Review TRENDS in Parasitology Vol.22 No.

10

Ecology of sea lice parasitic on farmed

and wild fish
Mark J. Costello
Leigh Marine Laboratory, University of Auckland, PO Box 349, Warkworth, New Zealand

Abstract
Glossary
Sea lice, especially Lepeophtheirus salmonis and
Chalimus (plural chalimi): the four stages of immature lice fixed to the host by
Caligus spp., have the greatest economic impact of a frontal filament around which they feed on host mucus and skin.
any parasite in salmonid fish farming and are also a Copepodid: post-naupliar larvae. In the case of sea lice the term refers only to
threat to wild salmonids. Here, I review how the biology the free-living, non-feeding, planktonic larva that must find a host to survive, as
the next immature life-stage is called the chalimus stage.
and ecology of various louse and host species influence Degree days: in aquaculture, the sum of temperature degrees experienced daily
their pathogenicity and epidemiology. Recent discov- (e.g. 40 days at 10 8C = 400 8d). It is a useful index of the temperature required for
eries of new species and genotypes emphasize the need the growth and development of ectotherms within their range of tolerance.
Diel: over a 24-hour period of night and day.
for more basic research on louse taxonomy and host Epizootics: epidemics in non-human species.
preferences. Louse development rates are strongly Fallowing: the process of leaving cages on a farm site empty of fish so as to
dependent on temperature, and increasing mean sea interrupt parasite and disease cycles and/or to enable the seabed to recover
from waste sedimentation.
temperatures are likely to increase infestation pressure Frontal filament: an organ attaching chalimi and moulting mobiles of
on farms and wild fish, as well as affecting the geogra- Lepeophtheirus salmonis to the host.
phical distribution of hosts and parasites. Despite pro- Mobile lice: pre-adult and adult stages that move freely over the host fish.
Commonly referred to as mobiles.
gress in finding L. salmonis larvae in the plankton and in Nauplius (plural nauplii): two life-stages of free-living non-feeding planktonic
modelling louse production in several countries, more larvae that hatch from the egg and moult to become copepodids.
Ovigerous female: a female louse carrying two conspicuous uniseriate egg
data on larval behaviour and distribution are required to
strings containing a total of 100–1000 eggs.
develop dispersal and transmission models for both Parasiticide: a chemical or chemotherapeutants used to kill parasites. Can be
L. salmonis and Caligus spp. This knowledge could be called a medicine, pesticide, or drug in different countries.
Pre-adult: immature mobile louse. There are two pre-adult stages in
used to take measures to reduce the risks of lice affecting Lepeophtheirus species and there is some debate as to whether they occur
farmed and wild fish. in Caligus spp.
Pycnocline: a zone of rapid change in density in a water body, typically
Introduction attributable to temperature and/or salinity.
Sea trout: sea-running individual of the brown trout Salmo trutta L.
Sea lice (Copepoda, Caligidae) have been the most wide- Smolt: juvenile salmonid fish physiologically adapted for living in seawater. The
spread pathogenic marine parasite in the 30 year-old term is applied to fish immediately prior to their first migration from freshwater
to the sea, and can be applied to farm fish within their first year in seawater.
Atlantic salmon (Salmo salar L.) farming industry, and
Uniseriate: in a single row.
in the past 15 years pathogenic infestations on other
cultured fish and wild salmonids have escalated [1–3].
All but one species of sea lice parasitize bony marine fish
(Actinopterygii), and 54% of copepod infestations of farmed
fish are caligids [4]. Their impact ranges from mild skin
damage to stress induced mortality of individual fish
(Figure 1, Box 1), and includes epizootics (see Glossary)
in wild fish populations in Europe and British Columbia.
Research has concentrated on Lepeophtheirus salmonis
(Krøyer, 1837) because it has the greatest impact on
Atlantic salmon farms (Box 2). However, this research
has wider implications because other crustacean ectopara-
sites, including other caligids and isopods, are pathogenic
to salmonids and other cultured finfish [1,4–6]. Four spe-
cies of Caligus occur on farms in British Columbia, Chile,
Europe and Japan (Box 2).
Eggs carried by the female louse hatch into non-feeding
planktonic larvae that infect a new host (Box 3). How these
larvae disperse and find a new host has been one of the
most challenging issues, because of its relevance to
Figure 1. A typical heavy infestation of an Atlantic salmon by the sea louse
Corresponding author: Costello, M.J. ([email protected]). Lepeophtheirus salmonis, showing removal of skin over the head, and female lice
Available online 21 August 2006. bearing paired egg-strings on the back. Reproduced with permission from Alan Pike.

www.sciencedirect.com 1471-4922/$ – see front matter ß 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.pt.2006.08.006
476 Review TRENDS in Parasitology Vol.22 No.10

Box 1. Sea louse pathogenicity Box 2. Sea lice in salmon farms

Sea lice use rasping mouthparts to graze the host and remove Lepeophtheirus salmonis parasitizes Salmonidae in the northern
mucus, skin and underlying tissues [1] (Figure 1, main text). They hemisphere oceans: it has been recorded on 12 species in the
can occur anywhere on the body but often congregate on the head genera Salmo (North Atlantic salmon and trout), Salvelinus (trout
in farmed and wild fish. They grip the host with their second pair of and charr) and Oncorhynchus (Pacific salmon) [2], and two species
antennae and maxillipeds. Mobile sea lice are designed so that of cyprinids in marine waters in and near Japan [9]. In Chile, Caligus
water flow presses them to the host surface over which they swim rogercresseyi Boxshall and Bravo, 2000 is the dominant species on
by jet propulsion. Some salmon leaping behaviour appears to be a farmed salmonids. In Japan, L. salmonis is present on farmed
response to irritation by sea lice [64] and an attempt to dislodge salmonids, but it is C. orientalis Gussev, 1951 that is the more
them [1]; this can attract predators, distract the fish and has energy pathogenic [9]. Caligus elongatus Nordmann, 1832 is common on
costs. Impacts on the host skin include epithelium loss, bleeding, farmed salmonids in the northern hemisphere and is sometimes
increased mucus discharge, altered mucus biochemistry, tissue pathogenic, and like C. orientalis (in Japan), C. clemensi Parker and
necrosis and consequent loss of physical and microbial protective Margolis, 1964 (in British Columbia) and C. rogercresseyi and
function [4,7]. In heavy infestations, chalimi can attach in such C. teres Wilson, 1905 (in Chile), it is not host-specific [8,72].
numbers that they can be lost from the fins as a result of skin Although L. salmonis is the most pathogenic species on Atlantic
erosion. The attachment of chalimi to the gills appears to be an farms, probably because of its larger body size, it is also more
artefact of laboratory conditions [65] and would explain their prevalent and persistent on farmed fish than C. elongatus.
absence on the gills of wild fish [7]. However, it might also be due Salmonids are probably secondary hosts to the other Caligus
to loss of copepodids from the gills following initial settlement [63]. species recorded on farmed fish, as most are known to occur on
Host fish have reduced appetite, growth and food-conversion one or more wild non-salmonid hosts [8]. Nevertheless, these lice
efficiency, and the stress and wounds expose fish to secondary can be pathogenic to their secondary host, and it is crucial that
infections [1], to which they are more susceptible [66]. Changes to the parasites are correctly identified to understand their origins. One
the host blood include anaemia, reduced lymphocytes, protein, ion species, C. rogercresseyi, was only recently described from farmed
imbalance and elevated cortisol [4,7,8]. These changes indicate a salmon in Chile, where it had been mistakenly identified as
stressed and weakened host, with reduced osmoregulatory and C. flexispina. Genetic analysis indicates that the apparently
respiratory ability and impaired immunocompetence. In Europe, widespread C. elongatus consists of at least two genetically distinct
heavily infested sea trout return to fresh water prematurely [67], populations in the North Atlantic, both occurring on the same and a
suggesting that this could reduce osmoregulatory stress and/or help variety of hosts [41,72], and that North Atlantic and Pacific
remove lice. Laboratory studies found swimming performance of populations of L. salmonis are distinct [35]. This demonstrates the
louse-infested fish improved when transferred from sea to fresh need for continued taxonomic research on caligids and their hosts
water [68]. Host blood is not an important part of the diet of sea lice, and for new identification guides. Louse species have varying
as suggested by some authors, and female lice do not ingest more environmental tolerances, behaviour as adults and larvae and
than males as might be the case for blood-feeding parasites [69]. growth and survival on different hosts, yet species identity has not
However, physiologically significant host blood loss can occur with been well determined in studies aimed to determine whether sea
high levels of louse infestation [70]. The risk that sea lice transmit lice spread from farms to wild fish [29,43]. Differences between
bacterial and viral pathogens is a concern [71]. Although the risk is different host and parasite species, as well as different develop-
low for L. salmonis [2,7], it is higher for Caligus species because mental stages of the host and parasite, must be clarified to prevent
they occur on more host species and adults of at least C. elongatus confusion in modelling epidemiological impacts of sea lice and
occur in the plankton [1]. developing integrated pest management strategies.

transfer within and between fish farms and also from mature adult for L. salmonis and C. elongatus on Atlantic
farms to wild fish populations. Here, I focus on the patterns salmon is 40 days at 10 8C (i.e. 400 degree days) for males
of sea louse infestation and the aspects of their biology that and 10 days longer for females [1,2,10]. Generation times
influence transmission, because these issues have received can be shorter for C. rogercresseyi [11], and if derived from
least attention in previous reviews [2,4,7,8]. Space limita- monitoring field populations, generation times can appear
tions require that references given are those published longer because cohorts are not as synchronized as in the
since previous reviews on aspects of this subject laboratory [11]. In addition, development rates can vary on
[1,2,4,5,7–9]. It should be noted that many observations different hosts [7]. Typically for crustaceans, sea lice live
in the literature have not been replicated across localities, longer and grow larger at colder temperatures, and larger
populations or species, and future studies are needed to females produce more eggs [2]. Consequently, over-
test the generalizations drawn from previous studies. wintering females are larger and release more eggs in
the spring than summer brooders. Because spring eggs
Infestation patterns are also larger, spring larvae have greater food reserves
Although the abundance of sea lice depends on their intrin- and thus they might spend longer in the plankton search-
sic fecundity and rates of growth and development, it could ing for a suitable host. Laboratory studies could determine
also depend on density-dependant competition within and larval viability in relation to parent body size and
between species, and on host responses to infestation. Key larval size. Although summer generations of females are
factors affecting these characteristics and interactions smaller and have fewer eggs per brood because of the
include sea temperature, and host abundance and distribu- shorter generation time at warmer temperatures,
tion. The concentration of hosts on salmon farms has the summer populations can increase exponentially. The
increased lice abundance locally, with consequences for lice different temperature regimes in salmon farming areas
infestations on farmed and wild hosts. (1–14 8C in Atlantic Canada, 6–18 8C in Ireland and
1–20 8C in some Norwegian fjords) are thus likely to result
Louse population dynamics in different sea louse population dynamics. However,
Sea louse growth is strongly dependent on temperature. In further research on different sea louse species and popula-
the laboratory, the generation time from egg extrusion to tions is required to explain variation in their development
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 Review TRENDS in Parasitology Vol.22 No.10 477

Box 3. Sea louse life-cycles Box 4. Sea louse control on salmonid farms
Sea louse eggs are carried in a pair of uniseriate strings of 100 to The following guidelines give the best practice for sea louse control
1000 eggs extruded from the abdomen of the female [1] (Figure I). on salmonid farms [76]:
The number of eggs per sea louse varies with time of year, louse  To break the population cycle of sea lice, farms should have a
size, louse age, host species and population and is affected on farms fallow period during which no farmed fish are present in an area
by the effects of parasiticides [1]. The use of 500 eggs per sea louse for 4–6 weeks. This is facilitated by having only one year class of
on farmed salmon and 1000 on wild fish for modelling louse fish per site.
populations [25] would thus have been conservative in estimating  Cleaner-fish should be stocked into fish cages where they are
production of sea lice on farms. Further quantitative data on the available.
relationship of egg production to the above variables is important  In-feed parasiticides should be given to smolts in freshwater tanks
for assessing infestation risks [10,73]. before transfer to sea cages and louse abundance should then be
The eggs hatch in sequence from the distal end and the female monitored to guide future treatment.
can produce six to eleven broods [2]. Two nauplius stages of larvae  Sick (moribund) fish should be removed from sea cages and net
are non-feeding and planktonic for 5–15 days (temperature-depen- fouling should be minimized to maximize water flow.
dent) and moult into infective free-living copepodids that attach to a  If present, lice should be treated during the winter to remove egg-
host by their antennae [1]. Eggs manually removed from the female bearing females before the spring.
hatch in the laboratory and can be easily reared to copepodids.  Where parasiticides are used regularly in an area, louse sensitivity
Evidence suggests that copepodids (i) respond visually to host (resistance) to them should be monitored.
shadows and flashes from host scales, (ii) use mechanoreceptors on  The health status of fish stocked into a farm should be made
their antennae to respond to vibrations such as those a host creates known to neighbouring farms.
and (iii) use chemoreceptors to determine host suitability (and later  Prevention of escaped salmon will reduce the risks of transfer to
mate detection) [2,11,74]. Recent research also indicates that other farms and wild fish.
copepodids and mobile lice could use water-borne chemical cues  The potential of transfer of sea lice (and other pathogens) should
(semiochemicals) to recognize hosts [75]. be considered in the selection of farm sites.
The copepodid moults into a chalimus that is attached to the host Cleaner-fish were the first successful use of biological control in
by a special frontal filament [2]. There are four successive sessile finfish culture; they include five species of wrasse (Labridae) in
chalimus stages that feed on the host skin around their point of Europe [1,77]. Wrasse remove larger lice first, thus eliminating egg-
attachment. In Lepeophtheirus, but not necessarily in Caligus bearing females and do so without stressing the salmon, with
species [5], there are two immature pre-adult stages that move consequent benefits in growth and food-conversion efficiency. If
freely over the host skin to feed. These mobile stages attach to the wrasse escape or insufficient numbers are available, a parasiticide
host with a chalimus-like filament when moulting [2]. Although treatment can be undertaken, even with wrasse in the cage. This
Kabata suggested in 1972 (reviewed in [5]) that all Caligidae have practice is well-established in Norway, including the use of novel
ten life-stages (two nauplius, copepodid, four chalimus, two pre- fisheries and traps and special good husbandry practices [78–80].
adult, adult), and that the apparent absence of one or two pre-adult Parasiticides against sea lice can be applied as an in-situ
stages in descriptions of some Caligus species was an oversight by ‘bath’ by enclosing the salmon cage in a plastic covering, or
researchers (including himself), a recent review considers Caligus they can be mixed with the food pellets as ‘in-feed’ treatments [1].
species to have no pre-adult stage [5]. Bath treatments are generally less effective because it is very
Although direct measurement of individual life-spans is difficult, difficult to get a uniform concentration within the cage, so some
laboratory studies and the fact that lice over-winter on wild salmon lice are not removed and concentrations can stress the fish [1,81].
[48] indicate individuals can live for over seven months. The loss of In addition, crowding stresses the fish, and it is very difficult to
lice from fish in the laboratory cannot be assumed to be natural treat all cages on a site on the same day so lice can transfer to
mortality as sea lice can easily escape from outflow pipes, and re-infest fish previously treated in other cages. However, in-feed
where mortality occurs this might reflect suboptimal environmental treatments cannot be used when fish are not feeding. Furthermore,
conditions (e.g. poor water quality). because they are systemic, it takes longer for levels in the fish to
be reduced to those permissible for human consumption; which
might delay harvest. The initial parasiticides used against sea
lice were baths of the organophosphates trichlorvos and
dichlorvos, now replaced by azamethiphos (also an organopho-
sphate), cypermethrin and deltamethrin (permethrins) and hydro-
gen peroxide. The in-feed treatments are the chitin synthesis
inhibitors diflubenzuron and teflubenzuron and the most
popular sea louse parasiticide emamectin benzoate. Resistance to
organophosphates, permethrins and hydrogen peroxide has been
recorded [82–84].

Increased average sea temperatures, whether due to

annual variation or as predicted by climate change sce-
narios for future decades (http://www.ipcc.ch), are likely to
increase louse abundance on wild and farmed fish as a
Figure I. The ten life-stages in the life-cycle of the sea louse Lepeophtheirus result of shorter generation times. In addition, they are
salmonis. Free-living planktonic stages are shown in bold.
likely to affect the geographical distribution of sea lice and
their wild hosts, potentially bringing new sea louse species
and fecundity with temperature [10]. In addition, how the into contact with wild and farmed fish. Moreover, locally
parasite–host interaction varies with temperature, as well increased maximum temperatures might stress sea lice
as with the parasite and host species, remains unstudied, and/or their hosts.
despite its implications for fish health management on Treatments that remove egg-bearing females during the
salmon farms. winter or early spring could prevent the release of many
Temperature-dependent life-cycle characteristics have larvae during the spring, leading to lower infestations on
important implications for louse control on farms (Box 4). farmed and possibly wild salmon in the vicinity (Box 4). If a
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478 Review TRENDS in Parasitology Vol.22 No.10

farm is exposed to infestations (from other farms or from Louse productivity

wild fish) during the summer, parasiticide treatments are Most sea louse larval production in Ireland [22,23], Scot-
required more frequently to interrupt the life cycle and land [24] and Norway [25] is currently from salmon farms,
prevent exponential population growth. If a treatment because there are far more farmed than wild Atlantic
affects only mobile stages, then repeat treatments are salmon in coastal waters and farmed salmon are present
necessary when the chalimus stages moult to pre-adults, all year around. By contrast, wild salmonids migrate from
perhaps only every one or two weeks at summer their natal freshwaters to the sea annually, and some
temperatures. species move away from coastal waters during their mar-
ine residence. In Norway, there are 100 times more farmed
Intra- and interspecific competition than wild salmon, and escaped farm salmon have 10 times
Competition for mates and avoidance interactions can more lice than wild salmon [26]. Thus, escaped fish could be
affect the distribution of lice on the host. Adult male lice a significant reservoir of sea lice and could bring sea lice
actively compete for and guard females before mating. into close proximity to wild fish. Significant numbers of
Although the male transfers a spermatophore that blocks escaped farmed salmon also occur in the lower Bay of
the female from further mating [12,13] for a time, females Fundy, Canada, and their louse burdens are similar to
can mate again and polyandry is common [14]. Sperm levels on wild fish and on nearby farms [27], suggesting a
storage reduces the need for mating at low parasite common infestation pool. More significant reservoirs of lice
densities. occur on wild salmonids in the northern Pacific Ocean than
The fact that the first infestations on farms are often in the Atlantic Ocean because more species of salmonids
C. elongatus, later replaced by L. salmonis, which occur there and these fish are more abundant. This expo-
thereafter remains the dominant species [15], suggests sure to infestation from wild fish is a concern for Pacific
density-dependent inter-specific competition. Schram farms, but transfer of lice from farms to wild fish could also
et al. [16] rejected competitive exclusion between these be locally significant [28,29].
species, but the intensity of infestation on the wild sea
trout (Salmo trutta L.) that they analysed was low (< 0.04 Aggregation of lice on hosts
lice g 1), so it is possible that no competition had occurred. On wild fish and during the early stages of farm infesta-
Variation in the abundance of C. elongatus over time is tions, the frequency of occurrence of lice on the host popu-
greater than might be expected from population growth lation is highly aggregated and the numbers of chalimus
and mortality on wild sea trout [16] and on farmed Atlantic are fewer than of mobile stages [1,30], reflecting the longer
salmon [17] and suggests that mobile stages might infest duration of the mobile life stage. This aggregated distribu-
and leave their hosts. Although in the past L. salmonis has tion is typical of most parasites, with most hosts having few
typically increased in abundance on farms despite or no sea lice. By contrast, when pathogenicity occurs on
anti-parasite ‘bath’ treatments [17], C. elongatus farmed and wild fish, all or almost all hosts are infested,
abundance is similar on farmed salmon in their first and the abundance of lice increases (Figure 2). Concomi-
and second sea-years. This suggests re-infestation from tantly, the frequency distribution of parasites changes
wild sources, which could explain the lack of benefit of from highly dispersed to normal [1], a pattern generally
parasiticide treatments for C. elongatus on Scottish farms considered to indicate parasite-induced mortality [31].
[17]. Epizootics on wild sea trout smolts [1] and wild juvenile
The prevalence and intensity (i.e. abundance on infected Pacific salmon [28] are characterized by the dominance of
fish only) of sea lice generally increases with the age of wild chalimus stages. Laboratory infections typically have a
Pacific salmon and with fish size. However, louse intensity normal distribution, probably related to more homogenous
per unit area of fish surface does not increase with fish size experimental infestations, but also perhaps the result of
[18,19], suggesting a maximum intensity of lice per host. lower genetic variation in farmed fish [18].
This could be a consequence of antagonistic interactions
(interference competition) between sea lice jockeying for Abundance of pathogenic lice
the best positions or competing for mates and/or the host The prevalence (% population infested) and the abundance
being able to shed parasites by physically dislodging them. of lice on hosts increase in concert and show similar
Immunological factors might be involved whereby an patterns for wild Pacific and Atlantic salmon and for sea
increased host response offsets the increase in the sea trout in areas without salmon farms (Figure 2). Sea trout in
louse population. For example, if the host developed sig- areas with salmon farms generally have more sea lice at all
nificant immunity with age or duration of infestation, levels of prevalence, reflecting the higher proportions of
decreased louse intensity would be expected, as occurs chalimi. Epizootics recorded on sea trout in Europe and
for other ectoparasites [1]. One study found that repeated Pacific salmon in British Columbia tended to have over
laboratory infections of Atlantic salmon with L. salmonis 60% prevalence and more than five lice per fish. Such louse
do not predict later levels [20], but another suggested that levels have occurred on wild fish (Figure 2), and more
prior louse infestation stimulates genetically based resis- heavily infested fish might not live to be sampled. Although
tance of Atlantic salmon to L. salmonis [21]. Thus, before it this suggests that lice are pathogenic to more wild
can be concluded that no long-term immune protection populations than previously appreciated, it should be
develops in individual fish, such experiments need to be noted that Pacific salmon are less impacted by L. salmonis
repeated at different louse intensities on fish of varying than Salmo spp., and larger fish can support more sea lice.
age, size, genotype and physical condition. Levels of infection of < 0.1 mobile lice g 1 (i.e. ten lice on
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 Review TRENDS in Parasitology Vol.22 No.10 479

Figure 2. Relationship of mean L. salmonis abundance to prevalence on samples from wild salmonids. Solid green circles, Pacific salmon; open blue circles, Atlantic
salmon; blue triangles, sea trout outside areas with salmon farms; red triangles, sea trout within areas with salmon farms; open black diamonds, samples from epizootics
on wild sea trout and sockeye salmon that represent known pathogenic infestations. Numbers include pre-adult, adult and chalimus stages, but the chalimus stages might
have been underestimated in some samples. Sample sizes and host body size varied. The occurrence of some wild fish data within the area encompassed by the epizootic
data, and the higher abundance on sea trout in areas near salmon farms, suggest that levels on wild fish above 60% prevalence and five lice per fish were pathogenic. The
data and sources used to compile the figure are detailed in the Online Supplementary Material.

100 g fish) in experimental infections caused changes in infective planktonic copepodids. Plankton sampling in
host physiology, biochemistry and immunology, in both the sea inlets in the mid-west of Ireland revealed that louse
presence and absence of a host stress response [7,8]. Farm larvae, especially infective copepodids, are most abun-
observations suggest that more than ten mobile lice per dant in shallow estuarine areas, ideal locations to inter-
fish reduce the appetite of a 3–4 kg Atlantic salmon [32,33], cept migratory salmonids [42]. These studies revealed a
and five per fish (0.05 to 0.1 mobile lice g 1) generally rapid decrease in sea louse nauplius concentrations away
trigger treatment of smolts on farms. Thus, experimental from fish farms, but no such trends for copepodids.
infections of individual fish, farm experience and patterns Sampling programmes in two Scottish lochs repeatedly
across populations indicate that more than 5–10 lice per produced the highest concentrations of copepodids in
fish (> 0.1 lice g 1) can or will become pathogenic. shallow water near the estuary mouth [43,44]. Indeed,
the highest concentrations of these larvae were caught
Transmission with hand-nets by researchers wading along the shore,
How copepodids increase their chances of intercepting a rather than from nets towed by boats. It thus seems that
host has been one of the most challenging questions for L. salmonis larvae not only move vertically in the water
researchers. The diversity of caligids, many specific to column, but are transported horizontally towards shal-
certain species, genera or families of marine fish, demon- low waters, where salmonids are more abundant. An
strates effective host-specific transmission. Microsatellite alternative hypothesis to explain estuarine concentra-
[34] and mitochondrial [35] DNA analysis showed that tions of copepodids is that ovigerous lice detach from
L. salmonis is a single population in the North Atlantic, salmonids that are migrating up rivers and the eggs
but Atlantic and Pacific populations were distinct, survive and hatch in the estuary [42]. This hypothesis
reflecting dispersal by their migratory hosts and plank- was proposed in part because the observed gradient of
tonic larvae. Although genetics cannot discriminate decreasing concentrations of nauplii 2 km from a fish
between populations of sea lice on wild and/or farmed fish farm was interpreted as requiring an alternative source
[36–38], measures influenced by diet such as carbon–nitro- of louse infestation in the estuary. However, the
gen stable isotope ratios [39], and by diet, environment and same study found no such gradient for copepodids, and
genes such as elemental signatures [40], can do so. all other evidence suggests that larvae with a planktonic
Furthermore, genetic analyses of other louse species have life span of several days disperse over much
found sub-populations or cryptic species, illustrating the greater distances than 2 km (see below). Furthermore,
need for caution in generalizing between populations and L. salmonis do not fall off their host until in fresh water
species [41]. for some days and their eggs do not hatch in fresh
water [1].
Distribution of louse larvae
Epizootics of sea lice on wild fish consist almost entirely Larval dispersal
of chalimus stages [1,28] (Figure 2), indicating that the Lepeophtheirus salmonis do not find their hosts only in
fish simultaneously encounter high concentrations of the estuaries. The presence of chalimi on wild salmon in the
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480 Review TRENDS in Parasitology Vol.22 No.10

offshore Atlantic and Pacific oceans indicate they receive surface at night [1]. Some populations of scallop larvae
low levels of L. salmonis infestation when away from have vertical migration adapted to local hydrographic
the coast [9,46–48]. The typical development of conditions [55]. The evidence suggests that L. salmonis
infestations on farmed salmon indicate that many larvae behaviour facilitates interception of salmonids migrating
are available to re-infest their parent’s hosts, and plankton through estuaries. The fact that it survives much longer in
sampling has shown that not all copepodids disperse away fresh water than C. elongatus [1], up to 14 days when
from the cages [42]. A study on C. elongatus infesting attached to its host [58], could be an adaptation to survive
haddock (Melanogrammus aeglefinus L.) suggested that on hosts that frequent brackish waters.
louse larvae are distributed in a mid-water layer and Both active and passive mechanisms to aid host inter-
intercept haddock that swim through this zone [1]. ception are probably involved. The larvae might have
Salmonids typically feed at the surface in farm cages endogenous tidal rhythms, respond to sunlight, moonlight,
and also come near the surface to feed in the wild. Thus salinity or water pressure, or detect turbulence associated
vertical movement of sea louse larvae or their hosts could with high current velocities to stimulate upward swim-
increase opportunity for parasite–host contact. ming and thus position themselves to be passively trans-
Significant correlations between L. salmonis abundance ported in tidal currents as other larvae do
on salmon in farms and on wild sea trout in Ireland has [7,55,56,59,60,61]. The larvae of many species concentrate
been found up to 30 km from the farms [7,22]. Salmon on along pycnoclines [61], and vertical migration and reaction
Norwegian farms that are > 10 km apart seem to have to salinity gradients is known for L. salmonis larvae [62].
fewer lice [49], as do pristine areas where farms In laboratory flumes, copepodid attachment to hosts was
were absent [46]. A field and modelling study in British greatest in conditions of medium light (300 lux), full salin-
Columbia found that larval dispersal and infestation on ity (35 parts per thousand) and low velocity (0.2 cm s 1)
wild salmonids extends 30 km from a farm and that [63].
secondary production of lice from infested migrating wild Sea louse infestations have been observed to arrive in
fish is detectable up to 75 km from the farm [29]. Sea louse pulses. This could be a passive consequence of lunar peri-
larvae could disperse in a concentration gradient that odicity of the tides; the difference between spring and neap
depends on tidal currents and prevailing wind patterns tides can result in concentration or dilution of sea louse
[43,44,50]. larvae through changes of 25–30% of the tidal seawater
Studies on other marine organisms that disperse in the volume in a bay. The risk of dilution could be offset by
plankton have demonstrated passive transport of 2–23 km larvae concentrating in surface waters and against halo-
in one 6 hour tide for seagrass [45], and mussel larvae clines. Further research into these mechanisms will enable
can disperse an average of 20–30 km and have a population more spatially explicit estimates of the risk of infestation
range of 60 km [51]. Decapod and cirripede crustaceans can on farmed and wild fish.
invade new areas at a rate of 33–160 km per year [52].
From known larval survival data and dispersal distance it A transmission model for L. salmonis
is possible to predict that louse larvae could disperse an The following process could explain how sea louse larvae of
average of 27 km (range 11–45 km) over 5–15 days [53]. L. salmonis are transported and concentrated into shallow
Predicted average dispersal of sea louse larvae ranges from coastal and estuarine waters that salmonids frequent.
12 km (range 5–17 km) in low currents (5 cm s 1) to Nauplii swim upwards during the day but do not actively
47 km (range 23–70 km) in higher currents (20 cm s 1) swim downwards. They are thus likely to concentrate in
(B. Kinlan, personal communication). This suggests that surface waters. During the day, onshore winds generated
sea louse larvae can typically disperse 10–50 km. However, by thermo-convection from warmer land drive surface
the interaction between larval behaviour and local hydro- waters containing the sea lice towards the shore and
graphic conditions can vary locally and could lead to larval towards estuaries (as these are further inland). Where
retention within some areas [23]. Simple diffusion models fresh water lies on the surface, sea louse larvae can con-
predicted dispersal of louse larvae from a farm in British gregate along the halocline. Thus larvae can concentrate
Columbia and subsequent infestation of juvenile wild fish at the surface and/or the marine–freshwater interface,
[29]. The species of sea lice infesting the farm was not which salmon smolts migrate through to enter ocean
reported, but 53 of the 65 ovigerous lice on juvenile wild waters. Tidal currents increase in estuaries as the tidal
fish were C. clemensi, a species found to infest returning volume is forced into a narrow channel. This increase in
wild Pacific salmon in these coastal waters [54]. The dis- current velocity increases the likelihood of copepodids
persion model could apply to this species or both it and being close to a potential host, although host attachment
L. salmonis. The abundance of L. salmonis on wild fish has might be more difficult in stronger currents [63]. These
also been linked to farms in the area [28]. options for the transmission model could be tested by
giving particles a daily vertical migration behaviour in
Behaviour of Lepeophtheirus salmonis larvae a previously validated 3D hydrographic model that
Larvae of many species, including crustaceans and mol- includes wind direction. A consequence of this transmis-
luscs, migrate vertically with diel and tidal periodicities, sion mechanism is that the risk of infestation could be at
with consequent transport into or out of estuaries and thus least as high near the shore and in estuaries as at an
settlement in their preferred habitats [55–57]. Copepodids infested fish cage. This was the pattern observed on sal-
of the copepod parasite Lernaeenicus sprattae (Sowerby. mon in experimental cages in Killary Harbour, Ireland
1806), and their juvenile fish hosts, concentrate at the sea [42].
www.sciencedirect.com
 Review TRENDS in Parasitology Vol.22 No.10 481

Future research Aberdeen), Per A. Kvenseth (Norsk Sjømatsenter, Bergen), Peter A.

Heuch (National Veterinary Institute, Oslo), Geoff Boxshall (Natural
The most abundant and pathogenic sea lice on farmed fish
History Museum, London) and the anonymous referees that provided
in Chile was recently found to be a species new to science, helpful comments on earlier drafts.
and the commonest species in the North Atlantic, C. elon-
gatus, has at least two genotypes. These findings empha- Appendix A. Supplementary data
sise the need for more basic research on sea louse taxonomy Supplementary data associated with this article can be
and natural hosts. found, in the online version, at doi:10.1016/
Research indicates roles for both the host immune j.pt.2006.08.006.
response in reducing sea lice impacts and the parasite in
suppressing such responses [8]. The former could reduce References
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