia have not been deliberately used in Atlantic salmon farming, wild salmon populations that migrate close to salmon farms may act as natural refugia. In this paper we describe an agent-based model that explores the influence of different sizes of wild salmon populations on resistance evolution in sea lice on a salmon farm. Using the model, we demonstrate that wild salmon populations can act as refugia that limit the evolution of resistance in the sea louse populations. Additionally, we demonstrate that an increase in the size of the population of wild salmon results in an increased effect in slowing the evolution of resistance. We explore the effect of a population fitness cost associated with resistance, finding that in some cases it substantially reduces the speed of evolution to chemical treatments.     

Sea louse infection of juvenile sockeye salmon in relation to marine salmon farms on Canada's west coast

Background

Pathogens are growing threats to wildlife. The rapid growth of marine salmon farms over the past two decades has increased host abundance for pathogenic sea lice in coastal waters, and wild juvenile salmon swimming past farms are frequently infected with lice. Here we report the first investigation of the potential role of salmon farms in transmitting sea lice to juvenile sockeye salmon (Oncorhynchus nerka).

Methodology/Principal Findings

We used genetic analyses to determine the origin of sockeye from Canada''s two most important salmon rivers, the Fraser and Skeena; Fraser sockeye migrate through a region with salmon farms, and Skeena sockeye do not. We compared lice levels between Fraser and Skeena juvenile sockeye, and within the salmon farm region we compared lice levels on wild fish either before or after migration past farms. We matched the latter data on wild juveniles with sea lice data concurrently gathered on farms. Fraser River sockeye migrating through a region with salmon farms hosted an order of magnitude more sea lice than Skeena River populations, where there are no farms. Lice abundances on juvenile sockeye in the salmon farm region were substantially higher downstream of farms than upstream of farms for the two common species of lice: Caligus clemensi and Lepeophtheirus salmonis, and changes in their proportions between two years matched changes on the fish farms. Mixed-effects models show that position relative to salmon farms best explained C. clemensi abundance on sockeye, while migration year combined with position relative to salmon farms and temperature was one of two top models to explain L. salmonis abundance.

Conclusions/Significance

This is the first study to demonstrate a potential role of salmon farms in sea lice transmission to juvenile sockeye salmon during their critical early marine migration. Moreover, it demonstrates a major migration corridor past farms for sockeye that originated in the Fraser River, a complex of populations that are the subject of conservation concern.     

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.     

Increased susceptibility of Atlantic salmon Salmo salar to infections with Gyrodactylus derjavini induced by dexamethasone bath treatment

Dexamethasone, a known immunosuppressant, was administered by bath or injection to Atlantic salmon Salmo salar (Conon stock) to study if this treatment could affect the susceptibility of fish to infections with a Danish strain of Gyrodactylus derjavini (Monogenea). Three groups of S. salar (Conon stock) were immersion treated either with 10, 60 or 240 microg dexamethasone l-1 water, respectively. In addition, one group (positive control) was treated intraperitoneally with 200 microg dexamethasone per fish and one negative control group was kept untreated. A single G. derjavini parasite was placed on the anal fin of each fish and the infection was subsequently monitored weekly for 6 weeks. An increase in parasite populations on the salmon was positively correlated with the amount of immunosuppressant used. Infection levels in the group immersion treated with dexamethasone (240 microg l-1 water) and in the i.p. treated positive control group were significantly higher compared to the untreated control group.     

Allee effects may slow the spread of parasites in a coastal marine ecosystem

Allee effects are thought to mediate the dynamics of population colonization, particularly for invasive species. However, Allee effects acting on parasites have rarely been considered in the analogous process of infectious disease establishment and spread. We studied the colonization of uninfected wild juvenile Pacific salmon populations by ectoparasitic salmon lice (Lepeophtheirus salmonis) over a 4-year period. In a data set of 68,376 fish, we observed 85 occurrences of precopular pair formation among 1,259 preadult female and 613 adult male lice. The probability of pair formation was dependent on the local abundance of lice, but this mate limitation is likely offset somewhat by mate-searching dispersal of males among host fish. A mathematical model of macroparasite population dynamics that incorporates the empirical results suggests a high likelihood of a demographic Allee effect, which can cause the colonizing parasite populations to die out. These results may provide the first empirical evidence for Allee effects in a macroparasite. Furthermore, the data give a rare detailed view of Allee effects in colonization dynamics and suggest that Allee effects may dampen the spread of parasites in a coastal marine ecosystem.     

Disease interaction between farmed and wild fish populations

This paper reviews the literature on disease interaction between wild and farmed fish and recommends strategies to reduce the disease risks to both populations. Most, if not all, diseases of farmed fish originate in wild populations. The close contact between farmed and wild fish readily leads to pathogens exchange. Aquaculture creates conditions ( e.g. high stocking levels) conducive to pathogen transmission and disease; hence pathogens can overspill back, resulting in high levels of challenge to wild populations. This is exemplified by sea lice infections in farmed Atlantic salmon. Stocking with hatchery reared fish or aquaculture escapees can affect disease dynamics in wild populations. Whirling disease has been spread to many wild rainbow trout populations in the US with the release of hatchery reared stock. The greatest impact of aquaculture on disease in wild populations has resulted from the movement of fish for cultivation. Examples of exotic disease introduction following movement of live fish for aquaculture with serious consequences for wild populations are reviewed. The salmon parasite, Gyrodactylus salaris, has destroyed wild salmon populations in 44 Norwegian rivers. Crayfish plague has wiped out European crayfish over much of Europe. Eels numbers have declined in Europe and infection with the swimbladder nematode Anguillicola crassus has in part been blamed. The impact of disease in farmed fish on wild populations can mitigated. Risk analysis methods need to be refined and applied to live fish movement and new aquacultural developments. Appropriate biosecurity strategies, based on risk assessments, should be developed to reduce pathogen exchange and mitigate the consequences.     

Evolution of virulence under intensive farming: salmon lice increase skin lesions and reduce host growth in salmon farms

Parasites rely on resources from a host and are selected to achieve an optimal combination of transmission and virulence. Human‐induced changes in parasite ecology, such as intensive farming of hosts, might not only favour increased parasite abundances, but also alter the selection acting on parasites and lead to life‐history evolution. The trade‐off between transmission and virulence could be affected by intensive farming practices such as high host density and the use of antiparasitic drugs, which might lead to increased virulence in some host–parasite systems. To test this, we therefore infected Atlantic salmon (Salmo salar) smolts with salmon lice (Lepeophtheirus salmonis) sampled either from wild or farmed hosts in a laboratory experiment. We compared growth and skin damage (i.e. proxies for virulence) of hosts infected with either wild or farmed lice and found that, compared to lice sampled from wild hosts in unfarmed areas, those originating from farmed fish were more harmful; they inflicted more skin damage to their hosts and reduced relative host weight gain to a greater extent. We advocate that more evolutionary studies should be carried out using farmed animals as study species, given the current increase in intensive food production practices that might be compared to a global experiment in parasite evolution.     

Temporal and spatial patterns of sea lice levels on sea trout in western Scotland in relation to fish farm production cycles

The relationship between aquaculture and infestations of sea lice on wild sea trout (Salmo trutta) populations is controversial. Although some authors have concluded that there is a link between aquaculture and lice burdens on wild fish, others have questioned this interpretation. Lice levels have been shown to be generally higher on Atlantic salmon farms during the second years of two-year production cycles. Here we investigate whether this pattern relates to lice burdens on wild fish across broad temporal and spatial axes. Within Loch Shieldaig across five successive farm cycles from 2000 to 2009, the percentage of sea trout with lice, and those above a critical level, were significantly higher in the second year of a two-year production cycle. These patterns were mirrored in 2002–2003 across the Scottish west coast. The results suggest a link between Atlantic salmon farms and sea lice burdens on sea trout in the west of Scotland.     

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.     

Some consequences of Pacific salmon hatchery production in Kamchatka: changes in age structure and contributions to natural spawning populations

Aggregate hatchery production of Pacific salmon in the Kamchatka region of the Russian Federation is very low (< 0.5% of total harvest, with five hatcheries releasing approximately 41 M juvenile salmon annually), but contributions in certain rivers can be substantial. Enhancement programs in these rivers may strongly influence fitness and production of wild salmon. In this paper we document significant divergence in demographic traits in hatchery salmon populations in the Bolshaya River and we estimate the proportion of hatchery chum salmon in the total run in the Paratunka River to demonstrate the magnitude of enhancement in this system. We observed a reduction in the expression of life history types in hatchery populations (ranging from 1 to 9 types) compared to wild populations (17 types) of sockeye salmon in the Bolshaya River. We found similar trends in Chinook salmon in the same river system. This reduced life history diversity may make these fish less resilient to changes in habitat and climate. We estimate hatchery chum salmon currently contribute 17-45% to the natural spawning population in the Paratunka River. As hatchery fish increase in numbers at natural spawning sites, this hatchery production may affect wild salmon production. It is important to investigate the risk of introgression between hatchery and wild salmon that can lead to reduction in salmon fitness in Kamchatka rivers, as well as the potential of ecological interactions that can have consequences on status of wild salmon and overall salmon production in this region.     

Identifying ‘firebreaks’ to fragment dispersal networks of a marine parasite

Marine ecosystems are beset by disease outbreaks, and efficient strategies to control dispersal of pathogens are scarce. We tested whether introducing no-farming areas or ‘firebreaks’ could disconnect dispersal networks of a parasitic disease affecting the world’s largest marine fish farming industry (～1000 farms). Larval salmon lice (Lepeophtheirus salmonis) are released from and transported among salmon farms by ocean currents, creating inter-farm networks of louse dispersal. We used a state-of-the-art biophysical model to predict louse movement along the Norwegian coastline and network analysis to identify firebreaks to dispersal. At least one firebreak that fragmented the network into two large unconnected groups of farms was identified for all seasons. During spring, when wild salmon migrate out into the ocean, and louse levels per fish at farms must be minimised, two effective firebreaks were created by removing 13 and 21 farms (1.3% and 2.2% of all farms in the system) at ～61°N and 67°N, respectively. We have demonstrated that dispersal models coupled with network analysis can identify no-farming zones that fragment dispersal networks. Reduced dispersal pathways should lower infection pressure at farms, slow the evolution of resistance to parasite control measures, and alleviate infection pressure on wild salmon populations.     

Application of genome editing in aquatic farm animals: Atlantic salmon

Gene editing offers opportunities to solve fish farming sustainability issues that presently hampers expansion of the aquaculture industry. In for example Atlantic salmon farming, there are now two major bottlenecks limiting the expansion of the industry. One is the genetic impact of escaped farmed salmon on wild populations, which is considered the most long-term negative effect on the environment. Secondly and the utmost acute problem is the fish parasite salmon lice, which is currently causing high lethality in wild salmonids due to high concentrations of the parasite in the sea owing to sea cage salmon farming. There are also sustainability issues associated with increased use of vegetable-based ingredients as replacements for marine products in fish feed. This transition comes at the expense of the omega-3 content both in fish feed and the fish filet of the farmed fish. Reduced fish welfare represents another obstacle, and robust farmed fish is needed to avoid negative stress associated phenotypes such as cataract, bone and fin deformities, precocious maturity and higher disease susceptibility. Gene editing could solve some of these problems as genetic traits can be altered positively to reach phenotype of interest such as for example disease resistance and increased omega-3 production.

     

Assessing introgression of foreign strains in wild Atlantic salmon populations: variation in microsatellites assessed in historic scale collections

1. Genetic variation at five microsatellite loci was analysed in a collection of scales (1970–97) sampled from Atlantic salmon adults returning to the Nivelle River (South France).
2. Native and foreign fish (from an allochthonous Scottish stock introduced into the river to increase population size) were clearly identified as all foreign individuals released in the river were physically marked.
3. Introgression of foreign genes into the native gene pool has occurred, although the reproductive success of foreign Atlantic salmon in the wild was lower than that of native individuals.
4. The utility of old scale samples for investigating the impact of foreign stocking on wild fish populations is demonstrated in this work.     

The physiological effects of salmon lice infection on post-smolt of Atlantic salmon

The physiological effects of salmon lice infections on post-smolt of Atlantic salmon were examined by experimentally infecting hatchery reared post-smolts with infective copepodids. Even at high infection intensities, ranging from 30–250 lice per fish, early chalimus stages did not have severe, physiological effects on the fish. There was a sudden increase in fish mortality after the appearance of preadult I stages. Infected fish were then suffering due to lesions and osmoregulatory failure. Plasma chloride level increased significantly and total protein, albumin and haematocrit decreased significantly in infected compared to uninfected fish. All infected fish became moribund before adult lice appeared. Infection intensities above 30 salmon lice larvae per fish thus appear to cause death of Atlantic salmon post-smolt soon after the lice reach their pre-adult stage.     

Distribution and abundance of the salmonid parasite Parvicapsula minibicornis (Myxozoa) in the Klamath River basin (Oregon-California, U.S.A.)

The distribution and abundance of the myxosporean parasite Parvicapsula minibicornis in the Klamath River mirrored that of Ceratomyxa shasta, with which it shares both its vertebrate and invertebrate host. Assay of fish held at sentinel sites and water samples collected from those sites showed that parasite prevalence was highest below Iron Gate dam, which is the barrier to anadromous salmon passage. Above this barrier parasite levels fluctuated, with the parasite detected in the free-flowing river reaches between reservoirs. This was consistent with infection prevalence in the polychaete host, Manayunkia speciosa, which was greater than 1% only in populations tested below Iron Gate dam. Although a low prevalence of infection was detected in juvenile out-migrant fish in the Trinity River, the tributaries tested did not appear to be a significant source of the parasite to the mainstem despite the presence of large numbers of infected adult salmon that migrate and spawn there. Rainbow trout became infected during sentinel exposure, which expands the host range for P. minibicornis and suggests that wild rainbow trout populations are a reservoir for infection, especially above Iron Gate dam. High parasite prevalence in the lower Klamath River is likely a combined effect of high spore input from heavily infected, spawned adult salmon and the proximity to dense populations of polychaetes.     

The road to extinction is paved with good intentions: negative association of fish hatcheries with threatened salmon

Hatchery programmes for supplementing depleted populations of fish are undergoing a worldwide expansion and have provoked concern about their ramifications for populations of wild fish. In particular, Pacific salmon are artificially propagated in enormous numbers in order to compensate for numerous human insults to their populations, yet the ecological impacts of this massive hatchery effort are poorly understood. Here we test the hypothesis that massive numbers of hatchery-raised chinook salmon reduce the marine survival of wild Snake River spring chinook, a threatened species in the USA. Based on a unique 25-year time-series, we demonstrated a strong, negative relationship between the survival of chinook salmon and the number of hatchery fish released, particularly during years of poor ocean conditions. Our results suggest that hatchery programmes that produce increasingly higher numbers of fish may hinder the recovery of depleted wild populations.     

Lessons from sea louse and salmon epidemiology

Effective disease management can benefit from mathematical models that identify drivers of epidemiological change and guide decision-making. This is well illustrated in the host–parasite system of sea lice and salmon, which has been modelled extensively due to the economic costs associated with sea louse infections on salmon farms and the conservation concerns associated with sea louse infections on wild salmon. Consequently, a rich modelling literature devoted to sea louse and salmon epidemiology has been developed. We provide a synthesis of the mathematical and statistical models that have been used to study the epidemiology of sea lice and salmon. These studies span both conceptual and tactical models to quantify the effects of infections on host populations and communities, describe and predict patterns of transmission and dispersal, and guide evidence-based management of wild and farmed salmon. As aquaculture production continues to increase, advances made in modelling sea louse and salmon epidemiology should inform the sustainable management of marine resources.