A review of host finding behaviour in the parasitic sea louse, Lepeophtheirus salmonis (Caligidae: Copepoda)

Ectoparasitic sea lice are the most important parasite problem to date for the salmon farming industry in the northern and southern hemispheres. An understanding of host location in the specialist species, Lepeophtheirus salmonis , the most important louse species in the North Atlantic, is now being realized using behavioural in vitro and in vivo bioassays coupled with chemical analysis of fish conditioned waters. Both physical and chemical cues are important in host location. Responses of sea lice to physical cues such as light and salinity may enable them to gather in areas where host fish are likely to be found. Mechanoreception is an important sensory modality in host location and acts by switching on specific behaviours that enable landing on a fish. Chemoreception plays a defining role in host location and recognition. The detection of host kairomones switches on 'host search' behavioural patterns and also induces landing responses whereas non-host kairomones fail to induce attraction or significant landing behaviour. Semiochemicals derived from salmon and also non-host fish have been identified, and may prove useful for the development of integrated pest management strategies, by the introduction of odour traps for monitoring lice numbers, and by the use of stimulo-deterrent diversionary (push:pull) strategies in their control.     

Investigations on the role of the salmon louse,Lepeophtheirus salmonis (Caligidae), as a vector in the transmission of Aeromonas salmonicida subsp. salmonicida

A bacteria–parasite challenge model was used to study the role of sea lice, Lepeophtheirus salmonis (Copepoda), as a vector of Aeromonas salmonicida subsp. salmonicida. Three hypotheses were tested: (i) L. salmonis can acquire A. salmonicida subsp. salmonicida via water bath exposure; (ii) L. salmonis can acquire the bacteria via parasitizing infected Atlantic salmon, Salmo salar; and (iii) L. salmonis can transmit the bacteria to naïve Atlantic salmon via parasitism. Adult L. salmonis exposed to varying A. salmonicida subsp. salmonicida suspensions (10¹–10⁷ cells mL^?1) for 1.0, 3.0 or 6.0 h acquired the bacteria externally (12.5–100%) and internally (10.0–100%), with higher prevalences associated with the highest concentrations and exposures. After exposure to 10⁷ cells mL^?1, viable A. salmonicida subsp. salmonicida could be isolated from the external carapace of L. salmonis for 120 h. Lepeophtheirus salmonis also acquired the bacteria externally and internally from parasitizing infected fish. Bacterial transmission was observed only when L. salmonis had acquired the pathogen internally via feeding on ‘donor fish’ and then by parasitizing smaller (<50 g) ‘naive’ fish. Under specific experimental conditions, L. salmonis can transfer A. salmonicida subsp. salmonicida via parasitism; however, its role as a mechanical or biological vector was not defined.     

Genetic characterization of populations of the ectoparasitic caligid, Lepeophtheirus salmonis (Krøyer 1837) using randomly amplified polymorphic DNA

Genetic variability within salmon louse, Lepeophtheirus salmonis (Caligidae: Copepoda), populations parasitizing farmed and wild Scottish Atlantic salmon (Salmo salar) was investigated using analysis of randomly amplified polymorphic DNA (RAPD) fragments. Seven individual decamer primers were used to analyse samples of salmon lice collected from 15 different locations in Scotland. The polymerase chain reaction products were separated using agarose gel electrophoresis and the resulting band patterns were analysed using a semi‐automated analytical scoring system. Dendrograms were produced using the unweighted pair‐group average (UPGMA) method using Dice similarity values. The summary dendrogram of the analysis of all RAPD bands showed two separate clusters of salmon lice, the larger being sub‐divided into a further two sections. The collections of lice occupying each of these sub‐divisions, however, were a mix of sites, which did not exhibit a structured geographical pattern.     

Development of microsatellite PCR typing methodology for the sea louse, Lepeophtheirus salmonis (Krøyer)

In order to develop a microsatellite typing system for Lepeophtheirus salmonis (Krøyer), a DNA preparation method for individual sea lice suitable for analysis by polymerase chain reaction (PCR) was designed, and the DNA sequences of 50 L. salmonis microsatellite elements were determined. The microsatellites were composed of 60% perfect, 25% imperfect, and 15% compound repeats. Based on the flanking DNA sequences, four microsatellite‐PCR assays were optimized and used in a pilot study to analyse L. salmonis samples collected in Ireland, Norway and Scotland. Two of the microsatellite‐PCR assays targeted polymorphic loci amplifying seven and 10 alleles respectively. The results showed that microsatellite‐PCR typing could detect genetic variation both within and between the L. salmonis groups, and also was capable of amplifying group‐specific alleles.     

The settlement and reproductive success of Lepeophtheirus salmonis (Krøyer 1837; Copepoda: Caligidae) on atypical hosts

The reproductive success of Lepeophtheirus salmonis settled on host and non‐host fish has been compared. Triplicate single species tanks of Atlantic salmon, marine three‐spined sticklebacks, saithe and Atlantic cod were exposed to 10 adult female L. salmonis per tank (n=30 lice per species). Adult female L. salmonis settlement and egg string production occurred only on salmon and cod, with no egg production occurring on saithe and three‐spined sticklebacks. The number of eggs in egg strings, hatching success of eggs and the survival of all larval stages to the copepodid stage were severely affected by the species of fish on which female L. salmonis had settled. L. salmonis settled on cod produced significantly fewer eggs, lower hatching rates and lower survival rates of larvae than females on Atlantic salmon. The production of egg strings by L. salmonis females infecting cod, which successfully hatch and moult through to the infective copepodid stage, albeit in small numbers, is discussed in terms of the implications to aquaculture and salmon and cod farming scenarios.     

Distributions of planktonic sea lice larvae Lepeophtheirus salmonis in the inter-tidal zone in Loch Torridon, Western Scotland in relation to salmon farm production cycles

This study examines the relative density of sea lice, Lepeophtheirus salmonis (Krøyer), larvae in the inter‐tidal areas of Loch Torridon, a fjordic sea loch in Western Scotland and the site of several commercial salmon farms. Samples of planktonic sea lice were collected in each spring from 1999 to 2003 near the mouth of the River Shieldaig, where sea trout have been shown to congregate in the first few days after going to sea, and from 2001 to 2003 near the mouth of the River Balgy. No larval sea lice were found near the mouth of the River Shieldaig in spring 2000 or 2002, when gravid female sea lice were absent on local fish farms. The same finding was observed in 2002 at the mouth of the River Balgy. In springs of 1999, 2001 and 2003, peak densities of larval sea lice of 33, 94 and 143 m^?3, respectively, were observed at the mouth of the river Shieldaig. At the mouth of the River Balgy, peak densities of 74 and 78 lice m^?3 were observed in 2001 and 2003 respectively. At the time these samples were collected, the two local salmon farms were in the second year of their production cycle and gravid female sea lice were present. Samples of larval sea lice were also obtained year round, at approximately weekly intervals, from a 50‐m transect at the mouth of the River Shieldaig, from March 2001 to June 2003, and compared with frequencies of gravid female sea lice on the two local salmon farms. High levels were found in the winter. No planktonic sea lice were found in this transect when gravid females were not present on the local fish farms.     

The Three‐spined Stickleback,Gasterosteus aculeatus Linnaeus 1758, plays a minor role as a host of Lepeophtheirus salmonis (Krøyer 1837) in the Gulf of Maine

The sea louse, Lepeophtheirus salmonis (Krøyer 1837), is a significant parasite of farmed salmon throughout the Northern Hemisphere. Management of on‐farm louse populations can be improved by understanding the role that wild fish play in sustaining and providing refuge for the local population of sea lice. In this study, 1,064 sticklebacks were captured. Of these animals, 176 individuals were carrying a total of 238 sea lice, yielding a prevalence and intensity of 16.5% and 1.4 lice per fish, respectively. Detailed examination of the sea lice on the three‐spined sticklebacks captured in Cobscook Bay found two L. salmonis individuals using three‐spined sticklebacks as hosts. A 2012 survey of wild fish in Cobscook Bay, Maine, found multiple wild hosts for Caligus elongatus (von Nordmann 1832), including three‐spined sticklebacks (Gasterosteus aculeatus L.), but no L. salmonis were found in this earlier study.     

A review of the use of ivermectin as a treatment for sea lice [Lepeophtheirus salmonis (Krøyer) and Caligus elongatus Nordmann] infestation in farmed Atlantic salmon (Salmo salar L.)

Ectoparasitic sea lice, Lepeophtheirus salmonis (Krøyer) and Caligus elongatus (Nordmann) browse on the skin of farmed Atlantic salmon, Salmo salar L.. The resulting lesions cause stress and increase the susceptibility of the fish to secondary infections. In extreme infestations, fish can suffer from osmoregulatory failure and death. The most immediate treatment for the relief of sea lice infestations at fish farms is the use of chemotherapeutants, either by bath or oral administration. One compound which has been investigated for use as a chemotherapeutant is ivermectin. Ivermectin is a member of the avermectin group of macrocyclic lactones. The avermectins are neurotoxins, which have been used successfully in the treatment of helminthic parasitic infections in a number of terrestrial farm animals and also in the treatment of river blindness in humans. Owing to the low solubility of the compound, ivermectin has been administered as an oral treatment with the feed and has been found to be effective for the treatment of sea lice on Atlantic salmon. Ivermectin is poorly absorbed by fish with a high percentage of the administered dose being excreted in the faeces. The highest concentrations of the absorbed ivermectin were found in lipid‐rich organs. The ivermectin remained in the tissues of the treated fish for a prolonged period of time and was excreted mainly in the unchanged form. Ivermectin can reach the marine environment via excretion from the bile, unabsorbed via the fish faeces and by uneaten food pellets and has a strong affinity to lipid, soil and organic matter. Risk assessments have shown that ivermectin is likely to accumulate in the sediments and that the species therein would be more at risk than the species in the pelagic environment. Ivermectin has been shown to be toxic to some benthic infaunal species in single species tests, but there is no evidence that treatment of fish with ivermectin has affected multispecies benthic communities in the field situation. This review paper ends with details of the development and the status of the use of ivermectin in the treatment of sea lice infestations at Scottish fish farms.     

Reducing sea lice (Lepeophtheirus salmonis) infestation of farmed Atlantic salmon (Salmo salar L.) through functional feeds

Health diets for Atlantic salmon have become an important component of the integrated pest management strategies targeting sea lice. A challenge trial was performed to examine the effect of supplementing salmon diets with either immunostimulants or essential oils. One control and four experimental diets containing immunostimulants or natural identical extracts were fed to Atlantic salmon in triplicate tanks for 4 weeks before challenging the fish with the sea lice copepodids. Prevalence of infection was 100%, and the mean abundance of infection was 21.2. The lowest mean lice count of 17 per fish (P < 0.05) was found in the group fed a mix of natural identical plant extracts (PX I). This represents a 20% reduction in infection, showing the potential for health diets to be employed as a tool to help control sea lice. To gain an understanding of the mechanisms of action underlying this protection, fish fed the control diet and fish fed the PX I diet were compared using quantitative histology of the epidermis and proteomic analysis of epidermal mucus. No significant differences were seen in the thickness of the epidermis or mucous cell percentage area, but differences in expression were seen for a number of proteins, including heat shock proteins, in epidermal mucus.     

Susceptibility,behaviour, and retention of the parasitic salmon louse (Lepeophtheirus salmonis) differ with Atlantic salmon population origin

Atlantic salmon populations across the world have diverse ecological and evolutionary histories, from wild anadromous or landlocked, to domestication and genetic modification. The natural host behaviours confer protection from infestation by ectoparasitic salmon lice Lepeophtheirus salmonis, yet whether genetic origin results in different behaviours and thus susceptibility to infestation is unknown. In common garden experiments, we tested antiparasite behaviours, susceptibility and retention of salmon lice in wild anadromous, wild landlocked, domesticated and genetically modified domesticated strains. Within domesticated strains, we tested two infestation histories (previously infested and naïve) and a new phenotype (albino colouring). Farmed stocks initially acquired 24%–44% higher levels of parasite density than the wild and landlocked strains. Burst swimming and displacement behaviours were higher in the domesticated groups, and jumping was more prevalent in the domesticated strains. At 34 days post‐infestation, domesticated strains and the wild anadromous strain did not differ significantly from each other; however, landlocked salmon had increased infestation levels considerably. Domesticated strains lost ~20% (±9.9%–16.5%; 95% CI) of their initial parasite load, while parasite load increased by 5.5% (±30.1%) for wild salmon and 20.1% (±28.5%) in landlocked salmon. This study provides early evidence for diverged host–parasite interactions associated with domestication in this system.     

Life cycle of Caligus rogercresseyi, (Copepoda: Caligidae) parasite of Chilean reared salmonids

Caligus rogercresseyi, [Contrib. Zool. 69 (2000) 137] is the only caligid known to affect the salmon industry in Southern Chile. Economic losses due to reduced fish quality, cost of chemical treatment and outbreaks of other diseases such as the Piscirickettsiosis occur. The life cycle of C. rogercresseyi is described in rainbow trout reared in seawater tanks from observations made under natural conditions of light and temperature between January 1997 and April 1998. Fish were infected with laboratory-cultured larvae obtained from ovigerous females. Rainbow trout were periodically slaughtered for parasite collection and identification. C. rogercresseyi life cycle includes the following stages: two nauplius, one copepodid, four chalimus and the adult. No preadult stage was observed. Timing of the different stages of development was directly dependent on water temperature. The maturation of the eggs or the time for a complete life cycle took place at 45 days in July at 10.3 °C, 31–32 days in April at 12.4 and 12.8 °C, respectively, and at 26 days in November at 15.2 °C. In January, at 16.7 °C, only the appearance of first eggs were observed at 18 days. A simple degree–day (dd) model is proposed for each developmental stage between 4 and 17 °C, where the development rate is a linear function of the average temperature of water. Using this degree–day model, the proportion of fourth stage chalimus was maximum at 172 dd of effective temperature, adult males at 193 degree–days, adult females at 208 dd. The minimum temperature threshold is at 4.2 °C where there is no development of the parasite. The appearance of first eggs occurred at 231 dd and the first pigmented eggs at 277 dd. The temperature-independent degree–days value allowed to predict the timing of C. rogercresseyi life cycle at any temperature within the evaluated range.     

The host transfer ability of Lepeophtheirus salmonis (Copepoda: Caligidae) from farmed Atlantic salmon, Salmo salar L.

The ability of mobile stages of Lepeophtheirus salmonis to transfer between salmon, Salmo salar L., hosts was examined by two methods. The first of these was the removal of certain stages on farmed fish, while the second comprised the placement of mobile lice on clean fish in the laboratory. In one-sea-winter farmed salmon, 63% of males and 52% of female lice transferred to new hosts over a period of 4 days. In laboratory trials on post-smolts, 61% of males and 69% of female lice transferred to new hosts over 3 days. In another experiment, free-swimming adult male lice were added to the tank, and 90% of these were found on fish after 24 h. Immigration of lice to fish in trial cages and the large proportion of lice transferring between fish in both laboratory and farm trials indicates that L. salmonis can transfer between hosts.     

Safety and efficacy of emamectin benzoate administered in-feed to Atlantic salmon, Salmo salar L., smolts in freshwater, as a preventative treatment against infestations of sea lice, Lepeophtheirus salmonis (Krøyer)

The safety and efficacy of emamectin benzoate, administered in-feed to Atlantic salmon smolts, Salmo salar L., held in freshwater, was evaluated as a preventative treatment against sea lice, Lepeophtheirus salmonis, following transfer of fish to seawater.

In the safety study, salmon smolts held in freshwater were fed with diets containing emamectin benzoate at nominal doses of 0 (control), 50 (recommended dose) and 250 (5× recommended dose) μg kg⁻¹ fish day⁻¹ for 7 days (days 0–6). Actual dose rates, based on measured concentrations of emamectin benzoate in feed, differences in fish weight, and feed consumed, were 0, 54, and 272 μg kg⁻¹ day⁻¹, respectively. On day 9, fish were transferred to seawater and observed for 14 days. No differences in feeding response, coordination, behaviour, gross and histological appearance were observed between control fish and those that received 54 μg kg⁻¹ day⁻¹. Among smolts that received 272 μg kg⁻¹ day⁻¹, approximately 50% exhibited darker coloration, and one fish (1%) exhibited uncoordinated swimming behaviour. No pathognomonic signs of emamectin benzoate toxicity were identified.

In the efficacy study, smolts held in freshwater were fed an unmedicated ration (control group) or emamectin benzoate at 50 μg kg⁻¹ day⁻¹ (treated group) for 7 days (days 0–6). On day 9, fish were re-distributed to eight seawater tanks, each holding 30 control and 30 treated fish. On days 28, 56, 77 and 109, respectively, control and treated fish in two tanks were challenged with L. salmonis copepodites. When lice in each group reached chalimus stage IV, fish were sampled and the numbers of lice were recorded. Fish challenged at day 109 were sampled for the second time when lice were at the adult stage. Efficacy was calculated as the reduction in the mean number of lice on treated fish relative to the mean on control fish. Treatment with emamectin benzoate resulted in an efficacy of 85.0–99.8% in fish challenged at days 28–77, from the start of treatment, and lice counts were significantly lower (P<0.001) on treated fish than on controls. When fish challenged at day 109 were sampled at day 128, efficacy was 44.3%, but survival of chalimus to adult lice on treated fish was lower, and at day 159, efficacy had increased to 73%. These results demonstrate that treatment of salmon smolts with emamectin benzoate in freshwater was well tolerated and highly effective in preventing sea lice infestation following transfer of fish to seawater.     

The effect of artificial light treatment and depth on the infestation of the sea louse Lepeophtheirus salmonis on Atlantic salmon (Salmo salar L.) culture

Two field studies were carried out with farmed Atlantic salmon (Salmo salarL.) in sea cages to examine various effects of artificial light (AL) and the vertical distribution of salmon on lice infestation.

The use of AL light caused an overall increase in lice infestation in both experiments. The first study showed that salmon held at 0–4 m depth in cages developed higher infestation than salmon held at greater depths (4–8 and 8–12 m) under both natural light (NL) and AL. In the second study, salmon maintained in 14-m deep sea cages that were exposed to AL with different light intensities. The AL treatments resulted directly in different diel and seasonal patterns of vertical distribution of the salmon and also different temporal patterns in lice infestations. So indirectly the infestation pattern appeared to be correlated with median day-time swimming depth of the salmon.     

An assessment of salmon farms and wild salmonids as sources of Lepeophtheirus salmonis (Krøyer) copepodids in the water column in Loch Torridon, Scotland

Wild salmonids and farmed salmon can both be sources of Lepeophtheirus salmonis (Krøyer, 1838) larvae . Farmed salmon smolts free of L. salmonis infections are stocked in sea cages and may subsequently contract L. salmonis infections, probably from wild fish. The contribution of gravid L. salmonis at Atlantic salmon, Salmo salar L., farms to populations of L. salmonis larvae in the water column has in the past been based on estimated parameters, such as louse fecundity. This present study augments these calculations by combining empirical data on densities of infective L. salmonis copepodids in the field with estimates of the number of gravid L. salmonis on farmed and wild salmonids in Loch Torridon. Data collected between 2002 and 2007 show a significant correlation between mean densities of L. salmonis copepodids recovered in the water column and the numbers of gravid L. salmonis at the local salmon farms. Generally, the farms with greatest numbers of salmon were observed to have stronger correlations with densities of copepodids in the water than the farms with fewer fish. The study suggests that louse management approaches, e.g. treatment trigger levels, need to take account of individual farm biomass, or numbers of fish. This study highlights the importance of control of L. salmonis on salmon farms for the co-existence of both wild salmonid populations and the aquaculture industry.     

Infestation parameters for Lepeophtheirus salmonis (Kroyer) (Copepoda: Caligidae) parasitic on sea trout, Salmo trutta L., off the west coast of Ireland during 1990 and 1991

Abstract. Infestation parameters for the calígíd copepod Lepeophtheirus salmonis (Kroyer) infesting sea trout, Salmo trutta L., were established for a number of locations off the west coast of Ireland during 1990 and 1991. Based on these parameters sites were classified into two groups in 1990 and three in 1991. Median parasitic intensity in these groups was 11·6 and 77 in 1990 and 9·5, 29·5 and 55 in 1991. Fish were parasitized mainly by chalimus stages of the parasite which attached preferentially to the fins. Heaviest infestations were invariably due to chalimus stages and early pre-adult lice and there was a progressive decrease in the correlation between parasitic intensity and the number of each successive stage in the life cycle. This suggested either host or parasite mortality as the parasite matured. Large numbers of lice-infested fish returned prematurely from the sea to estuarine areas at a number of sites. Extensive morphological damage, especially to the fins, was apparent on a proportion of these fish as a result of the infestation. Mortality of heavily infested fish was directly observed.