A Review of the Impact of Parasitic Copepods on Marine Aquaculture

A Review of the Impact of Parasitic Copepods on Marine Aquaculture

Stewart C. Johnson1,*, Jim W. Treasurer2, Sandra Bravo3, Kazuya Nagasawa4, and Zbigniew

Kabata5

1Institute for Marine Biosciences, National Research Council, Canada, 1411 Oxford St., Halifax, Nova Scotia B3H 2Z1, Canada

Tel:902-426-2630. Fax: 902-426-9413. E-mail: Stewart.Johnson@nrc.ca

2Sea Fish Industry Authority, Marine Farming Unit, Ardtoe, Acharacle, Argyll PH34 4LD, Scotland

E-mail: J_Treasurer@seafish.co.uk

3Instituto de Acuicultura, Universidad Austral de Chile, Puerto Mont Campus, Puerto Mont, Chile

E-mail: sbravo@uach.cl

4Nikko Branch, National Research Institute of Aquaculture, Fisheries Research Agency, Chugushi, Nikko, Tochigi, 321-1661, Japan

E-mail: ornatus@fra.affrc.go.jp

5Biological Sciences Branch, Department of Fisheries and Oceans, Pacific Biological Station, Nanaimo V9R 5K6, B.C., Canada

(Accepted January 18, 2004)

Stewart C. Johnson, Jim W. Treasurer, Sandra Bravo, Kazuya Nagasawa, and Zbigniew Kabata (2004) A

review of the impact of parasitic copepods on marine aquaculture. Zoological Studies 43(2): 229-243.

Parasitic copepods are common on cultured and wild marine finfish, and there is a substantive literature

describing their taxonomy, life cycles, and host ranges. Although many species have long been recognized to

have the potential to affect the growth, fecundity, and survival of their hosts, it has only been with the develop-

ment of semi-intensive and intensive aquaculture that their importance as disease-causing agents has become

evident. Members of the family Caligidae are the most commonly reported species on fish reared in brackish

and marine waters. These species, often referred to as sea lice, are responsible for most disease outbreaks.

The impacts of sea lice on marine salmonid aquaculture are well documented, with catastrophic losses report-

ed for disease outbreaks that have resulted in high levels of mortality. With the development of a variety of

treatments and management strategies to reduce infection levels, mortality caused by sea lice has been greatly

reduced. At present, economic losses due to sea lice are primarily from the costs of treatments, the costs of

the management strategies, the costs associated with reduced growth rates that are a direct result of infection

and/or treatment, and the costs of carcass downgrading at harvest. Indirect and direct losses due to sea lice in

salmonid aquaculture globally are estimated to be greater than US$100 million annually. In other areas of

marine aquaculture, the impact of parasitic copepods is not well documented. This is especially true for

species such as Atlantic halibut, Atlantic cod, turbot, and haddock that have only recently entered commercial-

scale production. This review discusses the global importance of parasitic copepods as disease-causing

agents in marine aquaculture. We also provide a brief review of the environmental and husbandry factors that

may affect parasitic copepod abundance and the potential roles that parasitic copepods play as vectors for

other disease agents. http://www.sinica.edu.tw/zool/zoolstud/43.2/229.pdf

Key words: Sea lice, Disease, Caligidae.

Zoological Studies 43(2): 229-243 (2004)

Parasitic copepods are common on cultured

and wild marine finfish, and there is a vast litera-

ture describing their taxonomy and host ranges.

Many of these species have long been recognized

to have the potential to affect the growth, fecundity

and survival of wild hosts (White 1940, Kabata

1958, Hewitt 1971, Neilson et al. 1987, Johnson et

al. 1996). With the development of semi-intensive

and intensive brackish water and marine aquacul-

ture, the importance of parasitic copepods as dis-

ease causing agents has become more evident.

Members of the family Caligidae, also often

referred to as sea lice, are the most commonly

reported species on marine and brackish water

229

*To whom all correspondence and reprints requests should be addressed.

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Zoological Studies 43(2): 229-243 (2004)

230

cultured fish throughout the world, accounting for

approximately 61% of all reports (Tables 1, 2).

Members of this family have been responsible for

most of the documented disease outbreaks.

Parasitic copepods feed on host mucous, tis-

sues, and blood, and their attachment and feeding

activities are responsible for any primary disease

that develops. The relationship of the number of

parasitic copepods to severity of the disease is

dependent on 1) the size and age of the fish, 2)

the general state of health of the fish, and 3) the

species of copepod and the developmental stages

present (Pike and Wadsworth 1999 and references

therein). Losses associated with disease are the

result of direct mortality, mortality due to secondary

infections, reduced growth, loss of carcass value,

and costs associated with treatment (Lin et al.

1994, Pike and Wadsworth 1999, Ho 2000).

Caligid copepods generally have direct life

cycles consisting of 2 free-living planktonic nau-

plius stages, 1 free-swimming infectious copepodid

stage, 4 to 6 attached chalimus stages, 1 or 2

preadult stages, and 1 adult stage (Johnson and

Albright 1991a, Ogawa 1992, Lin et al. 1996, Lin et

al. 1997, Pike and Wadsworth 1999). Notable

exceptions include Caligus punctatus and C. elon-

gatus in which the preadult stage is reported not to

occur (Kim 1993, Piasecki and MacKinnon 1995,

Piasecki 1996). Through their attachment and

feeding activities, copepodid and chalimus stages

cause variable amounts of localized damage that

elicit only minor host tissue responses in most host

species (Bron et al. 1991, Johnson and Albright

1992, Roubal 1994, Pike and Wadsworth 1999).

However when present in high numbers especially

on gills, chalimus stages can cause significant

pathology that can result in mortality (Lin et al.

1994, Wu et al. 1997). In most cases, the preadult

and adult stages are not very invasive, generally

not penetrating deeply into host tissues and only

causing minor tissue damage (Ono 1984, Ogawa

1992, Roubal 1994, Johnson et al. 1996). How-

ever, in situations of severe disease such as is

seen in Atlantic salmon (Salmo salar) when infect-

ed by high numbers of Lepeophtheirus salmonis,

extensive areas of skin erosion and hemorrhaging

on the head and back, and a distinct area of ero-

sion and sub-epidermal hemorrhage in the peri-

anal region can be seen (Brandal and Egidius

1979, Pike and Wadsworth 1999). The formation

of similar skin and head lesions on Atlantic

salmon, Atlantic halibut (Hippoglossus hippoglos-

sus), and the rabbit fish (Siganus fuscescens) has

also been reported as the result of infection with

Caligus spp. (Wootten et al. 1982, Lin et al. 1996,

Bergh et al. 2001). Infection of the gills and gill

cavity of black sea bream (Acanthopagrus

schlegeli) by juvenile and adult Caligus multi-

spinosus was reported to cause gill congestion,

other damage, and mucous proliferation (Lin et al.

1994). In disease situations, death may be caused

by the development of secondary infections exac-

erbated by stress and the formation of open

wounds, osmoregulatory failure, and in the case of

the gills, respiratory impairment (Brandal and

Egidius 1979, Wootten et al. 1982, Johnson et al.

1996, Bjorn and Finstad 1997, Pike and

Wadsworth 1999, Bowers et al. 2000, Finstad et

al. 2000).

Parasitic copepods from other families have

also been reported from cultured fish and in some

instances have been responsible for disease

(Table 1). However, there are few reports of

pathology associated with their attachment and

feeding. The attachment and feeding activities of

Alella macrotrachelus on black sea bream resulted

in hyperplasia of the gill lamellae (Muroga et al.

1981). Hogans (1989) reported serious disease in

Atlantic salmon infected with Ergasilus labracis

that was characterized by severe gill hyperplasia

and high levels of mortality. Infection of the gills of

Borneo mullet (Liza macrolepis) with extremely

high numbers of the ergasilid copepod, Diergasilus

kasaharai, resulted in gill inflammation, necrosis,

high levels of mucous production, and death of the

hosts (Lin and Ho 1998). The formation of vac-

uoles within the gill tissues was reported for

Malabar reef-cod (Epinephelus malabaricus)

infected with Ergasilus lobus (Lin and Ho 1998).

IMPACT OF PARASITIC COPEPODS ON

MARINE SALMONID CULTURE

In marine salmon aquaculture, sea lice

belonging to the genera Caligus and Lepeoph-

theirus are commonly present, but their presence

does not always result in the development of dis-

ease (Table 1, Ho and Nagasawa 2001).

Unfortunately, under some circumstances, epi-

zootics do occur and result in serious disease and

high mortalities if untreated (Brandal and Egidius

1979, Wootten et al. 1982, Pike 1989, Pike and

Wadsworth 1999). Although infection with sea lice

is one of the major problems faced in marine

salmon farming, economic losses due to sea lice

are poorly documented. In addition to affecting the

profitability of salmonid aquaculture, the presence

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Johnson et al. -- Impact of Parasitic Copepods on Aquaculture

231

of sea lice on farmed salmonids and the necessity

for treatments also affects the regulation and pub-

lic perception of salmonid aquaculture in some

regions of the world, especially in areas where

they may affect wild salmonids.

NORTHERN HEMISPHERE

Major regions of marine salmon farming with-

in the northern hemisphere include Japan, the east

and west coasts of Canada, the northeastern US,

Ireland, Scotland, and Norway. The major sea lice

species reported from farmed salmonids in these

regions are Caligus clemensi (Pacific Ocean), C.

elongatus (Atlantic Ocean), and L. salmonis (Table

2, Johnson et al. 1997, Pike and Wadsworth,

1999). Lepeophtheirus salmonis has a circumpo-

lar distribution and is limited in its host range to

salmonids, except in very rare cases (Kabata,

1979). In comparison, C. clemensi and C. elonga-

tus have broad host ranges that include both non-

salmonid teleost and elasmobranch hosts

(Margolis et al. 1975, Kabata 1979). Many of

these non-salmonid hosts are common in the vicin-

ity of seawater farms and serve as a source of par-

asites for infection of salmonids.

Of these species, L. salmonis is the most

important with respect to disease. There is a vast

literature on the biology and control of L. salmonis

that is well summarized in a recent review by Pike

and Wadsworth (1999). With the exception of

Japan and the west coast of Canada, outbreaks of

disease caused by sea lice have been frequently

reported for all of these regions. In most of these

regions, the initial outbreaks of sea lice disease

resulted in high economic losses that were sus-

tained until adequate treatment and management

strategies were instituted. At present, outbreaks of

disease caused by sea lice are rarely reported,

although rates of sea lice infection remain high as

evidenced by the frequent requirement for treat-

ments. The lack of disease is due to the use of

management strategies that rely on medicines and

husbandry practices to maintain sea lice at low lev-

els of abundance. In some countries such as

Ireland, Scotland, and Norway, treatment thresh-

olds for sea lice have been regulated (Eithun 2000,

McMahon 2000). These regulations have been

put into effect as a response to concern that sea

lice emanating from farmed salmonids might be

responsible for sea lice problems seen on wild sea

trout and Atlantic salmon. Treatment thresholds in

Ireland are set at 0.3 to 0.5 egg-bearing females

per fish in the spring and 2 egg-bearing females

per fish at other times of the year (McMahon

2000). The treatment threshold for Norway is set

at 1 to 5 adult females per fish depending on the

season, water temperature, and site location

(Eithun 2000). In Scotland, a voluntary code sets

the treatment threshold at 1 ovigerous female per

10 fish in the spring (Rae 2002). In New

Brunswick, Canada, treatments are often initiated

when there are > 5 preadults per fish and/or 1 egg-

bearing female per fish depending on the water

temperature and season.

With the reduction in the occurrence of severe

sea lice disease, economic losses due to fish mor-

tality and carcass downgrading have been sub-

stantially reduced. However, sea lice still have a

significant economic impact due to reduced growth

performance resulting from the presence of the

sea lice and/or chemical treatments, as well as

from the costs of the treatments themselves

(Sinnott 1999, Rae 2002). As mentioned previous-

ly, there are few accurate estimates of the eco-

nomic costs of sea lice to salmonid aquaculture.

Rae (2002) estimated the cost of sea lice to the

Scottish salmon farming industry at between

$US31 and 46 million per annum based on a har-

vest of 130 000 tons (t). This cost includes an

approximately $US20 million loss due to stress

and loss of growth, and $US6.2 to 7.2 million loss

due to the cost of therapeutics. Another estimate

of the cost of sea lice infections in Scotland ranges

between US$0.18 and 0.45 kg-1 of salmon (Sinnott

1999). Norway

s annual losses due to sea lice

infection have been estimated to be approximately

$US67 million. Mustafa et al. (2001) estimated an

additional cost of US$0.08 to 0.11 kg-1 of fish due

to sea lice infection for sites in New Brunswick,

Canada that regularly treat for sea lice. Without

Table 1. Major groups of parasitic copepods

reported from fish cultured in brackish and marine

waters. Proportions are based on publications

cited in Table 2

Family/Genus

Proportion of all

species reported

Caligidae

61%

Caligus

40%

Lepeophtheirus

14%

Ergasilidae

15%

Other families

24%

Lernaepodidae

Lernanothropidae

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Zoological Studies 43(2): 229-243 (2004)

232

treatment, they estimated that farmers would lose

approximately US$0.35 kg-1 salmon through down-

grading of damaged fish and losses due to mortali-

ty.

In Japan, the salmonid aquaculture industry

farms both coho salmon (Oncorhynchus kisutch)

and to a lesser extent rainbow trout (Oncorhyn-

chus mykiss). Lepeophtheirus salmonis is com-

monly found on both of these species (Nagasawa

and Sakamoto 1993, Urawa et al. 1998, Ho and

Nagasawa 2001, Nagasawa 2003). Infection with

L. salmonis occurs immediately after salmonid

juveniles are introduced into sea net-pens in late

fall. The source of this infection is larvae released

from adult female parasites on migrating wild chum

salmon, Oncorhynchus keta. Sea lice abundance

is reported to increase through the on-growth peri-

od; however, unlike in Scotland, Norway, and

Eastern Canada, L. salmonis is not a serious prob-

lem in Japan, and treatments for sea lice on

salmonids are not carried out. The absence of dis-

ease caused by sea lice has been attributed to the

rearing of coho salmon, a species which is resis-

tant to infection, and to the practice of rearing fish

for only 1 year prior to harvest (Ho and Nagasawa

2001). It is known that salmonids heavily infected

with L. salmonis are disliked at fish markets, and

they thus have lower commercial value (Nagasawa

and Sakamoto 1993).

With respect to other groups of parasitic

copepods, a single outbreak of disease caused by

the ergasilid species, E. labracis, was reported in

Atlantic salmon parr being held in brackish (14 ppt)

waters in New Brunswick, Canada (Table 2,

Hogans 1989, O

Halloran et al. 1992). In that

instance, large numbers of all infectious develop-

mental stages of E. labracis were present on the

gills, resulting in severe gill hyperplasia and high

levels of mortality until treatment was administered

(Hogans 1989).

SOUTHERN HEMISPHERE

In the southern hemisphere, Atlantic salmon,

coho salmon, and rainbow trout are farmed com-

mercially in Chile, New Zealand, and Tasmania.

Sea lice have not been reported to cause disease

in New Zealand or Tasmania. In Chile, marine

salmonid aquaculture began in the 1980s with the

introduction of commercial-scale coho salmon pro-

duction. This was quickly followed with the devel-

opment of marine rearing of rainbow trout and

Atlantic salmon. At present, Chile is the 2nd-

largest producer of farmed salmonids with an esti-

mated production of 230 000 t in 1999 (Anony-

mous in press). As in the northern hemisphere,

sea lice were quickly recognized as economically

important disease causing agents (Reyes 1983,

Reyes and Bravo 1983a b).

Since 1840 when Caligus ornatus was first

described by Milne-Edwards, there have been a

wide variety of caligid copepods reported from wild

marine fishes in Chilean waters. Many of these

species have cosmopolitan distributions (Fagetti

and Stuardo 1961). To date, 2 species of sea lice,

Caligus teres and C. rogercressyi (originally identi-

fied as C. flexispina), have been documented as

economically important parasites of coho and

Atlantic salmon and rainbow trout (Table 2, Reyes

1983, Reyes and Bravo 1983 a b, Carvajal et al.

1998, Boxshall and Bravo 2000, Gonz�lez et al.

2000). Both of these species have also been iden-

tified from a variety of wild marine fishes that are

common within the vicinity of farm sites (Carvajal

et al. 1998).

Under both laboratory and field conditions,

coho salmon are generally less susceptible to

infection with these sea lice species than are either

rainbow trout or Atlantic salmon (Gonz�lez et al.

2000, Bravo 2001). Outbreaks of sea lice disease

in Chile are most common in stocks of Atlantic

salmon and rainbow trout (Gonz�lez et al. 2000).

Due to establishment of a treatment threshold of >

10 sea lice per fish and the availability of effective

treatments, there are now few instances where

infection with sea lice results in mortality.

However, infection with sea lice has a significant

economic impact in Chile. The costs of treatments

and reduced growth performance, as well as costs

associated with delousing of the carcasses during

processing are estimated to be approximately

US$0.30 kg-1 (Carvajal et al. 1998). Based on a

field study of a farm that required 3 treatments per

year of emamectin benzoate (SLICE�, Schering

Plough) to control sea lice on Atlantic salmon and

rainbow trout, the estimated cost of treatments

alone was approximately US$0.022 kg-1 for the

production period (Sandra Bravo, pers. comm.).

In Chile, it is recognized that infection with

sea lice can predispose fish to the development of

other diseases such as infectious pancreatic

necrosis, bacterial kidney disease, and salmonid

rickettsial septicemia. These diseases are difficult

to treat and can result in high levels of mortality

(Sandra Bravo, pers. comm.).

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Johnson et al. -- Impact of Parasitic Copepods on Aquaculture

233

IMPACT OF PARASITIC COPEPODS ON

MARINE NON-SALMONID CULTURE

The presence of parasitic copepods has been

reported on a large number of species of non-

salmonid fish cultured in brackish and marine

waters (Table 2). However there are few well-doc-

umented cases of disease and no estimates of the

economic costs of these infections.

Ergasilid copepods have been reported from

a variety of non-salmonid finfish reared in brackish

and marine waters (Table 2). Outbreaks of dis-

ease caused by ergasilids are a major source of

copepod-induced mortality in brackish water finfish

culture. Heavy infections of Ergasilus lizae have

been reported to cause mortalities in grey mullet

(Mugil cephalus) cultured in brackish water ponds

in Israel (reviewed in Paperna 1975). Lin and Ho

(1998) reported 4 outbreaks of disease caused by

ergasilid copepods on 4 different host species in

Taiwan. Ergasilid copepods have also been

reported to cause mortalities in the southern floun-

der (Paralichthys lethostigma) in the US and red

sea bream (Pagrus major) in Japan (Yamashita

1980, Benetti et al. 2001). In all of these

instances, heavy infections on the gills resulted in

gill damage, morbidity, and in most instances, sub-

stantial mortalities.

Caligid copepods have also been reported

from a large number of cultured non-salmonid fin-

fish (Tables 1, 2, Ho 2000). As in salmonid culture,

sea lice are responsible for most disease out-

breaks that occur on non-salmonids when they are

cultured in full salinity seawater. Infection of hatch-

ery reared postlarval stages of Atlantic cod (Gadus

morhua) with C. elongatus, Holobomolochus con-

fusus, and Clavella adunca has been associated

with the feeding of natural zooplankton assem-

blages (Karlsbakk et al. 2001). Caligus spp. are

also known to be important parasites of wild juve-

nile Atlantic cod and haddock (Melanogrammus

aeglefinus), and C. elongatus has been found on

wild caught haddock and Atlantic cod broodstock

(Neilson et al. 1987, Armstrong et al. 1999 cited in

Bergh et al. 2001, Stewart Johnson, unpubl. data

for Canada). Lepeophtheirus hippoglossi and C.

elongatus have been reported from wild Atlantic

halibut and have been collected from captive

broodstock (Kabata 1988, Stewart Johnson,

unpubl. data for Canada). Laboratory infections of

Atlantic halibut with L. hippoglossi have resulted in

the development of large hemorrhagic lesions that

demonstrate the potential of this species to cause

disease (Armstrong et al. 1999 cited in Bergh et al.

2001). Heavy infections of pen reared Atlantic hal-

ibut with C. elongatus have been reported in

Norway (Bergh et al. 2001). Infections of greater

than 100 copepods per 500 g fish resulted in the

development of severe head lesions. These infec-

tions were successfully treated with organophos-

phates.

To date, there have been no published reports

of sea lice causing disease in cultured Atlantic cod

or haddock in Scotland, Norway, or Canada.

However there have been verbal reports from cod

farmers in Norway of sea lice problems (Frank

Nilsen, pers. comm.). In one of these cases,

examination of infected fish revealed infection by

C. elongatus although there were also a few C.

curtus present (Frank Nilsen, pers. comm.). The

broad host range of C. elongatus and the presence

of many of wild hosts in the vicinity of many marine

farm sites suggest that disease problems caused

by this species may become more common as

production levels of Atlantic cod and haddock

increase.

Pseudocaligus apodus and Caligus pageti

have been reported to cause disease in mullet cul-

ture in the Eastern Mediterranean (Paperna 1975).

Papoutsoglou et al. (1996) reported infrequent

infection of European sea bass (Dicentrarchus

labrax) with low numbers of Caligus minimus at

sites in Greece, but no disease outbreaks. Caligus

minimus has also been reported from European

sea bass raised on the French Atlantic coast with-

out mention of disease (Paperna and Baudin

Laurencin 1979). Pavoletti et al. (1999) reported

on a disease outbreak in European sea bass in

Italy caused by C. minimus. In that instance, fish

from 30 g to 2 kg in size were infected with an

average of 40 copepods per fish. Infected fish

were anorexic and lethargic, and there was

approximately 9% mortality of the stock.

In Japan, there are 5 major species of non-

salmonid marine finfish cultured: Japanese amber-

jack (yellowtail) (Seriola quinqueradiata), greater

amberjack (Seriola dumerili), red sea bream,

Japanese flounder (Paralichthys olivaceus), and

tiger puffer (Takifugu rubripes). Other species,

such as the black sea bream (Acanthopagurs

schlegeli), striped jack (Pseudocaranx dentex),

and spotted halibut (Verasper variegatus) are also

cultured but at relatively low levels of production.

Numerous species of parasitic copepods have

been reported from these species in culture includ-

ing: Caligus spinosus, C. lalandei, and

Eobranchiella elegans seriolae from Japanese

amberjack; C. fugu, Psuedocaligus fugu, and

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Zoological Studies 43(2): 229-243 (2004)

234

Neobrachiella fugu from the tiger puffer; A. macro-

trachelus from the black sea bream; C. lalandei

from yellowtail amberjack; C. longipedis from

striped jack; Lepeophtheirus paralichthydis from

Japanese flounder; L. longiventris from spotted

halibut; and unidentified caligid copepods from red

sea bream (Muroga et al. 1981, Ogawa 1992,

Ogawa and Inoue 1997, Ogawa and Yokoyama

1998, Ho 2000, Ho et al. 2001) (Table 2). Caligus

spinosus infections on farmed Japanese amber-

jack occur mainly on the gill arches and rakers,

and high levels of infection have resulted in mortali-

ties (Fujita et al. 1968). Infected fish are emaciat-

ed, dark-colored, and inactive, often swimming

near the water surface. Recently, Ho et al. (2001)

reported C. lalandei on the body surface of farmed

yellowtail amberjack from western Japan. The

authors reported that the wild yellowtail juveniles

used as seeds for culture are sometimes infected

with C. spinosus or C. lalandei. Caligus lalandei is

a cosmopolitan species found also in South Africa,

Mexico, Chile, New Zealand, and Korea (Ho et al.

2001). Eobrachiella elegans seriolae is found near

the base of pectoral fins and on the walls of the

oral cavity of cultured Japanese amberjack. To

date, there is no report of this species causing dis-

ease in Japan (Ono 1984). Caligus lalandei

(reported as Caligus sp. in Ogawa and Yokoyama

1998) is also known to infect farmed yellowtail

amberjack (Ho et al. 2001). Ho et al. (2001) noted

that although this species has not yet caused seri-

ous problems in Japanese aquaculture, its larger

size when compared to C. spinosus gives it the

potential to be a serious disease causing agent.

As a parasite of black sea bream, the biology

and impacts of A. macrotrachelus have been well

studied (Kawatow et al. 1980, Muroga et al. 1981).

This copepod attaches to and feeds on gill tissue

resulting in hyperplasia of the gill lamellae (Muroga

et al. 1981). Copepod numbers are generally seen

to increase in fall and late spring or early summer

and decline in winter and summer due a lack of

recruitment and parasite death (Muroga et al.

1981).

Farmed striped jack can be infected with C.

longipedis, with the body of infected fish showing

bruising (Kubota and Takakuwa 1963 [as C. ampli-

furcus], Ogawa 1992). Ho (2000) compiled infor-

mation on parasitic copepod infections by the 2

caligid genera Caligus and Lepeophtheirus on

cage-cultured fishes in marine and brackish waters

of Asia including Japan. Although information is

very limited, Ho (2000) reported that L. paralichthy-

dis and L. longiventris caused mortality of pen cul-

tured Japanese flounder and spotted halibut,

respectively.

An unidentified species of Caligidae or

Pennellidae (originally reported as Ergasilus sp.)

was reported from the body surface of larval red

sea bream in Japan (Yamashita 1980). On tiger

puffer, P. fugu occurs on the body surfaces, and C.

fugu and N. fugu on the walls of the buccal cavity.

Of these species, N. fugu is the most commonly

reported species, being present throughout the

year with a peak population size during the warm

water months (Ogawa and Inoue 1997). Diseases

caused by these copepods have not been reported

from Japanese waters.

In China, South Korea, and Taiwan, disease

outbreaks caused by Caligus species have been

reported from cultured milk fish (Chanos chanos),

Mozambique tilapia (Oreochromis mossambicus),

banded grouper (yellow grouper) (Epinephelus

awoara), rabbit fish, black sea bream, common

spade fish (Scatophagus argus), Malabar reef-cod,

large scale mullet (Liza macrolepis), grey mullet

(Mugil cephalus), blue tilapia (Oreochromis

aureus), three-striped tigerfish (Terapon jarbua),

snubnose pompano (Trachinotus blochii), and sea

bass (barramundi) (Lates calcarifer) (Table 2,

Lavinia 1977, Jones 1980, Lin and Ho 1993 1998,

Lin et al. 1994 1996 1997, Choi et al. 1995, Wu

and Pan 1997, Ho 2000). The species responsible

for these disease outbreaks include Caligus acan-

thopagri, C. epidemicus, C. orientalis, C. patulus,

and C. rotundigenitalis (cf. Ho 2000). In some of

these cases, high levels of mortality were reported,

but the economic impacts of these outbreaks were

not quantified.

The economic impacts of parasitic copepods

on non-salmonid marine aquaculture are unknown.

Large scale mortality of adult yellowtail farmed in

the Goto Islands, southern Japan, was reported in

the spring of 1967 as being due to a heavy infec-

tion with C. spinosus (cf. Fujita et al. 1968). Other

large scale mortalities have not been reported.

The economic impacts of parasitic copepods on

fish growth, susceptibility to other diseases, cost of

production, and loss of product value have not

been quantified.

FACTORS THAT INFLUENCE PARASITIC

COPEPOD ABUNDANCE

A variety of environmental and biological fac-

tors and husbandry and management practices

that may influence the abundance and impact of

Page 7

Johnson et al. -- Impact of Parasitic Copepods on Aquaculture

235

able 2.

Parasitic copepods reported from finfish cultured in brackish a

nd marine waters

Family Caligidae Caligus acanthopagri

black sea bream

Taiwan

Lin et al. 1994

(Acanthopagrus schlegeli

)

Lin 1996 cited in Ho

common spade fish

2000

(Scataphagus argus

)

Malabar rock cod (Epinephelus malabaricus

)

Mozambique tilapia (Oreochromis mossambicus

)

Caligus antennatus

Sobaity sea bream

Kuwait

reen 1986

(Sparidentex hasta

)

(listed as

Acanthopagrus

cuvieri

)

Caligus

olive flounder

South Korea

Choi et al. 1995

brevicaudatus

(Paralichthys olivaceus

)

Caligus clemensi

Atlantic salmon (

Salmo

Pacific coast,

Stewart Johnson

salar

)

Canada

unpubl. data

coho salmon (Oncorhynchus kisutch

)

rainbow trout (Oncorhynchus mykiss

)

Caligus curtus

Atlantic cod

Atlantic coast,

Hogans and T

rudeau

(Gadus morhua

)

1989

Atlantic salmon

Canada

Frank Nilsen, pers.

Norway

comm.

Caligus elongatus

Arctic charr

Atlantic coast,

Bergh et al. 2001

(Salvelinus alpinus

)

Canada

Hogans and T

rudeau

Atlantic cod

1989a b

Atlantic halibut

Northeast

Hogans 1994

(Hippoglossus

Atlantic coast,

Karlsbakk et al. 2001

hippoglossus

)

Mustafa and

Atlantic salmon

MacKinnon 1993

rainbow trout

Ireland

Shaw and Opitz 1993

striped bass

Scotland

ully 1989

(Morone saxatilis

)

Norway

ootten et al. 1982

Caligus epidemicus

black porgy

Australia

Lin and Ho 1992

(Acanthopagrus schlegeli

)

Taiwan

1993

blue tilapia

Philippines

Lin 1996 cited in Ho

(Oreochromis aurea

)

2000

common spade fish

Regidor and Aurthur

giant perch

1986

(Lates calcarifer

)

Roubal 1994 1995

grey mullet (Mugil cephalus

)

large scale mullet (Liza macrolepis

)

Malabar rock cod milk fish (Chanos chanos

)

Mozambique tilapia snubnose pompano (T

rachinotus blochii

)

three-striped tiger fish (Terapon jarbua

)

yellowfin bream (Acanthopagrus australis

)

Caligus fugu

tiger puffer

Japan

Ogawa and Inouye

(Takifugu rubripes

)

1997 Ogawa and Y

okoyama1998

Caligus lalandei

yellowtail amberjack

Japan

Ho et al. 2001

(Seriola lalandi

)

Caligus latigenitalis

black sea bream

Japan

Izawa and Choi 2000

Caligus longipedis

striped jack

Japan

Kubota and

(Pseudocaranx dentex

)

Takakuwa 1963 (as Caligus amplifurcus

)

Ogawa 1992

Caligus minimus

European sea bass

Atlantic coast,

Paperna and Boudin

(Dicentrarchus labrax

)

France Laurencin 1979 Italy

Papoutsoglou et al. 1996

Greece

Pavoletti et al. 1999

Caligus

black sea bream

Taiwan

Lin et al.1994 1997

multispinosus

Caligus nanhaiensis

banded grouper

China

and Pan 1997

(Epinephelus awoara

)

u et al. 1997

Caligus orientalis

black porgy

Japan

Hwa 1965

giant perch

China

Lin 1996 cited in Ho

grey mullet

Taiwan

2000

large scale mullet

Urawa and Kato

Species

Hosts

Geographical

References

location

Species

Hosts

Geographical

References

location

Page 8

Zoological Studies 43(2): 229-243 (2004)

236

able 2.

(Cont.)

Malabar rock cod

1991

milk fish Mozambique tilapia snubnose pompano rainbow trout

Caligus oviceps

rabbit fish (

Siganus

Taiwan

Lin et al. 1996

fuscescens

)

Caligus pageti

grey mullet

France

Paperna 1975

thinlip mullet

Israel

Raibaut et al. 1980

(Liza ramada

) Egypt

(listed as

Mugil capito

)

white sea bream (Diplodus sargus sargus

)

Caligus patulus

milk fish

Philippines

Lavinia 1977

Indonesia

Jones 1980

Caligus pelamydis

Japanese sea perch

South Korea

Choi et al. 1995

(Lateolabrax japonicus

)

Caligus punctatus

black porgy

Taiwan

Lin 1996 cited in Ho

black sea bream

2000

blue tilapia giant perch grey mullet Japanese sea bass (Lateolabrax japonicus

)

large scale mullet Malabar rock cod milk fish Mozambique tilapia snubnose pompano three-striped tiger fish

Caligus

Atlantic salmon

Chile

Carvajal et al. 1998

rogercresseyi

coho salmon

Boxshall and Bravo

(identified by Carvajalsea trout

2000

et al. as

Caligus

(Oncorhynchus mykiss

)

flexispina

)

Caligus

black porgy

Taiwan

Lin et al.1994

rotundigenitalis

black sea bream

Lin 1996 cited in Ho

common spade fish

et al. 2000

Malabar rock cod

Caligus spinosus

Japanese amberjack

Japan

Fujita et al. 1968

(Seriola quinqueradiata

)

Izawa 1969 Ogawa and Y

okoyama 1998

Caligus

sp.

dhufish

Australia

Pironet and Jones

(Glaucosoma hebraicum

)

2000

Caligus

sp.

black sea bass

Malaysia

Leong and W

ong

(Lates calcarifer

)

1986

Caligus

sp.

brown-marbled grouper

Indonesia

Leong and W

ong

(Epinephelus

1988

fuscoguttatus

)

Malaysia

Koesharyani et al.

humpback grouper

1999

(Cromileptes altivelis

)

leopard coral grouper (Plectropomus leopardus

)

Malibar grouper (Epinephelus malabaricus

)

orange-spotted grouper (Epinephelus coioides

)

Caligus

sp.

haddock (

Melanogrammus

Atlantic Coast,

Stewart Johnson,

aeglefinus

)

Canada

unpubl. data

Caligus

sp.

greater amberjack

Japan

Ogawa and

(Seriola dumerili

)

okoyama 1998

Caligus teres

sea trout

Chile

Reyes and Bravo

coho salmon

1983 Carvajal et al. 1998 Boxshall and Bravo 2000

Lepeophtheirus

rabbit fish

Taiwan

Lin et al. 1996

atypicus

(Siganus fuscescens

)

Lepeophtheirus

rainbow trout

Pacific coast of

Johnson and Albright

cuneifer

Atlantic salmon

Canada

1991c

Lepeophtheirus

Atlantic halibut

Atlantic coast,

Stewart Johnson,

hippoglossi

(Hippoglossus

Canada

unpubl. data

hippoglossus

)

Lepeophtheirus

spotted halibut

Japan

Ho 2000

longiventris

erasper variegatus

)

Lepeophtheirus

olive flounder

Japan

Ho 2000

paralichthydis

(Paralichthys olivaceus

)

Lepeophtheirus

Atlantic salmon

Pacific and

Brandal and Egidius

salmonis

chinook salmon

Atlantic coasts

1979

(Oncorhynchus

Canada

ootten et al. 1982

Species

Hosts

Geographical

References

location

Species

Hosts

Geographical

References

location

Page 9

Johnson et al. -- Impact of Parasitic Copepods on Aquaculture

237

able 2.

(Cont.)

tshawytscha

)

Northwest and

Hogans and T

rudeau

coho salmon

northeast

1989a

rainbow trout

coasts of the

ully 1989

Nagasawa and

Faroes

Sakamoto 1993

Japan

Shaw and Opitz 1993

Norway

Urawa et al. 1998

Scotland

Pike and W

adsworth

Ireland

1999 (and references within) Ho et al. 2001

Lepeophtheirus

sp.

brown-marbled grouper

Indonesia

Koesharyani et al

humpback grouper

1999

leopard coral grouper Malibar grouper Orange-spotted grouper

Lepeophtheirus

sp.

sea trout

Boxshall and Bravo 2000

Parapetalus

cobia

Taiwan

Ho and Lin 2001

occidentalis

(Rachycentron canadum

)

Pseudocaligus

grey mullet

Israel

Paperna 1975

apodus

Pseudocaligus fugu

tiger puffer

Japan

Ogawa and Inouye

(Takifugu rubripes

)

1997 Ogawa and Y

okoyama 1998

Unidentified

red sea bream

Japan

Ogawa and

Caligoida

okoyama 1998

Unidentified Caligid

red sea bream

Japan

amashita 1980

or Pennellid

Family Ergasilidae Diergasilus kasaharai

Borneo mullet

Taiwan

Lin and Ho 1998

(Liza macrolepis

)

milkfish tilapia (Oreochromis

sp.)

Ergasilus

yellowfin bream

Australia

Roubal 1995

australiensis

(Acanthopagrus australis

)

Ergasilus

greasy grouper

Malaysia

Leong and W

ong

borneoensis

(Epinephelus malabaricus

)

1988

Ergasilus

Asian cichlid

Sri Lanka

Wijeyaratne and

ceylonensis

(Etroplus suratensis

)

Gunawardene 1988

Ergasilus labracis

Atlantic salmon

Atlantic Coast,

Hogans 1989

Canada

’

Halloran et al.

1992

Ergasilus lizae

grey mullet

Eastern

Paperna 1975

carp (

Cyprinus

sp.)

Mediterranean

Ergasilus lobus

Malabar reef-cod

Taiwan

Lin and Ho 1998

Ergasilus

sp.

southern flounder

United States

Benetti et al. 2001

(Paralichthys lethostigma

)

Psuedoergasilus

ayu

Japan

Nakajima and Egusa

zacconis

(Plecoglossus altivelis

1973

altivelis

)

Other Families Alella macrotrachelus

black sea bream

Japan

Muroga et al. 1981

yellowfin bream

Australia

Ueki and Sugiyama 1978 Roubal 1995

Alella

sp.

Korean rockfish

South Korea

Choi et al. 1997

(Sebastes schlegeli

)

Bomolochus stocki

yellowfin bream

Australia

Roubal 1995

Clavella adunca

Atlantic cod

Norway

Karlsbakk et al. 2001

Lernanthropus atrox

yellowfin bream

Australia

Roubal 1995

Lernanthropus

yellowfin bream

Australia

Roubal 1995

chrysophrys

Lernanthropus

Sobiaty sea bream

Kuwait

Tareen 1986

lappaceus

(listed as

Acanthopagras

cuvieri

)

Colobomatus

European sea bass

Atlantic coast,

Paperna and Baudin

labrachis

France

Laurencin 1979

Eobrachiella elegans

yellowtail amberjack

Japan

Ogawa and

seiolae

okoyama 1998

Hemobaphes

Atlantic salmon

Pacific coast,

Kent et al. 1997

disphaerocephalus

Canada

Holobomolochus

Atlantic cod

Norway

Karlsbakk et al. 2001

confusus

Neobrachiella fugu

tiger puffer

Japan

Ogawa and Inouye 1997 Ogawa and Y

okoyama 1998

Species

Hosts

Geographical

References

location

Species

Hosts

Geographical

References

location

Page 10

Zoological Studies 43(2): 229-243 (2004)

238

sea lice on farmed salmonids have been identified

(reviewed in Costello 1993, Pike and Wadsworth

1999, Rae 2002). These factors and husbandry

practices have been used to develop management

strategies for sea lice on farmed salmonids.

Although empirically it would seem that these fac-

tors and husbandry practices should have an

impact on sea lice abundance, this has not always

been demonstrated experimentally or by analysis

of sea lice abundance from the field. Revie et al.

(2002) used sea lice counts from 35 Scottish farms

collected from 1996 to 2000 to investigate factors

affecting sea lice abundance. Analysis of the data

revealed large differences between years in sea

lice infestation parameters. Stock type, geographi-

cal region, level of coastal exposure, and water

temperature did not appear to affect mean levels

of abundance. However, treatments did have a

pronounced effect on sea lice infection parame-

ters. It is likely for any given farm site that a differ-

ent suite of environmental and biological factors

and husbandry practices will affect sea lice abun-

dance, and that generalizations across sites are at

present impossible to make. Regardless, knowl-

edge of these factors and husbandry practices is

important, as they are likely to also influence the

abundance of other parasitic copepod species on

non-salmonid finfish. A very brief overview of

these factors and husbandry practices follows.

Environmental and Engineering Factors

Proper site selection and design of rearing

structures can reduce the number of infectious

stages that are transported to and/or retained with-

in the rearing environment, as well as ensuring

that fish stocks remain healthy and thereby more

resistant to infection. Factors such as water depth,

tidal range, patterns of water circulation, flow rate,

temperature, and salinity have been suggested as

important factors with respect to sea lice infection

of salmonids (reviewed in Pike and Wadsworth

1999). As mentioned previously, Revie et al.

(2002) were unable to demonstrate a relationship

between L. salmonis abundance and stock type,

geographical region, level of coastal exposure, or

water temperature. However in Chile, salmonid

culture sites that are located in closed bays and

shallow waters are generally reported to have

higher levels of Caligus spp. infection than those

seen at sites in more open waters (Sandra Bravo,

pers. comm.).

In Chile, sea lice are absent or present in only

very low numbers on salmonids reared in brackish

and estuarine waters. Under these conditions, sea

lice are reported to have little effect on fish health

and condition (Sandra Bravo, pers. comm.).

Tucker et al. (2000) reported that L. salmonis had

a higher growth rate and rate of settlement at a

salinity of 34 ppt when compared to 24 ppt.

Temperature is the most important environ-

mental factor controlling the development times of

parasitic copepods and the rate at which their pop-

ulation size increases in the absence of treat-

ments. With respect to L. salmonis, a great deal of

effort has gone into determining the effects of tem-

perature on growth, egg production, and larval set-

tlement. Growth rates, egg production, survival,

and recruitment are reported to be higher at higher

water temperatures (Wootten et al. 1982, Hogans

and Trudeau 1989a b, Tully 1989, Johnson and

Albright 1991b, Tully and Whelan 1993, Boxaspen

1997, Wadsworth 1998, Pike and Wadsworth 1999

and additional references therein, Tucker et al.

2000). These data have been used in the devel-

opment of management and treatment strategies

for L. salmonis. For other species of parasitic

copepods, the development of effective manage-

ment and treatment strategies will require as a

minimum, a good knowledge of development times

over the range of temperatures experienced in the

culture system. This is especially true for treat-

ments that are not effective against all of the life

history stages.

Husbandry Practices

Modification of husbandry practices can be a

very effective method to reduce the magnitude of

infection by parasitic copepods (Costello 1993,

Pike and Wadsworth 1999). Using husbandry

practices to control parasitic copepod abundance

requires a good knowledge of parasite biology

(e.g., growth rates, duration of survival of infec-

tious stages off-host, etc.) and host range. As with

other infectious diseases, any management activi-

ties (e.g., stocking density, water quality manage-

ment, etc.) that reduce stress and maintain optimal

fish health are likely to reduce the impact of para-

sitic copepods. It is well recognized that poorly

smolted or otherwise unhealthy salmonids are

more susceptible to infection by L. salmonis (cf.

Grimnes and Jakobsen 1996, Finstad et al. 2000).

In pond culture, overcrowding and poor water qual-

ity have been cited as factors responsible for the

development of parasitic copepod diseases

(Singhal et al. 1986, Tareen 1986).

Year-class separation is a very effective tech-

Page 11

Johnson et al. -- Impact of Parasitic Copepods on Aquaculture

239

nique that can substantially reduce the infection

rate of newly introduced juveniles. This technique

has been successfully used in the salmon culture

industry in Scotland, Norway, and Ireland (Grant

and Treasurer 1993, Boxaspen 1997, Jackson et

al. 1997, Rae 2002). Fallowing of sites prior to

restocking can reduce subsequent infection rates,

providing that the fallow period is long enough to

ensure that all infectious stages have died due to a

lack of hosts (Bron et al. 1993, Grant and

Treasurer 1993, Rae 2002). The effectiveness of

these husbandry techniques depends on the

absence of wild hosts and/or other infected sites

that are within transport distance for the infectious

stages.

In situations where year-class separation

and/or fallowing is not possible, treatment of fish

on site prior to restocking will often reduce the rate

of infection on newly introduced fish. When wild

caught juveniles or broodstock are used in culture,

administration of a treatment for parasitic cope-

pods at the time of introduction to the rearing sys-

tem will likely reduce the rate of parasite popula-

tion increase. Ho et al. (2001) reported that wild

yellowtail juveniles used as seeds for culture are

sometimes infected with C. spinosus or C.

lalandei. In Atlantic Canada, parasitic copepods

present on wild Atlantic halibut and haddock

broodstock at capture have caused problems in

broodstock holding facilities (Stewart Johnson,

unpubl. observ.). These problems were resolved

by treatment and increasing the flushing rates of

broodstock tanks.

Frequent cleaning of nets or other techniques

that improve water flow through the rearing habitat

may result in lower rates of infection, due to

improved fish health and removal of infectious

stages off-site. Net fouling has been demonstrat-

ed to result in the retention of high numbers of L.

salmonis naupliar and copepodid stages within net

pens (Costelloe et al. 1996). Increased flushing

rates of a land based salmonid growout facility

reduced the level of infection of rainbow trout by

Lepeophtheirus cuneifer in British Columbia

(Stewart Johnson, unpubl. observ.).

Biological Factors

It is well recognized that both wild and cul-

tured fish have the potential to serve as reservoirs

of infection for sea lice and other parasitic cope-

pods (Paperna 1975, Carvajal et al. 1998, Ho and

Nagasawa 2001). When selecting sites for aqua-

culture, the presence of wild hosts within the water

source or within the local environment, as well as

the distance and direction (with respect to water

movements) of other aquaculture sites should be

noted. Consideration of these factors will assist in

the selection of sites with reduced rates of infec-

tion and/or sites that will have lower impacts with

respect to parasitic copepod transfer from cultured

to wild hosts. Parasitic copepods with relatively

narrow host ranges, such as L. salmonis, can be

easier to control, especially where there are few

wild hosts present. Species with broad host

ranges and/or abundant wild hosts in the vicinity of

aquaculture sites are generally considerably more

difficult to control. This has been well demonstrat-

ed in Chile where Caligus species that transfer

from wild non salmonid hosts cause serious and

chronic disease problems in salmonid aquaculture

(Reyes and Bravo 1983a b, Carvajal et al. 1998,

Gonz�lez et al. 2000).

SEA LICE AS VECTORS OF OTHER DISEASES

Due to their feeding activities on host

mucous, tissue, and blood, it has been suggested

that parasitic copepods may serve as vectors of

viral and bacterial diseases of fish (Nylund et al.

1991 1993). The sea louse, L. salmonis has been

demonstrated in the laboratory to be able to func-

tion as a vector for the viral agent responsible for

infectious salmon anemia (ISA), especially during

epidemic and endemic phases (Nylund et al. 1993

1994). Although not implicated in the transfer of

the bacterium, Aeromonas salmonicida, the

causative agent of furunculosis, it has been isolat-

ed from the surface of L. salmonis (Nesse 1992

cited in Nylund et al. 1993). More recently the

virus responsible for infectious pancreatic necrosis

has also been isolated from L. salmonis (Jim

Treasurer, unpubl. data). Although there is no evi-

dence from field studies that L. salmonis acts as

vectors for diseases, as a precautionary measure,

sea lice control has been adopted as an integral

part of management strategies for the control of

ISA in Atlantic Canada and Scotland.

CONCLUSIONS

In summary, parasitic copepods, especially

sea lice, are economically important parasites in

marine aquaculture. In salmonid culture, disease

outbreaks and subsequent mortalities caused by

sea lice are now rare due to the development of a

Page 12

Zoological Studies 43(2): 229-243 (2004)

240

variety of effective treatments. However, large

economic losses still occur as the result of reduced

feed conversion and growth, indirect mortality, loss

of product value, and treatment costs. Although it

is well understood that parasitic copepods have a

major impact on non salmonid aquaculture, there

are relatively few published reports of disease

and/or disease treatments. There are no reports

of economic costs associated with these infec-

tions. Husbandry practices as well as a variety of

engineering, environmental, and biological factors

can have an impact on the level of infection by par-

asitic copepods. However, the relative importance

of these factors in controlling copepod abundance

varies between sites. There is no evidence from

field studies to support the suggestion that para-

sitic copepods such as sea lice can act as vectors

for fish diseases.

Acknowledgments: The authors would like to

thank Drs. Shigehiko Urawa, Frank Nilsen, Karin

Boxaspen, and Ju-shey Ho for their generous

assistance and for information used in the produc-

tion of this review.

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