Ecology of sea lice parasitic on farmed and wild fish

Sea lice, especially Lepeophtheirus salmonis and Caligus spp., have the greatest economic impact of any parasite in salmonid fish farming and are also a threat to wild salmonids. Here, I review how the biology and ecology of various louse and host species influence their pathogenicity and epidemiology. Recent discoveries of new species and genotypes emphasize the need for more basic research on louse taxonomy and host preferences. Louse development rates are strongly dependent on temperature, and increasing mean sea temperatures are likely to increase infestation pressure on farms and wild fish, as well as affecting the geographical distribution of hosts and parasites. Despite progress in finding L. salmonis larvae in the plankton and in modelling louse production in several countries, more data on larval behaviour and distribution are required to develop dispersal and transmission models for both L. salmonis and Caligus spp. This knowledge could be used to take measures to reduce the risks of lice affecting farmed and wild fish.     

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.     

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.     

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.     

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.     

Physiological impact of sea lice on swimming performance of Atlantic salmon

Atlantic salmon Salmo salar were infected with two levels of sea lice Lepeophtheirus salmonis (0·13 ± 0·02 and 0·02 ± 0·00 sea lice g⁻¹). Once sea lice became adults, the ventral aorta of each fish was fitted with a Doppler cuff to measure cardiac output ( ̇ ), heart rate ( f _H) and stroke volume ( V _S) during swimming. Critical swimming speeds ( U _crit) of fish with higher sea lice numbers [2·1 ± 0·1 BL (body lengths) s⁻¹] were significantly lower ( P  < 0·05) than fish with lower numbers (2·4 ± 0·1 BL s⁻¹) and controls (sham infected, 2·6 ± 0·1 BL s⁻¹). After swimming, chloride levels in fish with higher sea lice numbers (184·4 ± 11·3 mmol l⁻¹) increased significantly (54%) from levels at rest and were significantly higher than fish with fewer lice (142·0 ± 3·7 mmol l⁻¹) or control fish (159·5 ± 3·5 mmol l⁻¹). The f _H of fish with more lice was 9% slower than the other two groups at U _crit. This decrease resulted in ̇ not increasing from resting levels. Sublethal infection by sea lice compromised the overall fitness of Atlantic salmon. The level of sea lice infection used in the present study was lower than has previously been reported to be detrimental to wild Atlantic salmon.     

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.     

Randomized clinical trial to investigate the effectiveness of teflubenzuron for treating sea lice on Atlantic salmon

A double-blind, randomized control clinical trial was performed to investigate the effectiveness of teflubenzuron in controlling sea lice Lepeophtheirus salmonis on farmed Atlantic salmon Salmo salar. A total of 40 sea cages from 3 commercial cage sites in Atlantic Canada were used in this Good Clinical Practice (GCP) trial. The teflubenzuron was administered in the feed at a dosage of 10 mg kg(-1) biomass d(-1) for 7 d. Medicated and control cages were matched by site, cage size, and pre-treatment mean lice counts using cages as the unit of concern. Post-treatment lice counts and staging of developmental stages were performed at 1 and 2 wk after the end of treatment. Chalimus stages in medicated cages were significantly lower than in control cages at 1 wk (79% reduction in mean lice counts, p < 0.001), and at 2 wk (53% reduction, p < 0.001). Mobile (pre-adult and adult) stages were also significantly reduced in medicated cages at 1 wk (69% reduction, p < 0.01), and at 2 wk (40% reduction, p < 0.01) post-treatment, respectively. Teflubenzuron was proven effective for reducing lice burdens on salmon despite the low parasite levels experienced during the trial and the recruitment of lice from the untreated cages. The use of cage as the unit of concern was an important design component of this trial.     

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.     

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.     

Effects of salmon lice infection and salmon lice protection on fjord migrating Atlantic salmon and brown trout post-smolts

Effects of artificial salmon lice infection and pharmaceutical salmon lice prophylaxis on survival and rate of progression of Atlantic salmon (n = 72) and brown trout post-smolts (n = 72) during their fjord migration, were studied by telemetry. The infected groups were artificially exposed to infective salmon lice larvae in the laboratory immediately before release in the inner part of the fjord to simulate a naturally high infection pressure. Groups of infected Atlantic salmon (n = 20) and brown trout (n = 12) were also retained in the hatchery to control the infection intensity and lice development during the study period. Neither salmon lice infection nor pharmaceutical prophylaxis had any effects on survival and rate of progression of fjord migrating Atlantic salmon post-smolts compared to control fish. Atlantic salmon spent on average only 151.2 h (maximum 207.3 h) in passing the 80 km fjord system and had, thus, entered the ocean when the more pathogenic pre-adult and adult lice stages developed. The brown trout, in comparison to Atlantic salmon, remained to a larger extent than Atlantic salmon in the inner part of the fjord system. No effect of salmon lice infection, or protection, was found in brown trout during the first weeks of their fjord migration. Brown trout will, to a larger extent than Atlantic salmon, stay in the fjord areas when salmon lice infections reach the more pathogenic pre-adult and adult stages. In contrast to Atlantic salmon, they will thereby possess the practical capability of returning to freshwater when encountering severe salmon lice attacks.     

Historical control clinical trial to assess the effectiveness of teflubenzuron for treating sea lice on Atlantic salmon

A historical control clinical trial was performed to assess the effectiveness of teflubenzuron in controlling sea lice Lepeoptheirus salmonis burdens on farmed Atlantic salmon Salmo salar over time. The study site comprised 9 sea cages, all of which were treated. The teflubenzuron was administered in the feed, at a dosage of 10 mg kg(-1) biomass d(-1), over a treatment period of 7 d. At 1 wk post-treatment, sea lice chalimus and mobile stages were reduced by 92 and 74% (both p < 0.001), respectively. At 2 wk post-treatment, chalimus stages were reduced by 41% and mobile stages 61% (both p < 0.001) compared to pre-treatment levels. At 3 wk post-treatment, chalimus stages were still 36% (p < 0.001) lower than pre-treatment levels, but mobile stages had increased to above pre-treatment levels. Our results show that the effects of teflubenzuron are limited to a 3 wk duration, but that with appropriate management, farms could benefit from these reduced lice burdens for longer periods.     

Commercial trials using emamectin benzoate to control sea lice Lepeophtheirus salmonis infestations in Atlantic salmon Salmo salar

Two trials were conducted at commercial salmon farms to evaluate the efficacy of emamectin benzoate (Slice, 0.2% aquaculture pre-mix, Schering-Plough Animal Health) as a treatment for sea lice Lepeophtheirus salmonis (Kr?yer) and Caligus elongatus Nordmann infestations in Atlantic salmon Salmo salar L. Trials were carried out in 15 m2 commercial sea pens, at temperatures of 5.5 to 7.5 degrees C and 10.8 to 13.8 degrees C. Each pen was stocked with 14,000 to 17,500 fish with mean weights of 0.44 to 0.74 and 1.33 to 1.83 kg. Fish were naturally infested with sea lice at the start of each trial. At Day -1, samples of 10 or 15 fish were taken from each pen to determine pre-treatment numbers of lice. Emamectin benzoate was administered in feed, to 4 replicate pens, at a dose of 50 micrograms kg-1 biomass d-1 for 7 consecutive days (Days 0 to 6). Sea lice were counted again, between Days 7 and 77, and comparisons made with untreated control fish. Despite adverse weather conditions, wide variations in fish weights and exposure to new infestations, treatment was effective against chalimus and motile stages of L. salmonis. In the autumn trial, efficacy at Day 27 was 89%, and lice numbers remained lower on treated fish than on control fish 64 d from the start of treatment. In the winter trial, reductions in lice numbers at low temperatures were slower but good efficacy was achieved by Day 35. Although control fish had to be treated with hydrogen peroxide at Day 21, fish treated only with emamectin benzoate on Days 0 to 6 still had 89% fewer lice than control fish at Day 35. There were very few C. elongatus present, but at the end of both trials numbers were lower on treated fish. No adverse effects were associated with treatment of fish with emamectin benzoate.     

Mathematical model ofLaminaria production near a British Columbian salmon sea cage farm

The technical and economical feasibility of farmingLaminaria saccharina for a food base product near a salmon sea cage farm was evaluated. Suitability of kelp for nutrient removal was also analyzed. A computer model of a conceptualized system was developed in order to make the assessments. Kelp growth was modelled as a linear function of temperature and background dissolved inorganic nitrogen concentration, and it was partially experimentally validated. Based on model simulations, aLaminaria farm containing 10,60 m ropes on each end of a salmon sea cage farm is fertilized by the salmon farm and yields annually 1600 kg of dried kelp. The payback period for the initial investment of $61 × 10³ is 6 years after which an annual net profit of 20 × 10³ Canadian dollars ($16.68 × 10³ US) can be achieved. The net present worth of the kelp farm was positive for a rate of return up to 25%. Kelp production on multiple salmon farms or at a higher kelp density could increase the overall revenue.The kelp farm does not appreciably affect background nutrient or oxygen levels. With a few modifications in the model,Nereocystis andMacrocystis farming can be substituted and evaluated for feasibility and nutrient removal efficiency.     

Susceptibility of rainbow trout Oncorhynchus mykiss,Atlantic salmon Salmo salar and coho salmon Oncorhynchus kisutch to experimental infection with sea lice Lepeophtheirus salmonis

Physiological, immunological and biochemical parameters of blood and mucus, as well as skin histology, were compared in 3 salmonid species (rainbow trout Oncorhynchus mykiss, Atlantic salmon Salmo salar and coho salmon O. kisutch) following experimental infection with sea lice Lepeophtheirus salmonis. The 3 salmonid species were cohabited in order to standardize initial infection conditions. Lice density was significantly reduced on coho salmon within 7 to 14 d, while lice persisted in higher numbers on rainbow trout and Atlantic salmon. Lice matured more slowly on coho salmon than on the other 2 species, and maturation was slightly slower on rainbow trout than on Atlantic salmon. Head kidney macrophages from infected Atlantic salmon had diminished respiratory burst and phagocytic capacity at 14 and 21 d post-infection (dpi), while infected rainbow trout macrophages had reduced respiratory burst and phagocytic capacities at 21 dpi, compared to controls. The slower development of lice, coupled with delayed suppression of immune parameters, suggests that rainbow trout are slightly more resistant to lice than Atlantic salmon. Infected rainbow trout and Atlantic salmon showed increases in mucus lysozyme activities at 1 dpi, which decreased over the rest of the study. Mucus lysozyme activities of infected rainbow trout, however, remained higher than controls over the entire period. Coho salmon lysozyme activities did not increase in infected fish until 21 dpi. Mucus alkaline phosphatase levels were also higher in infected Atlantic salmon compared to controls at 3 and 21 dpi. Low molecular weight (LMW) proteases increased in infected rainbow trout and Atlantic salmon between 14 and 21 dpi. Histological analysis of the outer epithelium revealed mucus cell hypertrophy in rainbow trout and Atlantic salmon following infection. Plasma cortisol, glucose, electrolyte and protein concentrations and hematocrit all remained within physiological limits for each species, with no differences occurring between infected and control fish. Our results demonstrate that significant differences in mucus biochemistry and numbers of L. salmonis occur between these species.     

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.     

The chemical cues of male sea lice Lepeophtheirus salmonis encourage others to move between host Atlantic salmon Salmo salar

Adult male sea lice Lepeophtheirus salmonis were more likely to leave host fish Atlantic salmon Salmo salar if they detected the chemical cues of other adult male lice than if they detect cues of female lice. The detection of both male and female chemical cues yielded an intermediate response. These results suggest that males use chemical cues to balance competition for resources and mate acquisition, and they highlight the need for further studies of the chemical ecology of this important parasite.     

Ammonium and nitrate uptake by Laminaria saccharina and Nereocystis luetkeana originating from a salmon sea cage farm

In the laboratory, ammonium and nitrate uptakes were measured for juvenile Laminaria saccharina (L.) Lamour. and Nereocystis luetkeana (Mert.) Post. et Rupr. originating from a salmon sea cage farm in northwestern British Columbia, Canada. The effect of various concentrations of NH4+ and NO3-, which are typical of salmon farming environments, on uptakes values were examined. Both L. saccharina and Nereocystis revealed simultaneous uptake of NH4+ and NO3- when both NH4+ and NO3- were present in the medium. During a 3-h incubation, mean uptake rates of NH4+ and NO3- by L. saccharina ranged from 6.0–8.9 and 4.6–10.6 μmol gdw-1 h-1, respectively, and by Nereocystis, they ranged from 6.6–9.3 μmol gdw-1 h-1 and 6.1–17.0 μmol gdw-1 h-1, respectively. The highest uptake rates (14.8 μmol NH4+ gdw-1 h-1by L. saccharina and 27.2 μmol NO3- gdw-1 h-1 by Nereocystis) occurred at the highest concentration (40 μM NH4+ plus 30 μM NO3-) during a 1 h incubation. Nitrate uptake by both L. saccharina and Nereocystis increased linearly up to the highest nitrate level tested (30 μM), whereas uptake rates of ammonium were stable beyond 10 μM NH4+ to reach approximately 10 and 13 μmol gdw-1 h-1, respectively, for L. saccharina and Nereocystis. Unlike L. saccharina, Nereocystis showed a significant preference for NO3- when more than 20 μM NO3- was present in the medium ( p <0.05). Both L. saccharina and Nereocystis would be suitable for integrated cultivation of salmon/kelp. This revised version was published online in June 2006 with corrections to the Cover Date.     

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.