Veterinary Parasitology 163 (2009) 207–216

Contents lists available at ScienceDirect

Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar

Selected parasitosis in cultured and wild fish

F.C. Guo a,*, P.T.K. Woo b
a
Novartis Animal Health Canada Inc., Aqua Heath Business, 797 Victoria Road, Victoria, PE, C0A 2G0, Canada
b
Department of Integrative Biology, University of Guelph, Guelph, ON, Canada

A R T I C L E I N F O A B S T R A C T

Keywords: While intensive aquaculture has and will continue to supply the ever growing population
Caligus rogercresseyi with highly nutritious protein, it also comes with problems which include more frequent
Cryptobia salmositica outbreaks of diseases in fish farms and transmission of diseases between farmed and wild
Gyrodactylus salaris fish. We have selected four Phyla of economically important fish parasites for our present
Lepeophtheirus salmonis
discussion—a haemoflagellate (Cryptobia salmositica), a microsporidian, (Loma salmonae),
Loma salmonae
a monogenean (Gyrodactylus salaries) and two copepods (Lepeophtheirus salmonis, Caligus
Aquaculture
Parasitosis rogercresseyi). This review consists of two parts with a brief description of each parasite
Wild and farmed fish and its biology related to transmission, followed by discussions on epizootic outbreaks in
both wild and farmed fish, interactions between wild and farmed fish, and disease
prevention and control.
ß 2009 Published by Elsevier B.V.

1. Introduction disease outbreaks in the animals and the subsequent

The demand for animal protein will continue to escalate
as the world population increases from 6 billion (estimated
in 1989) to about 8 billion within the next 15 years. This
increase will exert additional pressures on food production
which is already competing with other essential human
activities (e.g., cultivation of crop, transportation, housing,
industry) for the finite amount of usable land. Animal
protein contains essential amino acids which are impor-
tant for a nutritional and well-balanced diet. Free ranging
land animals are no longer a significant source of protein
and the production costs of farm-raised animals continue
to increase as land becomes more expensive. Conse-
quently, farms have to be large and are usually close to
human habitations to increase efficiency, and reduce
production and transportation costs. The large scale
breeding of warm-blooded animals close to human
populations presents some serious problems, including
discharge and/or storage of animal wastes and associated
public health issues. There are also increased risks of
* Corresponding author. Tel.: +1 902 367 7438; fax: +1 902 658 2261.
E-mail address: fuci.guo@novartis.com (F.C. Guo).
interspecies transmission of zoonotic diseases to humans
(e.g., Nipah virus in pigs, avian influenza H5N1 virus in
birds, cryptosporidian parasite in cattle) (Woo, 2006a).
Fish is an excellent protein and is easily digestible.
Many species of marine fish have the beneficial poly-
unsaturated fatty acids (PUFA; Omega 3 fatty acid) which
include docosahexaenoic acid (DHA) and eicosapentaenoic
acid (EPA). Both DHA and EPA are physiologically essential
nutrients for normal brain function. DHA is also an
important component of phospholipids of cell membrane
and hence is necessary for proper function of the retina and
brain. PUFA has other beneficial effects and they include
reducing risks of cardio-vascular diseases. The capture-
fishery is on the decline or at least stagnant, and this has
partly been brought about by over and/or indiscriminate
fishing, destruction of spawning grounds, and no newly
discovered fishing grounds. Also, industrial wastes (e.g.,
organochlorine pesticides, PCBs, heavy metals) discharged
into the aquatic environment can reduce fish growth and
reproduction and in some areas fish are no longer
recommended for human consumption because they have
accumulated such high levels of pollutants. Aquaculture of
fish is a good option as production costs are lower over
time, especially in cage cultures. It has been the fastest

0304-4017/$ – see front matter ß 2009 Published by Elsevier B.V.

doi:10.1016/j.vetpar.2009.06.016
208 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216
growing food production sector since 1970 – with an
increase at a compounded rate of about 9.2% per year. Also,
it does not have some of the problems (e.g., public health
issues) associated with the large populations of warm-
blooded animals close to human habitations (Woo, 2006a).
Intensive aquaculture of fish is not without its
problems, and these include disease outbreaks and
consequences of introducing parasites to new hosts and/
or new localities with the transportation of live fish. Severe
epizootics have occurred and many of these are man-
made. Selected outbreaks are discussed to better under-
stand the nature and cause of the epizootics. The current
discussion is in two parts and is intended to highlight
epizootics caused by relatively well-studied parasites from
four Phyla (Phylum Euglenozoa – a haemoflagellate;
Phylum Microspora – a microsporidian; Phylum Platyhel-
minths – a flatworm; Phylum Arthropoda – sea lice) which
cause morbidity and mortality in fishes reared in
hatcheries, sea cages, and in their natural habitats. Part I
of the discussion is to provide sufficient relevant back-
ground information on the biology of these parasites as
they relate to the epizootics while Part II is on selected
epizootic outbreaks with control measures in both
cultured and wild fish stocks.
2. Biology of parasites
2.1. Cryptobia salmositica
Cryptobia salmositica (Fig. 1; Phylum Euglenozoa) is an
elongated extracellular haemoflagellate. It has a prominent
kinteoplast at the anterior end, a central nucleus and two
flagella. The parasite has been found in many fish species (all
the Pacific salmon, Oncorhynchus spp. and sculpins, Cottus
spp.) in streams and rivers along the west coast of North
America. It is normally transmitted indirectly from fish to
fish by the freshwater leech, Piscicola salmositica. Briefly, the
parasite is ingested during a blood meal, multiplies in the
crop of the leech, and is inoculated into a new host when
the leech feeds again. In the absence of the leech vector
direct transmission between fish can occur under certain
aquaculture conditions (e.g., during grading and weighing
when fish are brought into direct contact with each other,
crowding in tanks or in rearing cages). The prevalence of the
parasite in downstream migrants (pre-smolt salmon) can be
Fig. 1. Cryptobia salmositica (Phylum Euglenozoa) with a red blood cell
from a fish with microcytic and hypochromic anaemia. Reproduced from
Woo (2006b).
quite variable (e.g., 3–21%) in streams in Oregon, United
States, and fingerlings have detectable infections as early as
60 days after they hatch. Sexually mature salmon become
infected within days of returning to fresh water from the sea.
The parasite is not pathogenic to sculpins (reservoir hosts)
but causes disease in salmonids. Severe outbreaks of
salmonid cryptobiosis have occurred in fish maintained
in sea cages, in freshwater hatcheries and in streams
(Woo, 2003).
2.2. Loma salmonae
Microsporidians are a diverse group of unicellular
organisms that live as obligate intracellular parasites in
many invertebrates and are reported from all classes of
vertebrate hosts. Many microsporidian species are widely
distributed in teleosts in freshwater, brackish and marine
habitats (Dykova, 2006). Once considered as the most
primitive eukaryotes, they are now regarded as highly
specialized fungi with simple life cycles consisting of
merogony and sporogony stages (Keeling and Fast, 2002).
Microsporidians are single walled spores with length of
2–10 mm, mostly ellipsoidal or egg shaped and lack
mitochondria. The spores contain extrusive apparatus
capable of injecting sporoplasm into host cell via extrud-
able polar tube (Dykova, 2006).
Loma salmonae (Putz et al., 1965; Fig. 2; Phylum
Microspora) causes microsporidial gill disease (MGD) in
seven salmonid species of the genus Oncorhynchus (Bruno
et al., 1995; Hauck, 1984; Kent et al., 1989; Magor, 1987;
Morrison and Sprague, 1983; Speare et al., 1989), brook
trout, Salvelinus fontinalis (Shaw et al., 2000), and brown
trout, Salmo trutta (Bader et al., 1998). The typical clinical
signs include pale gills with petechial hemorrhages,
hyperplasia, and white cysts called xenomas (Wales and
Wolf, 1955; Hauck, 1984; Kent, 1992). Fish with high
numbers of xenomas in their gills suffered respiratory
distress, secondary infection and high mortality rates.
(Speare et al., 1998; Becker and Speare, 2007). Laboratory
studies show that L. salmonae can be transmitted directly
via ingestion of spores by fish. Briefly, the spore enters the
gut and injects sporoplasm into an epithelial cell, it
migrates to the heart, then to the gill, and forms a spore-
laden xenoma within the gill filaments. The rupture of
xenoma causes proliferative branchitis and massive
number of spores release (Shaw et al., 1998; Sanchez
et al., 2001b, Becker and Speare, 2007).
2.3. Gyrodactylus salaris
Gyrodactylus salaris (Fig. 3; Phylum Platyhelminthes) is
a parasitic flatworm of fishes in freshwater rivers and
lakes. Numerous other species of monogeneans are known
to cause morbidity and mortality in freshwater and marine
fishes. Monogeneans have a direct life cycle and are either
viviparous (give birth to free-swimming larvae, e.g.,
Gyrodactylus) or are oviparous (produce eggs which hatch
after they are laid, e.g., Pseudodactylogyrus). In either case
the free-swimming larva (oncomiracidium) migrates to
specific sites (e.g., on the gills, the fins or the body surface)
where it attaches. On susceptible hosts the parasite has a
 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216 209

Fig. 2. Loma salmonae (Phylum Microspora) (a) Xenoma within the

primary gill filament of a Chinook salmon containing a hypertrophied
nucleus (N), meronts (arrowhead) and spores. Bar = 8 mm. (b) L. salmonae
spore with the electron-dense exospore (arrow) adjacent to the
translucent endospore and characteristic coiled polar tube
(arrowheads). Bar = 700 nm. Reproduced from Becker and Speare
(2007). (Photos courtesy of Dr. Jan Lovy).

high reproductive rate which rapidly increases the intensity

of infection, and this also promotes efficient transmission
between fish especially when fish are under crowded
conditions. Most monogeneans are ectoparasitic on specific
sites on the fish (e.g., on branchial arches, the fins, the head)
and they attach to the host using their opisthaptor (an organ
located at the posterior end of the worm) which is usually
equipped with large hooks, clamps and/or suckers. Species
like G. salaris cause morbidity and mortality in fish because
of their high intensities, and significant damage at the point
of attachment (with considerable host reactions) through
their opisthaptor and by grazing on exposed structures and
vulnerable integument. The parasite is mainly a pathogen of
Atlantic salmon, Salmo salar, in freshwater rivers and lakes in
Norway. Artic charr, Salvelinus alpinus, and rainbow trout, Fig. 3. Viviparous gyrodactylid monogenean (Gyrodactylus sp., Phylum
Oncorhynchus mykiss, are known reservoir hosts, and the Platyhelminthes), drawn by Beth Beyerholm. Reproduced from
parasite is in Norway, Sweden, Finland, Denmark, Russia and Buchmann and Bresciani (2006).

Germany. The pathogen is normally on the fins, to a lesser

degree on the body surface, cornea and nostrils, and very
rarely on the gill apparatus. The parasite is viviparous, and
worms with three generations (a worm with an embryo
which already has an offspring) in the uterus are sometimes
seen. (Buchmann and Bresciani, 2006).
2.4. Sea lice
Sea lice are common marine ectoparasites that belong
to the order of Copepoda (Phylum Arthropoda). In North
America (United States and Canada), Ireland, Scotland,
210 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216
Fig. 4. Lepeophtheirus salmonis (Phylum Arthropoda) adult female with
egg strings removed.
Faeroes and Norway, there are mainly three species of
sea lice that parasitize farmed salmonids, Lepeophtheirus
salmonis (Fig. 4), Caligus elongatus on the North Atlantic
coasts, and Caligus clemensi on the North Pacific coast. L.
salmonis is larger and more abundant with hosts confined
mainly to salmonids while Caligus spp. are more
cosmopolitan in distribution and have broad host ranges
that include salmonids and non-salmonids (Kabata,
1979; Treasurer and Grant, 1994). L. salmonis is a major
species of interest in northern hemisphere, while in the
southern hemisphere, the major species of interest is
Caligus rogercresseyi (Fig. 5) which parasitize farmed
salmonids and non-salmonids in Chile (Boxshall and
Bravo, 2000).
Adult sea lice usually show sexual dimorphism with the
female larger than the male. The female (10–18 mm long)
has a more prominent genital segment than the male (5–
7 mm long) (Kabata, 1979) and a paired of egg strings.
Caligus has frontal lunules which are absent in
Lepeophtheirus. Life cycle of L. salmonis has 10 stages,
two free living naupliar stages, one infective copepodid
stage, four attached chalimus stages, two mobile pre-adult
stages and one adult stage (Johnson and Albright, 1991)
whilst C. rogercresseyi has eight stages, two pre-adult
stages were not observed (González and Carvajal, 2003).
3. Epizootic outbreaks of parasitosis
3.1. Cryptobiosis
3.1.1. Wild fish stocks
C. salmositica is considered a lethal pathogen of salmon
in semi-natural and intensive fish culture facilities in North
America (Bower and Thompson, 1987). Pre-smolt salmon
retained their experimental infections when transferred
from fresh to salt water and mortality due to cryptobiosis
was not reduced after they were transferred to seawater.
As indicated earlier (Biology of parasites) the prevalence of
the Cryptobia in downstream salmon migrants (pre-
smolts) ranged from 3% to 21% in some streams in the
United States. Consequently, it has been suggested that the
disease may be an important cause of salmon mortality in
Fig. 5. Female (a) and male (b) Caligus rogercresseyi (Phylum Arthropoda).
Photos courtesy of Dr. Sandra Bravo. Reproduced from Dr. Sandra Bravo’s
presentation at World Aquaculture Conference 2007. Available at http://
www.puresalmon.org/pdfs/bravo_present_sealice_WAS.pdf (last accessed
on 21 April 2009).
the sea; however, to-date no field studies have been
conducted to validate this suggestion (Woo, 2006b).
The leech vector hatches from cocoons in late summer
and early autumn. Newly hatched leeches pick up the
infection by feeding on infected sculpins; however they
prefer to feed on salmon when they are available later in
the season. Briefly, the parasite from the torrent sculpin,
Cottus rhotheus (the main reservoir host of the pathogen) is
transmitted to other fishes including the adult salmon
soon after their return from the sea to freshwater streams.
The prevalence of the parasite in sculpins can be high, is
seasonal, and can be quite variable in streams (e.g., about
60% in the United States, and 8–95% in Canada). In general,
the prevalence is higher in large sculpins than in small fish
(Woo, 2003). According to Bower and Margolis (1984)
returning adult salmon in some streams in the Fraser River,
Canada had detectable infections within 5 days of
returning to fresh water (in November) and their para-
sitaemias increased with time. Parasitaemias were very
high at spawning salmon and many fish died before they
spawned. Also, the prevalence was initially relatively low
but steadily increased to 100% by December and January –
the assumption was that as the season progressed there
were increasing numbers of leech in the streams to
transmit the pathogen.
 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216
3.1.2. Freshwater hatcheries and sea cages
Serious outbreaks of salmonid cryptobiosis (high
mortality) in hatcheries had been reported in the United
States as early as 1955. These outbreaks were mainly in
juvenile Chinook salmon, Oncorhynchus tshawytscha,
sexually mature Chinook salmon and post-spawning
rainbow trout, O. mykiss. Also, high fish mortalities in
Russian hatcheries due to cryptobiosis had been reported
in pre-spawning pink salmon, Oncorhynchus gorbuscha,
and adult Caspian salmon, S. trutta caspius. However, very
little is known about this Cryptobia other than the parasite
is morphologically similar to C. salmositica and with similar
clinical signs in infected fish. As in salmonid cryptobiosis in
North America, and the infected fish also died with massive
numbers of parasites in the blood (Woo, 2006b).
As indicated earlier (Bower and Margolis, 1984)
sexually mature salmon become infected within days
after they return to fresh water. About 50% of sexually
mature Chinook salmon brought into hatcheries as brood-
stock from streams in the United States annually die from
cryptobiosis (Woo, 2006b). Currie and Woo (2007)
confirmed experimentally that sexually mature (‘sm’)
rainbow trout were more susceptible than juveniles to
cryptobiosis. They also showed that ‘sm’ females were
more susceptible (higher parasitaemias and mortality)
than ‘sm’ males and that there was a factor(s) in the plasma
of ‘sm’ fish that promoted rapid parasite multiplication
under in vitro conditions. Also, plasma from ‘sm’ females
were much more efficient (or in higher concentrations)
than plasma from ‘sm’ males in enhancing in vitro
multiplication of the pathogen.
Outbreaks of salmonid cryptobiosis were not merely
confined to freshwater hatcheries. In 1997 the parasite
caused significant morbidity and mortality in smolts and
pre-harvest Chinook salmon in a hatchery on Vancouver
Island, Canada. It was low (about 1%) in post-smolts after
the fish were transferred to sea cages, but the disease re-
emerged later to cause higher mortality in pre-harvest fish.
According to the hatchery personnel fish mortality seemed
to be associated with age and major stressors such as
harassment by marine mammals. In 2001 another out-
break of the disease occurred in sea cages in the same
hatchery. Briefly, the parasite was detected in late 1999 in
the blood of some fish while they were still in fresh water.
Clinical cryptobiosis (e.g., exophthalmia, anemia, anorexia)
was noticed in fish in sea cages in 2001 and the parasite
was isolated for confirmation studies. Fish mortality varied
between cages (ranged from 3.3% to 24.9%). It was
suggested that the outbreak was initially because of
relapse of the infection in a few infected fish and the
pathogen was subsequently transmitted directly between
fish especially when they were brought into direct contact
with each other during grading and weighing (Woo, 2003).
3.1.3. Control and prevention
3.1.3.1. Breeding Cryptobia-resistant fish. Some naı̈ve brook
charr, S. fontinalis, cannot be infected with the parasite
(Forward et al., 1995). The resistance to Cryptobia infection
in charrs is controlled by a dominant Mendelian locus and
it is inherited by progeny (Forward et al., 1995). Briefly, the
211
pathogen is lysed in the blood via the alternative pathway
of complement activation in Cryptobia-resistant charrs
(Forward and Woo, 1996). Little is known about this type
of immunity; further studies on the inheritance of natural
resistance by progeny would be rewarding as it could be
exploited to protect fish against pathogens (Woo, 1998).
3.1.3.2. Vaccination. Two experimental vaccines (a live
attenuated Cryptobia vaccine and a DNA-vaccine) have
been developed.
(a) Live vaccine: The attenuated live vaccine infects and
produces low parasitaemia in rainbow trout. It does not
cause disease, circulates in the blood for at least 6 months,
and protects 100% of the vaccinated fish from re-infection
(Woo and Li, 1990). In trout partial protection occurs at 2
weeks post vaccination and full protection is at 3–4 weeks
post vaccination (Li and Woo, 1995). A single dose of the
vaccine protects fish for at least 24 months (Li and Woo,
1997), and it has no detectable bioenergetic cost to
juvenile rainbow trout (Beamish et al., 1996).
Fish vaccinated in fresh water and transferred to
seawater were still protected (Li and Woo, 1997). The
complement fixing antibody titres (e.g., Li and Woo, 1995)
and cell-mediated response (Mehta and Woo, 2002) in
vaccinated fish rose significantly soon after parasite
challenge (a classical secondary response). Protection is
through the production of complement fixing antibodies
and enhanced cell-mediated cytotoxicity (antibody-inde-
pendent and antibody-dependent). Also, macrophages
from vaccinated fish are much more efficient in engulfing
live parasites under in vitro conditions, especially with
antibodies (Li and Woo, 1995).
(b) DNA-vaccine: A recombinant metalloprotease-plas-
mid vaccine (DNA-vaccine) have been produced (Tan et al.,
2008). Trout injected intramuscularly with the DNA-
vaccine had a slight anaemia during the first 3–4 weeks
post-vaccination (wpv), and had detectable agglutinating
antibodies against Cryptobia between 5–7 wpv. Fish
injected with the DNA-vaccine had lower parasitaemia
when challenged, delayed peak parasitaemia and faster
recovery.
3.1.3.3. Chemotherapy. The trypanocidal drug, isometami-
dium chloride, inoculated intramuscularly into fish is
effective against C. salmositica in experimentally infected
adult rainbow trout, Atlantic salmon and juvenile Chinook
salmon. The drug also provides prophylactic protection
against the parasite (Ardelli and Woo, 1999, 2001) and its
effectiveness in protecting against naturally infected
Chinook broodstock is encouraging (Chen, M. personal
communication, 2007).
3.1.3.4. Vector control. As well as infected fish, the leech
vector is often introduced into hatcheries via the water
supply as water is nearly always from nearby streams.
Leech cocoons have been subjected to various treatments
intended to reduce their viability. The results were
encouraging, for example chlorine was suggested as a
potential chemical that could be used on cocoons in
hatcheries to control the leech population (Bower and
Thompson, 1987; Bower et al., 1985).
212 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216
3.2. Microsporidiosis (microsporidial gill disease of
salmonids, MGDS)
3.2.1. Wild fish
Although L. salmonae is common, it is not usually
considered a severe pathogen in wild salmonids or in those
reared in freshwater hatcheries.
L. salmonae was detected in wild salmonids collected
from four rivers and one lake in British Columbia, Canada.
The prevalence was 30% in pre-spawning sockeye salmon
(Oncorhynchus nerka) that had recently entered fresh water
during their return migration to spawn. L. salmonae was
also present in migrating smolts (detected using a PCR test)
(Shaw et al., 2000). The smolts were likely infected by
conspecific freshwater salmonids or by spores deposited
with eggs as high prevalence of the parasite was found in
the ovaries of sexually mature Chinook salmon (Docker
et al., 1997).
A survey of fishes captured from open waters for
salmonid pathogens was conducted in the coastal waters
of British Columbia. L. salmonae was found in Chinook
salmon, chum salmon (O. keta), coho salmon (O. kisutch),
sockeye salmon (O. nerka), and pink salmon (O. gorbuscha),
all of which were captured well away from net-pens (Kent
et al., 1998).
3.2.2. Farmed fish
All cultured salmonids (Oncorhynchus), as well as brook
trout, brown trout, and Atlantic cod are susceptible to
MGDS, however, Atlantic salmon (S. salar) are resistant
(Kent et al., 1995). The most economically significant
problems with MGDS occur in Chinook salmon and coho
salmon reared in seawater (SW) net-pen aquaculture in
British Columbia (Kent and Poppe, 1998; Constantine,
1999). The disease most often affects salmon in their
second summer when the fish are near harvesting, and
outbreak can lead to a cumulative mortality rate over 30%
(Kent and Speare, 2005; Speare et al., 2007).
3.2.3. Interaction between cultured and wild fish
MGDS is transmitted directly to fish by either ingestion
of infected tissue or by free spores in the water column, or
by co-habitation with infected fish, or by horizontal
transmission from wild marine fishes (Shaw et al.,
1998). Infections can persist after fish are transferred to
seawater, and the associated lesions in the gills can
become severe in the pen-reared salmon (Speare et al.,
1989). Several Loma species have been described from
marine fishes, but transmission studies (Shaw et al., 1997)
and comparisons of rDNA sequences from marine fish
Loma spp. (Brown et al., 1998) strongly suggest that L.
salmonae only infects salmonid fishes. A marine non-
salmonid reservoir has not been identified and L. salmonae
has been found in ocean-caught wild salmon (Kent et al.,
1998). Thus a source of the infection for fish in marine net-
pens may be wild marine-phase salmonids (Kent, 2000).
3.2.4. Control and prevention
Currently there are no approved drugs for the control of
L. salmonae infections in the aquaculture industry in
Canada (Sanchez et al., 2001b). Several drugs have been
tested in rainbow trout using a Loma challenge model.
Dietary monensin at 1000 ppm significantly reduces the
size of xenomas (Becker et al., 2002); whilst fumagillin and
albendazole have some potential value in controlling L.
salmonae infection in trout while pyrimethamine + sul-
phaquinoxaline, amprolium and metronidazole were
ineffective (Speare et al., 1999). Intraperitoneal injection
of b-1,3/1,6-glucan to rainbow trout at 100 mg per fish was
found to produce significantly fewer xenomas (Guselle
et al., 2006). A live vaccine containing a low-virulence
strain of L. salmonae, and inactivated spore-based spore
vaccine are both effective in reducing xenoma counts
(Sanchez et al., 2001a; Rodrı́guez-Tovar et al., 2006; Speare
et al., 2007).
3.3. Gyrodactylosis
3.3.1. Wild fish
Hansen et al. (2003) examined the variations in
mitochondrial DNA between Swedish and Norwegian
isolates of the parasite and they concluded that G. salaris
most likely was introduced to Norwegian rivers in the 1970s
during the transfer of Baltic-Atlantic salmon from Sweden to
Norway. The parasite is highly pathogenic to the East-
Atlantic salmon in Norway and it has devastated the
populations of salmon fry in 46 Norwegian rivers. Since the
pathogen is viviparous it spreads rapidly because it can
reproduce excessively on Norwegian salmon. Also, there are
obvious concerns the pathogen may spread to other
European countries that have the highly susceptible East-
Atlantic salmon stock (Von Gersdorff Jorgensen et al., 2008).
It has been suggested the parasite does not adversely affect
the Baltic-Atlantic salmon in Norway and Scotland basically
because the parasite and the Baltic salmon have coexisted
for thousands of years. However, in Norway there has been
no natural selection for resistance to G. salaris in East-
Atlantic salmon prior to the 1970s, consequently the
devastating outbreaks of gyrodactylosis in the rivers
(Buchmann and Bresciani, 2006).
3.3.2. Control and prevention
Drastic control programs have been instituted for over a
decade to eradicate the pathogen from affected rivers.
Rotenone added to rivers kills both the fish and parasite
with subsequent re-stocking of the treated rivers with the
same fish stock. This control measure has met with some
success although a number of treated rivers have been re-
infected. Another option is the addition of aluminium
compounds to the rivers because aluminium is quite toxic
to gyrodactylids but is tolerated by fish at concentrations
used (Soleng et al., 1999).
3.4. Caligidosis
Sea lice are among the most notorious and damaging
parasite to the salmonid farming industry in both Europe
and the Americas (Costello, 2006; Lester and Hayward,
2006). Estimated costs of sea lice control based on 2006
salmonid production statistics (FAO, 2008) are s305
million for the seven salmon cage farming countries
(Costello, 2009). The damages are not just on the fish and
 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216
the environment, but also the public perceptions towards
aquaculture (Pike and Wadsworth, 1999; Costello et al.,
2001). Because of the importance of these parasites, a
series of international conferences on sea lice, and selected
articles has been published in special issues of interna-
tional journals (Pest Management Science, 58, 2002, pp.
622–629; Aquaculture Research, 35, 2004, pp 711–805;
and Journal of Fish Diseases, 32, 2009, pp. 1–113). Despite
major research efforts over three decades, as evident from
over 800 research publications, sea lice remain a persistent
problem.
3.4.1. Sea lice in wild fish and cultured fish, and their
interactions
Sea lice infestations are endemic in most countries
where salmonid is cultured. Declines in wild salmonid
populations in recent years have led to the widespread
belief that there could be a link between sea lice in farmed
fish and this decline.
Norway is the world largest producer of farmed Atlantic
salmon, wild salmon consists only about 1% of farmed
Atlantic salmon (Heuch et al., 2005). Consequently the
potential number of L. salmonis produced by farmed
salmonids could be large (Heuch and Mo, 2001), and cross-
infestation of L. salmonis could occur between farmed and
wild hosts. By examining the carbon and nitrogen stable
isotopes levels in the sea louse, Butterworth et al. (2004)
differentiated L. salmonis from farmed Atlantic salmon and
those from wild coho salmon. Generally sea lice are larger
on wild fish than on farmed fish (Nordhagen et al., 2000),
however, size is not a reliable indicator on the origin of lice
(Boxaspen, 2006). The average prevalence of natural C.
elongatus infections of wild coastal fishes on the Norwe-
gian south east coast is 15%, and great differences are found
between fish species and seasons. Lumpfish Cyclopterus
lumpus L. spawners are the most infected fish, with gadids
at the lower end, while sea trout (S. trutta L.) and herring
Clupea harengus L. are in between. Relatively high numbers
of chalimii on found on North Sea lumpfish suggest that
offshore fish sustain an oceanic population of C. elongatus
(Heuch et al., 2007).
Scotland, the second largest salmon producing region in
Europe has marked population declines of wild sea trout (S.
trutta), particularly in the north-west where salmon
culture is concentrated. On their first visit to sea in the
spring of the year following hatching, sea trout may be
confronted with very high concentrations of infective sea
lice larval stages and quickly become infested with lice. A
burden of only 10 adult lice is thought to be sufficient to
cause mortality, especially in immature fish already under
stress (Anon., 2002). Shinn et al. (2000) successfully
differentiated sea lice on cultured salmonids from those
on wild salmonids by analyzing the elements magnesium,
vanadium, and uranium on the lice.
Canada is among the top five farmed salmon producing
country. Salmon farming on the west coast of Canada has
been linked with declining wild pink salmon (O. gorbuscha)
by the environmental groups with sea lice as the culprit. By
using mathematical models, Krkosek et al. (2007) reported
that sea lice spread from salmon farms in the Broughton
Archipelago, British Columbia, have placed wild pink
213
salmon populations ‘‘. . . on a trajectory toward rapid local
extinction. . .’’ and that ‘‘. . . a 99% collapse in pink salmon
population abundance is expected in four salmon genera-
tions.’’ However, Riddell et al. (2008) counter-argued that
the risks were overstated as the dataset used for the
prediction were selected (excluding 2004 high return data,
and data from Glendale River which produces the largest
population of pink salmon), and the predictions were
inconsistent with recent observations of pink salmon
returns to the Broughton Archipelago. It is interested to
know that besides salmonids, wild sticklebacks (Gaster-
osteus aculeatus) appear to serve as temporary hosts for L.
salmonis, suggesting a role of this fish in the epizootiology
of the parasite (Jones et al., 2006). There is general
agreement between scientists and environmental groups
that sea lice pass freely to and from wild salmon; however,
the debate is whether the transfer of sea lice from the
farmed salmon to the wild salmon is on a sufficient scale to
have an impact (Anon., 2006). In assessing and managing
wild pink salmon in BC, all potential impacts on the wild
populations, including sea lice, should be acknowledged in
developing an effective management strategy (Riddell
et al., 2008). Brooks (2009) advocated to develop and
implement an area management plan coordinating sea lice
management efforts by all producers and close monitoring
of therapeutants efficacy and conducting specific field
bioassays as suggested by SEARCH (2004).
3.4.2. Prevention and control
Currently the salmon farming industry adopts the
integrated pest management (IPM) approach to deal with
sea lice which includes farm fallowing, regular monitoring
of lice burden, chemical control (use of parasiticides),
biological control (use of cleaner fish), monitoring and
reporting of drug resistance, strategic rotation of medi-
cines (Lees et al., 2008). With a limited range of approved
chemicals to choose and increasing speed of resistance
development, sea lice control remains the biggest problem
faced by the industry.
Parasiticides can be topical (bath) treatment by
enclosing the cage in canvas skirts or tarpaulins or they
can be used as oral (in-feed) treatment where the
medication is mixed with feed pellets and fed to the fish.
Bath treatments usually have quicker action than oral
treatments, however, it is very difficult to have a uniform
distribution of active compound within the salmon cage.
‘Hot’ spots (areas with over dose) are common which may
be toxic to fish (Roth et al., 1993), while cold spots (under
dose) lead to lice not being removed, and causing re-
infection. Bath treatment is labour-intensive and it is very
difficult to treat all cages in one site within the same day, so
lice from untreated fish can transfer to re-infect previously
treated fish. However, oral treatment takes a few days to
build up tissue concentration, and fish that are not eating
well will not get adequate amount of medicine, further
more there is a withdrawal period that is regulated strictly
by the authorities (Costello, 2006), but it offers sustained
periods of louse clearance (Stone et al., 2000a,b,c).
Organophosphates (OPs, trichlorfon and dichlorvos)
were the first chemotherapeutants used to control sea lice
as bath treatment. They were replaced by azamethiphos
214 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216
(also an organophosphate), hydrogen peroxide, and
synthetic pyrethroids (cypermethrin and deltamethrin).
The oral treatments are the chitin synthesis inhibitors
diflubenzuron and teflubenzuron, and the widely used
emamectin benzoate (Grant, 2002; Costello, 2006).
OPs kill 100% of post chalimus stage lice, but have little
efficacy against chalimi (Roth et al., 1996). Repeated
exposure to organophosphates can lead to resistance
development (Jones et al., 1992; Fallang et al., 2004) and
this has prompted for higher dosage and reduction of
safety margins in fish (Roth et al., 1993).
Hydrogen peroxide can dislodge 85–100% of sea lice at
1.5 g/L for a 20 min bath (Thomassen, 1993), however it is
toxic to fish when the temperature is over 14 8C (Alder-
man, 2002). Hydrogen peroxide can delay chalimus
development, but some pre-adult and adult lice recovered
and re-attached to fish (Johnson et al., 1993; McAndrew
et al., 1998; Pozo et al., 2008). Prolonged exposure also
caused gill damage (Thomassen, 1993) and resistance to
Hydrogen peroxide was also reported (Treasurer et al.,
2000).
Synthetic pyrethroids are currently the most popular
compounds used for bath treatment. These interventions
are applied more frequently toward the end of the
production cycle when salmon are larger, and oral
treatments are consequently more costly (Lees et al.,
2008). Furthermore, bath treatment requires almost none
withdrawal period. Resistance or reduced sensitivity to
these compounds was reported in Norway (Sevatdal and
Horsberg, 2003; Sevatdal et al., 2005).
Most recently, insect growth regulators (IGRs) have
been developed as in-feed sea lice treatment, they inhibit
chitin synthesis and thus not effective against adult lice.
Diflubenzuron was effective at an oral dose of 75 mg/kg
BW/day for 14 days, while teflubenzuron was effective at
10 mg/kg BW/day for 7 days (Branson et al., 2000; Ritchie
et al., 2002). The major disadvantage of IGRs is their
toxicity to marine crustaceans (Burridge et al., 2004;
Waddy et al., 2007). Emamectin benzoate (EB) was
effective at an oral dose of 50 mg/kg BW/day for 7
consecutive days. There have been anecdotal reports of
reduced sensitivity and potential resistance of sea lice to
EB, particularly in Chile. Most recently, Lees et al. (2008)
reported that not all treatments were effective and there
was a reduction in efficacy over a period of 5 years in
Scottish salmon farms.
4. Conclusions
It is obvious from this brief discussion that there is
transfer of (either man-made or natural) parasites from
farmed to wild fish stocks and vice versa. When this occurs
the parasite can cause severe epizootics (with high fish
mortalities) in either hatcheries or cage cultures or in
natural habitats (e.g., rivers).
Conflict of interest statement
FCG is an employee of Novartis Animal Health Canada
Inc., Victoria, Prince Edward Island, Canada and PTKW has
no financial nor personal relationships with other people
or organizations that could inappropriately influence
(bias) the contents of this publication.
References
Alderman, 2002. Trends in therapy and prophylaxis. Bull. Euro Assoc. Fish
Path. 22, 117–125.
Anon., 2002. Review and synthesis of the environmental impacts of
aquaculture. The Scottish Association for Marine Science and Napier
University. Scottish Executive Central Research Unit, UK, pp. 24–27.
Available at: http://www.scotland.gov.uk/Resource/Doc/46951/
0030621.pdf (last accessed on 29 April 2009).
Anon., 2006. Aquaculture Association of Canada. Available at: http://
www.aquacultureassociation.ca/news/Sea_Lice_Fact_Sheet.pdf (last
accessed on 9 March 2009).
Ardelli, B.F., Woo, P.T.K., 1999. The therapeutic use of isometamidium
chloride against Cryptobia salmositica in rainbow trout (Oncorhynchus
mykiss). Dis. Aqua. Org. 37, 195–203.
Ardelli, B.F., Woo, P.T.K., 2001. Therapeutic and prophylactic effects of
isometamidium chloride (Samorin) against the haemoflagellate Cryp-
tobia salmositica in chinook salmon (Oncorhynchus tshawytscha).
Parasitol. Res. 87, 18–26.
Bader, J.A., Shotts Jr., E.B., Steffens, W.L., Lom, J., 1998. Occurrence of Loma
cf. salmonae in brook, brown and rainbow trout from Buford trout
hatchery, Georgia, USA. Dis. Aquat. Organ. 34, 211–216.
Beamish, F.W.H., Sitja-Bobadilla, A., Jebbink, J.A., Woo, P.T.K., 1996. Bioe-
nergetic cost of cryptobiosis in fish: rainbow trout (Oncorhynchus
mykiss) infected with Cryptobia salmositica and with an attenuated
live vaccine. Dis. Aquat. Organ. 25, 1–8.
Becker, J.A., Speare, D.J., Daley, J., Dick, P., 2002. Effects of monensin dose
and treatment time on xenoma reduction in microsporidial gill dis-
ease in rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis. 25,
673–680.
Becker, J.A., Speare, D.J., 2007. Transmission of the microsporidian gill
parasite, Loma salmonae. Anim. Health Res. Rev. 8, 59–68.
Bower, S.M., Margolis, L., 1984. Distribution of Cryptobia salmositica, a
haemoflegellate of fishes in British Columbia and the seasonal pattern
of infection in a coastal river. Can. J. Zool. 62, 2512–2518.
Bower, S.M., Thompson, A.B., 1987. Hatching of the Pacific salmon leech
(Piscicola salmositica) from cocoons exposed to various treatments.
Aquaculture 66, 1–8.
Bower, S.M., Margolis, L., MacKay, R.J., 1985. Potential usefulness of
chlorine for controlling Pacific salmon leeches, Piscicola salmositica
in hatcheries. Can. J. Fish. Aquat. Sci. 42, 1986–1993.
Boxshall, G.A., Bravo, S., 2000. On the identity of the common Caligus
(Copepoda: Siphonostomatoida: Caligidae) from salmonid netpen
systems in southern Chile. Contrib. Zool. 69, 137–146.
Branson, E.J., Rønsberg, S.S., Ritchie, G., 2000. Efficacy of teflubenzuron
(Calicide1) for the treatment of sea lice, Lepeophtheirus salmonis
(Krøyer 1838), infestations of farmed Atlantic salmon (Salmo salar
L.). Aqua. Res. 31, 861–867.
Brooks, K.M., 2009. Considerations in developing an integrated pest
management programme for control of sea lice on farmed salmon
in Pacific Canada. J. Fish Dis. 32, 59–73.
Brown, A.M.V., Kent, M.L., Adamson, M.L., 1998. Phylogeny of microspor-
idian parasites of fishes reveals dispersed ribosomal RNA genes in
relatives of Loma salmonae. In: Program guide and abstracts – 73rd
Annual Meeting of the American Society of Parasitologists, 16–20
August. American Society of Parasitologists, Kona, Hawaii, p. 80 pp..
Bruno, D.W., Collins, R.O., Morrison, C.M., 1995. The occurrence of Loma
salmonae (Protozoa: Microspora) in farmed rainbow trout, Oncor-
hynchus mykiss Walbaum, in Scotland. Aquaculture 133, 341–344.
Boxaspen, K., 2006. A review of the biology and genetics of sea lice. ICES J.
Mar. Sci. 63, 1304–1316.
Buchmann, K., Bresciani, J., 2006. Monogenea (Phylum Platyhelminthes),.
In: Woo, P.T.K. (Ed.), Fish Diseases and Disorders. Protozoan and
Metazoan Infections, 2nd ed., vol. 1. CABI Publishing, Wallingford,
U.K., pp. 297–344.
Burridge, L.E., Hamilton, N., Waddy, S.L., Haya, K., Mercer, S.M., Green-
halgh, R., Tauber, R., Radecki, L.S., Wislocki, P.G., Endris, R.G., 2004.
Acute toxicity of emamectin benzoate (SLICETM) in fish feed to
American lobster, Homarus americanus. Aqua. Res. 35, 713–722.
Butterworth, K.G., Li, W.M., McKinley, R.S., 2004. Carbon and nitrogen
stable isotopes: a tool to differentiate between Lepeophtheirus
salmonis and different salmonid host species? Aquaculture 241,
529–538.
Constantine, J., 1999. Fact Sheet: Estimating the Cost of Loma salmonae to
B.C. Aquaculture. Animal Health Branch, Aquaculture Program, BC
 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216
Ministry of Agriculture and Food, Abbotsford Agriculture Centre,
Abbotsford.
Costello, M.J., Grant, A., Davies, I.M., Cecchini, S., Papoutsoglou, S., Quigley,
D., Saroglia, M., 2001. The control of chemicals used in aquaculture in
Europe. J. Appl. Ichthyol. 17, 173–180.
Costello, M.J., 2006. Ecology of sea lice parasitic on farmed and wild fish.
Trends Parasitol. 22, 475–483.
Costello, M.J., 2009. The global economic cost of sea lice to the salmonid
farming industry. J. Fish Dis. 32, 115–118.
Currie, J.L.M., Woo, P.T.K., 2007. Susceptibility of sexually mature rainbow
trout, Oncorhynchus mykiss to experimental cryptobiosis caused by
Cryptobia salmositica. Parasitol. Res. 101, 1057–1067.
Docker, M.F., Devlin, R.H., Richard, J., Kent, M.L., 1997. Sensitive and
specific polymerase chain reaction assay for detection of Loma sal-
monae (Microsporea). Dis. Aquat. Organ. 29, 41–48.
Dykova, I., 2006. Phylum microspora. In: Woo, P.T.K. (Ed.), Fish Diseases
and Disorders. Protozoan and Metazoan Infections, 2nd ed., vol. 1.
CABI Publishing, Wallingford, U.K, pp. 205–229.
Fallang, A., Ramsay, J.M., Sevatdal, S., Burka, J.F., Jewess, P., Hammell,
K.L., Horsbergs, T.E., 2004. Evidence for occurrence of an organopho-
sphate-resistant type of acetylcholinesterase in strains of sea
lice (Lepeophtheirus salmonis Krøyer). Pest Manage. Sci. 60, 1163–
1170.
FAO Fisheries and Aquaculture Information and Statistics Service, 2008.
Aquaculture Production 1950-2006. FISHSTAT Plus-Universal Soft-
ware for Fishery Statistical Time Series [Online or CD-ROM]. Food and
Agriculture Organization of the United Nations. Available at: http://
www.fao.org/fi/statist/FISOFT/FISHPLUS.asp (last accessed on 1
March 2009).
Forward, G.M., Woo, P.T.K., 1996. An in vitro study on the mechanism of
innate immunity in Cryptobia-resistant brook charr (Salvelinus fonti-
nalis) against Cryptobia salmositica. Parasitol. Res. 82, 238–241.
Forward, G.M., Ferguson, M.M., Woo, P.T.K., 1995. Susceptibility of brook
charr, Salvelinus fontinalis to the pathogenic haemoflagellate, Crypto-
bia salmositica, and the inheritance of innate resistance by progenies
of resistant fish. Parasitology 111, 337–345.
González, L., Carvajal, J., 2003. Life cycle of Caligus rogercresseyi, (Cope-
poda: Caligidae) parasite of Chilean reared salmonids. Aquaculture
220, 101–117.
Grant, A.N., 2002. Medicines for sea lice. Pest Manage. Sci. 58, 521–527.
Guselle, N.J., Markham, R.J., Speare, D.J., 2006. Intraperitoneal adminis-
tration of beta-1,3/1,6-glucan to rainbow trout, Oncorhynchus mykiss
(Walbaum), protects against Loma salmonae. J. Fish Dis. 29, 375–381.
Hansen, H., Buchmann, K., Bakke, T.A., 2003. Mitochondrial DNA variation
of Gyrodactylus spp. (Monogenea, Gyrodactylidae) populations infect-
ing Atlantic salmon, grayling and rainbow trout in Norway and
Sweden. Int. J. Parasitol. 33, 1471–1478.
Hauck, A.K., 1984. A mortality and associated tissue reactions of chinook
salmon, Oncorhynchus tshawytscha (Walbaum), caused by the micro-
sporidian Loma sp. J. Fish Dis. 7, 217–229.
Heuch, P.A., Bjørn, P.A., Finstad, B., Holst, J.C., Asplin, L., Nilsen, F., 2005. A
review of the Norwegian ‘‘National action plan against salmon lice on
salmonids’’: the effect on wild salmonids. Aquaculture 246, 79–92.
Heuch, P.A., Mo, T.A., 2001. A model of salmon louse production in
Norway: effects of increasing salmon production and public manage-
ment measures. Dis. Aquat. Organ. 45, 145–152.
Heuch, P.A., Øines, Ø., Knutsen, J.A., Schram, T.A., 2007. Infection of wild
fishes by the parasitic copepod Caligus elongatus on the south east
coast of Norway. Dis. Aquat. Organ. 77, 149–158.
Jones, M.W., Sommerville, C., Wootten, R., 1992. Reduced sensitivity of the
salmon louse, Lepeophtheirus salmonis, to the organophosphate
dichlorvos. J. Fish Dis. 15, 197–202.
Jones, S.R., Prosperi-Porta, G., Kim, E., Callow, P., Hargreaves, N.B., 2006.
The occurrence of Lepeophtheirus salmonis and Caligus clemensi (Cope-
poda: Caligidae) on three-spine stickleback Gasterosteus aculeatus in
coastal British Columbia. J. Parasitol. 92, 473–480.
Johnson, S.C., Albright, L.J., 1991. The developmental stages of
Lepeophtheirus salmonis (Kroyer, 1837) (Copepoda, Caligidae). Can.
J. Zool. 69, 929–950.
Johnson, S.C., Constible, J.M., Richard, J., 1993. Laboratory investigations of
the toxicological and histopathological effects of hydrogen peroxide
to salmon and its efficacy against the salmon louse Lepeophtheirus
salmonis. Dis. Aquat. Organ. 17, 197–204.
Kabata, Z., 1979. Parasitic Copepoda of British Fishes. The Ray Society,
London, 179 pp.
Keeling, P.J., Fast, N.M., 2002. Microsporidia: biology and evolution of
highly reduced intracellular parasites. Annu. Rev. Microbiol. 56, 93–
116.
Kent, M.L., 1992. Diseases of seawater netpen-reared salmonid fishes in
the Pacific Northwest. Can. Spec. Publ. Fish Aquat. Sci. 116, 39–42.
215
Kent, M.L., Elliott, D.G., Groff, J.M., Hedrick, R.P., 1989. Loma salmonae
(Protozoa: Microspora) infections in seawater reared coho salmon
Oncorhynchus kisutch. Aquaculture 80, 211–222.
Kent, M.L., Dawe, S.C., Speare, D.J., 1995. Transmission of Loma salmonae
(Microsporea) to chinook salmon in sea water. Can. Vet. J. 36, 98–102.
Kent, M.L., Poppe, T.T., 1998. Diseases of Seawater Netpen-reared Salmo-
nids. Pacific Biological Station Press, Nanaimo, British Columbia,
Canada, 138 pp.
Kent, M.L., Traxler, G.S., Kieser, D., Richard, J., Dawe, S.C., Shaw, R.W.,
Prosperi-Porta, G., Ketcheson, J., Evelyn, T.P.T., 1998. Survey of sal-
monid pathogens in ocean-caught fishes in British Columbia, Canada.
J. Aquat. Anim. Health 10, 211–219.
Kent, M.L., 2000. Marine netpen farming leads to infections with some
unusual parasites. Int. J. Parasitol. 30, 321–326.
Kent, M.L., Speare, D.J., 2005. Review of the sequential development of
Loma salmonae (Microsporidia) based on experimental infections of
rainbow trout (Oncorhynchus mykiss) and Chinook salmon (O. tsha-
wytscha). Folia Parasitol. (Praha) 52, 63–68.
Krkosek, M., Ford, J.S., Morton, A., Lele, S., Myers, R.A., Lewis, M.A., 2007.
Declining wild salmon populations in relation to parasites from farm
salmon. Science 318, 1772–1775.
Lees, F., Baillie, M., Gettinby, G., Revie, C.W., 2008. The efficacy of ema-
mectin benzoate against infestations of Lepeophtheirus salmonis on
farmed Atlantic salmon (Salmo salar L) in Scotland, 2002–2006. PLoS
ONE 3, e1549.
Lester, R.J.G., Hayward, C.J., 2006. Phylum Arthropoda. In: Woo, P.T.K.
(Ed.), Fish Diseases and Disorders. Protozoan and Metazoan Infec-
tions., 2nd ed., vol.1. CABI Publishing, Wallingford, U.K, pp. 466–565.
Li, S., Woo, P.T.K., 1995. Efficacy of a live Cryptobia salmositica vaccine, and
the mechanism of protection in vaccinated Oncorhynchus mykiss
(Walbaum) against cryptobiosis. Vet. Immunol. Immunopathol. 48,
343–353.
Li, S., Woo, P.T.K., 1997. Vaccination of rainbow trout, Oncorhynchus
mykiss (Walbaum) against cryptobiosis: efficacy of the vaccine in
fresh and sea water. J. Fish Dis. 20, 369–374.
Magor, B.G., 1987. First report of Loma sp. (Microsporida) in juvenile coho
salmon (Oncorhynchus kisutch) from Vancouver Island, British Colum-
bia. Can. J. Zool. 65, 751–752.
McAndrew, K., Sommerville, C., Wootten, R., Bron, J.e., 1998. The effects of
hydrogen peroxide treatment on different life-cycle stages of the
salmon louse, Lepeophtheirus salmonis (Krøyer 1837). J. Fish Dis. 21,
221–228.
Mehta, M., Woo, P.T.K., 2002. Acquired cell-mediated protection in rain-
bow trout, Oncorhynchus mykiss against the haemoflagellate, Crypto-
bia salmositica. Parasitol. Res. 88, 956–962.
Morrison, C.M., Sprague, V., 1983. Loma salmonae (Putz, Hoffman and
Dunbar, 1965) in the rainbow trout, Salmo gairdneri Richardson, and L.
fontinalis sp. nov. (Microsporida) in the brook trout, Salvelinus fonti-
nalis (Mitchill). J. Fish Dis. 6, 345–353.
Nordhagen, J., Heuch, P., Schram, T., 2000. Size as indicator of origin of
salmon lice, Lepeophtheirus salmonis (Copepoda: Caligidae). Contrib.
Zool. 69, 99–108.
Pozo, V., Bravo, S., Erranz, F., Bassaletti, P., 2008. Monitoring the effec-
tiveness of hydrogen peroxide in the control of sea lice Caligus
rogercresseyi in Chile. 7th International Sea Lice Conference, Puerto
Varas, Chile (Abstract).
Pike, A.W., Wadsworth, S.L., 1999. Sea lice on salmonids: their biology and
control. Adv. Parasit. 44, 233–337.
Putz, R.E., Hoffman, G.L., Dunbar, C.E., 1965. Two new species of Pleisto-
phora from North American fish with a synopsis of Microsporidia of
freshwater and euryhaline species. J. Protozool. 12, 228–236.
Riddell, B.E., Beamish, R.J., Richards, L.J., Candy, J.R., 2008. Comment on
‘‘Declining Wild Salmon Populations in Relation to Parasites from
Farm Salmon’’. Science 322, 1790–11790.
Ritchie, G., Rønsberg, S.S., Hoff, K.A., Branson, E.J., 2002. Clinical efficacy of
teflubenzuron (Calicide) for the treatment of Lepeophtheirus salmonis
infestations of farmed Atlantic salmon Salmo salar at low water
temperatures. Dis. Aquat. Organ. 51, 101–106.
Rodrı́guez-Tovar, L.E., Becker, J.A., Markham, R.J., Speare, D.J., 2006. Induc-
tion time for resistance to microsporidial gill disease caused by Loma
salmonae following vaccination of rainbow trout (Oncorhynchus
mykiss) with a spore-based vaccine. Fish Shellfish Immunol. 21,
170–175.
Roth, M., Richards, R.H., Sommerville, C., 1993. Current practices in the
chemotherapeutic control of sea lice infestations in aquaculture: a
review. J. Fish Dis. 16, 1–26.
Roth, M., Richards, R.H., Dobson, D.P., Rae, G.H., 1996. Field trial on the
efficacy of the organophosphate compound Azimethiphos for the
control of sea lice (Copepoda, Caligidae) infestations of farmed Atlan-
tic salmon (Salmo salar). Aquaculture 140, 197–217.
216 F.C. Guo, P.T.K. Woo / Veterinary Parasitology 163 (2009) 207–216
Sanchez, J.G., Speare, D.J., Markham, R.J.F., Jones, S.R.M., 2001a. Experi-
mental vaccination of rainbow trout against Loma salmonae using a
live low-virulence variant of L. salmonae. J. Fish Biol. 59, 442–448.
Sanchez, J.G., Speare, D.J., Markham, R.J.F., Wright, G.M., Kibenge, F.S.B.,
2001b. Localization of the initial development stages of Loma salmo-
nae in rainbow trout (Oncorhynchus mykiss). Vet. Pathol. 38, 540–546.
SEARCH, 2004. Sea lice resistance to chemotherapeutants: a handbook in
resistance management. Prepared in association with the EU-funded
project SEARCH (QLK2-CT-00809). Available at http://www.rotham-
sted.bbsrc.ac.uk/pie/search-EU/Handbook.pdf (last accessed on 18
April 2009).
Sevatdal, S., Horsberg, T.E., 2003. Determination of reduced sensitivity in
sea lice (Lepeophtheirus salmonis) against the pyrethroid deltamethrin
using bioassays and probit modelling. Aquaculture 218, 21–31.
Sevatdal, S., Fallang, A., Ingebrigtsen, K., Horsberg, T.E., 2005. Monoox-
ygenase mediated pyrethroid detoxification in sea lice
(Lepeophtheirus salmonis). Pest. Manage. Sci. 61, 772–778.
Shaw, R.W., Kent, M.L., Docker, M.F., Devlin, R.H., Brown, A., Adamson,
M.L., 1997. A new Loma species (Microsporea) in shiner perch (Cym-
atogaster aggregata). J. Parasitol. 83, 296–301.
Shaw, R.W., Kent, M.L., Adamson, M.L., 1998. Modes of transmission of
Loma salmonae (Microsporidia). Dis. Aquat. Organ. 33, 151–156.
Shaw, R.W., Kent, M.L., Brown, A.M.V., Whipps, C.M., Adamson, M.L., 2000.
Experimental and natural host specificity of Loma salmonae (Micro-
sporidia). Dis. Aquat. Organ. 40, 131–136.
Shinn, A., Bron, J., Gray, D., Sommerville, C., 2000. Elemental analysis of
Scottish populations of the ectoparasitic copepod Lepeophtheirus
salmonis. Contrib. Zool. 69, 79–87.
Soleng, A., Poleo, A.B.S., Alstad, N.E.W., Bakke, T.A., 1999. Aqueous alu-
minium eliminates Gyrodactylus salaris (Platyhelminthes, Monoge-
nea) infections in Atlantic salmon. Parasitology 119, 19–25.
Speare, D.J., Brackett, J., Ferguson, H.W., 1989. Sequential pathology of the
gills of coho salmon with a combined diatom and microsporidian gill
infection. Can. Vet. J. 30, 571–575.
Speare, D.J., Arsenault, G.J., Buote, M.A., 1998. Evaluation of rainbow trout
as a model for use in studies on pathogenesis of the branchial
microsporidian Loma salmonae. Contemp. Top. Lab. Anim. Sci. 37,
68–71.
Speare, D.J., Athanassopoulou, F., Daley, J., Sanchez, J.G., 1999. A preli-
minary investigation of alternatives to fumagillin for the treatment of
Loma salmonae infection in rainbow trout. J. Comp. Pathol. 121, 241–
248.
Speare, D.J., Markham, R.J.F., Guselle, N.J., 2007. Development of an
effective whole-spore vaccine to protect against microsporidial gill
disease in rainbow trout (Oncorhynchus mykiss) by using a low-
virulence strain of Loma salmonae. Clin. Vaccine Immunol. 14,
1652–1654.
Stone, J., Sutherland, I.H., Sommerville, C., Richards, R.H., Endris, R.G.,
2000a. The duration of efficacy following oral treatment with
emamectin benzoate against infestations of sea lice, Lepeophtheirus
salmonis (Krøyer), in Atlantic salmon Salmo salar L. J. Fish Dis. 23,
185–192.
Stone, J., Sutherland, I.H., Sommerville, C., Richards, R.H., Varma, K.J.,
2000b. Commercial trials using emamectin benzoate to control sea
lice Lepeophtheirus salmonis infestations in Atlantic salmon Salmo
salar. Dis. Aquat. Organ. 41, 141–149.
Stone, J., Sutherland, I.H., Sommerville, C., Richards, R.H., Varma, K.J.,
2000c. Field trials to evaluate the efficacy of emamectin benzoate
in the control of sea lice, Lepeophtheirus salmonis (Krøyer) and Caligus
elongatus Nordmann, infestations in Atlantic salmon Salmo salar L.
Aquaculture 186, 205–219.
Tan, C.W., Jesudhasan, R.R.R., Woo, P.T.K., 2008. Towards a DNA vaccine
against salmonid cryptobiosis caused by Cryptobia salmositica. Para-
sitol. Res. 102, 265–275.
Thomassen, J.M., 1993. Hydrogen peroxide as a delousing agent for
Atlantic salmon. In: Boxshall, G.A., Defaye, D. (Eds.), Pathogens
of Wild and Farmed Fish. Sea Lice, Ellis Horwood, New York, pp.
290–295.
Treasurer, J., Grant, A., 1994. ‘Second’ louse species must not be ignored.
Fish Farmer 17, 46–47.
Treasurer, J.W., Wadsworth, S., Grant, A., 2000. Resistance of sea lice
Lepeophtheirus salmonis (Krøyer), to hydrogen peroxide on farmed
Atlantic salmon, Salmo salar. Aqua. Res. 31, 855–860.
Von Gersdorff Jorgensen, L., Heinecke, R.D., Kania, P., Buchmann, K., 2008.
Occurrence of gyrodactylids on wild Atlantic salmon, Salmo salar L., in
Danish rivers. J. Fish Dis. 31, 127–134.
Waddy, S.L., Merritta, V.A., Hamilton-Gibsona, M.N., Aikena, D.E., Burrid-
gea, L.E., 2007. Relationship between dose of emamectin benzoate
and molting response of ovigerous American lobsters (Homarus amer-
icanus). Ecotox. Environ. Safe. 67, 95–99.
Wales, J.M., Wolf, H., 1955. Three protozoan diseases of trout in California.
Calif. Fish Game 41, 183–187.
Woo, P.T.K., 1998. Protection against Cryptobia (Trypanoplasma) salmosi-
tica and salmonid cryptobiosis. Parasitol. Today 14, 272–277.
Woo, P.T.K., 2003. Cryptobia (Trypanoplasma) salmositica and salmonid
cryptobiosis. J. Fish Dis. 26, 627–646.
Woo, P.T.K., 2006a. Strategies against piscine parasitosis: the Cryptobia
model. In: Phang, S.M., Aisyah, S., Chong, V.C., George, M., Siti Aisyah,
M., Ho, S.C. (Eds.), Innovations and Technologies in Oceanography for
Sustainable Development. Maritime Research Centre. University of
Malaya, Kuala Lumpur, Malaysia, pp. 17–28.
Woo, P.T.K., 2006b. Diplomonadida (Phylum Parabasalia) and Kinetoplas-
tea (Phylum Euglenozoa). In: Woo, P.T.K. (Ed.), Fish Diseases and
Disorders. Protozoan and Metazoan Infections., 2nd ed., vol. 1. CABI
Publishing, Wallingford, U.K, pp. 46–115.
Woo, P.T.K., Li, S., 1990. In vitro attenuation of Cryptobia salmositica and its
use as a live vaccine against cryptobiosis in Oncorhynchus mykiss. J.
Parasitol. 76, 752–755.