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Emerging viral diseases of fish and shrimpPeter J. Walker, James
R. Winton
To cite this version:Peter J. Walker, James R. Winton. Emerging
viral diseases of fish and shrimp. Veterinary Research,BioMed
Central, 2010, 41 (6), �10.1051/vetres/2010022�. �hal-00903183�
https://hal.archives-ouvertes.fr/hal-00903183https://hal.archives-ouvertes.fr
-
Review article
Emerging viral diseases of fish and shrimp
Peter J. WALKER1*, James R. WINTON2
1 CSIRO Livestock Industries, Australian Animal Health
Laboratory (AAHL), 5 Portarlington Road,Geelong, Victoria,
Australia
2 USGS Western Fisheries Research Center, 6505 NE 65th Street,
Seattle, Washington, USA
(Received 7 December 2009; accepted 19 April 2010)
Abstract – The rise of aquaculture has been one of the most
profound changes in global food production ofthe past 100 years.
Driven by population growth, rising demand for seafood and a
levelling of productionfrom capture fisheries, the practice of
farming aquatic animals has expanded rapidly to become a
majorglobal industry. Aquaculture is now integral to the economies
of many countries. It has providedemployment and been a major
driver of socio-economic development in poor rural and coastal
communities,particularly in Asia, and has relieved pressure on the
sustainability of the natural harvest from our rivers,lakes and
oceans. However, the rapid growth of aquaculture has also been the
source of anthropogenicchange on a massive scale. Aquatic animals
have been displaced from their natural environment, cultured inhigh
density, exposed to environmental stress, provided artificial or
unnatural feeds, and a prolific globaltrade has developed in both
live aquatic animals and their products. At the same time,
over-exploitation offisheries and anthropogenic stress on aquatic
ecosystems has placed pressure on wild fish populations.
Notsurprisingly, the consequence has been the emergence and spread
of an increasing array of new diseases.This review examines the
rise and characteristics of aquaculture, the major viral pathogens
of fish andshrimp and their impacts, and the particular
characteristics of disease emergence in an aquatic, rather
thanterrestrial, context. It also considers the potential for
future disease emergence in aquatic animals asaquaculture continues
to expand and faces the challenges presented by climate change.
disease emergence / shrimp / fish / virus
Table of contents
1.
Introduction...........................................................................................................................................
21.1. The rapid growth of
aquaculture.................................................................................................
21.2. Diversity of farmed aquatic species
............................................................................................
21.3. Characteristics of fish and shrimp production systems
..............................................................
21.4. The decline of capture fisheries
..................................................................................................
3
2. History of disease emergence in fish and shrimp
................................................................................
32.1. Problems associated with emerging diseases
..............................................................................
32.2. Emerging viral diseases of fish
...................................................................................................
42.3. Emerging viral diseases of shrimp
..............................................................................................
8
3. Impacts of emerging diseases of fish and
shrimp..............................................................................
133.1. Economic and social impacts
....................................................................................................
133.2. Environmental impacts
..............................................................................................................
13
* Corresponding author: [email protected]
Vet. Res. (2010) 41:51DOI: 10.1051/vetres/2010022
� INRA, EDP Sciences, 2010
www.vetres.org
This is an Open Access article distributed under the terms of
the Creative Commons Attribution-Noncommercial
License(http://creativecommons.org/licenses/by-nc/3.0/), which
permits unrestricted use, distribution, and reproduction in
anynoncommercial medium, provided the original work is properly
cited.
Article published by EDP Sciences
http://dx.doi.org/10.1051/vetres/2010022http://www.vetres.orghttp://www.edpsciences.org/
-
4. Factors contributing to disease emergence in aquatic
animals..........................................................
144.1. Activities related to the global expansion of aquaculture
........................................................ 154.2.
Improved
surveillance................................................................................................................
164.3. Natural movement of
carriers....................................................................................................
164.4. Other anthropogenic factors
......................................................................................................
16
5. Future disease emergence risks
..........................................................................................................
17
1. INTRODUCTION
1.1. The rapid growth of aquaculture
The farming of fish and other aquatic ani-mals is an ancient
practice that is believed todate back at least 4 000 years to
pre-feudalChina. There are also references to fish pondsin The Old
Testament and in Egyptian hiero-glyphics of the Middle Kingdom
(2050–1652BC). Fish farms were common in Europe inRoman times and a
recent study of land formsin the Bolivian Amazon has revealed a
complexarray of fish weirs that pre-date the Hispanic era[30, 49].
However, despite its ancient origins,aquaculture remained largely a
low-level, sub-sistence farming activity until the mid-20thcentury
when experimental husbandry practicesfor salmon, trout and an array
of tropical fishand shrimp species were developed andadopted.
Aquaculture is now a major globalindustry with total annual
production exceeding50 million tonnes and estimated value of
almostUS$ 80 billion [32]. With an average annualgrowth of 6.9%
from 1970–2007, it has beenthe fastest growing animal
food-producing sec-tor and will soon overtake capture fisheries
asthe major source of seafood [31].
1.2. Diversity of farmed aquatic species
In contrast to other animal production sec-tors, aquaculture is
highly dynamic and charac-terised by enormous diversity in both the
rangeof farmed species and in the nature of produc-tion systems.
Over 350 different species ofaquatic animals are farmed, including
34 finfish(piscean), 8 crustacean and 12 molluscan spe-cies each
for which annual production exceeds100 000 tonnes [32]. Aquatic
animals are
farmed in freshwater, brackishwater and marineenvironments, and
in production systems thatinclude caged enclosures, artificial
lakes,earthen ponds, racks, rafts, tanks and raceways.Farming can
be a small-scale traditional activitywith little human
intervention, through tosophisticated industrial operations in
which ani-mals are bred and managed for optimal perfor-mance and
productivity. The diversity ofaquaculture species and farming
systems alsoextends geographically from tropical to sub-arctic
climes and from inland lakes and riversto estuaries and open
offshore waters.
Aquaculture production is heavily domi-nated by China and other
developing countriesin the Asia-Pacific region which accounts
for89% by volume of global production and77% by value [31]. The
major farmed speciesare carp, oysters and shrimp of which 98%,95%
and 88% of production, respectively, orig-inates in Asia. By
contrast, Atlantic salmon pro-duction is dominated by Norway,
Chile, theUnited Kingdom and Canada which togetheraccount for 88%
by volume and 94% by value[32]. Capture fisheries and aquaculture,
directlyor indirectly, play an essential role in the liveli-hoods
of millions of people, particularly indeveloping countries. In
2006, an estimated47.5 million people were primarily or
occasion-ally engaged in primary production of aquaticanimals
[31].
1.3. Characteristics of fish and shrimpproduction systems
Although a significant component of thesmall-scale aquaculture
sector continues to relyon traditional methods of natural
recruitment ofseed into ponds, modern fish and shrimpproduction
systems more typically involve
Vet. Res. (2010) 41:51 P.J. Walker, J.R. Winton
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a hatchery/nursery phase in which broodstockare spawned or
stripped for the collection andhatching of eggs, and in which
larvae arenursed through to post-larvae or juvenile stages(i.e.,
fry, smolt, fingerling) for delivery to farms.Broodstock may be
captured from wild fisheriesor produced in captivity from mature
farmedstock or from closed-cycle breeding and geneticimprovement
programs. The use of wild brood-stock that may be healthy carriers
of viralpathogens is arguably the most significant bio-security
risk in aquaculture. Farming systemsemployed for grow-out may be
extensiveor intensive. Extensive farming employs fishor shrimp
trapped at low density in natural orman-made enclosures utilising
natural sourcesof feed with minimal human intervention.Intensive
systems employ medium-to-highstocking densities in cages or ponds
and artifi-cial or supplemental feeds. Intensive pond cul-ture
usually requires aeration and controlledwater exchange to maintain
water quality.Super-intensive recirculating aquaculture sys-tems
(RAS) are also employed for some spe-cies. On-farm biosecurity
measures to excludepathogens and minimise health risks are
morecommonly employed in intensive and super-intensive systems.
1.4. The decline of capture fisheries
Whilst aquaculture has been on a steady pathof expansion,
capture fishery production haslevelled since 1990 and many of the
world’smajor fisheries have been driven into a stateof decline by
unsustainable fishing practicesand environmental pressures. It has
been esti-mated that 11 of the 15 major fishing areasand 80% of
marine fishery resources are cur-rently overexploited or at their
maximum sus-tainable limit [31]. Much of the pressure onwild stocks
is due to commercial fishing butthe increasing popularity of
recreational anglinghas led to a growing awareness of the need
forregulation to ensure marine and inland fisherysustainability.
Disease emergence is also a con-cern in wild fisheries due to
environmentalpressures, the direct impact of human activitiesand
the risk of pathogen spread from aquacul-ture [102].
2. HISTORY OF DISEASE EMERGENCEIN FISH AND SHRIMP
Whilst various forms of disease have beenreported among aquatic
animals for centuries,most were either non-infectious (e.g.,
tumours),or caused by common endemic pathogens(mainly parasites and
bacteria), and thus alreadyknown among observers and those engaged
intraditional aquaculture.However, during the pastcentury, the rise
of novel forms of intensive aqua-culture, increased global movement
of aquaticanimals and their products, and various sourcesof
anthropogenic stress to aquatic ecosystemshave led to the emergence
of many new diseasesin fish and shrimp. In this review, we
considerthese emerging diseases as: (i) new or
previouslyunknowndiseases; (ii) knowndiseases appearingfor first
time in a new species (expanding hostrange); (iii) knowndiseases
appearing for thefirsttime in a new location (expanding
geographicrange); and (iv) known diseases with a newpresentation
(different signs) or higher virulencedue to changes in the
causative agent.
2.1. Problems associated with emerging diseases
Emerging disease epizootics frequently causesubstantial, often
explosive, losses among popu-lations of fish and shrimp, resulting
in largeeconomic losses in commercial aquaculture andthreats to
valuable stocks of wild aquatic ani-mals. However, the extent of
disease spread andimpacts are often exacerbated by other
problemsthat are typically encountered including: (i) delayin
developing tools for the confirmatory diagno-sis of disease or
identification of the causativeagent that allows infected animals
to go unde-tected; (ii) poor knowledge of the current orpotential
host range; (iii) inadequate knowledgeof the present geographic
range; (iv) no under-standing of critical epidemiological factors
(repli-cation cycle, mode of transmission, reservoirs,vectors,
stability); and (v) poor understandingof differences among strains
and/or relationshipsto established pathogens. Interventions to
pre-vent pathogen spread are also often limited bypoor capacity in
some developing countries forimplementation of effective quarantine
and/orbiosecurity measures and the illegal or poorly
Emerging viruses of fish and shrimp Vet. Res. (2010) 41:51
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regulated international trans-boundary move-ment of live aquatic
animals [128, 164].
2.2. Emerging viral diseases of fish
Important emerging viral pathogens of fishare found among many
families of vertebrateviruses that are well-known to include
patho-gens of humans or domestic livestock. How-ever, there are
significant differences betweenthe ecology of viral diseases of
fish and thoseof humans or other terrestrial vertebrates. Themost
significant amongst these differences arethat: (i) few fish viruses
are known to be vec-tored by arthropods; (ii) water is a
stabilizingmedium, but currents are less effective for longrange
virus transmission than are aerosols;(iii) wild reservoir species
are often at verylow densities (except for schooling and aggre-gate
spawning stocks); (iv) fish are poikilo-therms and temperature has
an exceptionallycritical role in modulating the disease processby
affecting both the replication rate of the virusas well as the host
immune response and otherphysiological factors involved in
resistance;(v) few fish viruses are transmitted sexuallybetween
adults, although high levels of someviruses are present in spawning
fluids and afew viruses are transmitted vertically from adultto
progeny, either intra-ovum or on the egg sur-face. However, as
occurs for avian diseases,migratory fish can serve as carriers for
long-range dispersal of viral pathogens.
The global expansion of finfish aquacultureand accompanying
improvements in fish healthsurveillance has led to the discovery of
severalviruses that are new to science. Many of theseare endemic
among native populations andopportunistically spill-over to infect
fish inaquaculture facilities. Other well-characterizedfish viruses
(e.g., channel catfish virus,Onchorhynchus masou virus) can also
causesignificant losses in aquaculture but do notseem to be
increasing significantly in host orgeographic range. In the
following sections,we consider the major emerging fish virus
dis-eases that cause significant losses in aquacultureand are
expanding in host or geographic range(Tab. I). Because of the risk
of spread throughcommercial trade in finfish, many of the dis-
eases are listed as notifiable by the WorldOrganization for
Animal Health (OIE).
2.2.1. Infectious haematopoietic necrosis
Infectious haematopoietic necrosis is oneof three rhabdovirus
diseases of fish that arelisted as notifiable by the OIE.
Originally ende-mic in the western portion of North Americaamong
native species of anadromous salmon,infectious haematopoietic
necrosis virus(IHNV) emerged in the 1970s to become animportant
pathogen of farmed rainbow trout(Oncorhynchus mykiss) in the USA
[11, 156].Subsequently, the virus was spread by the move-ment of
contaminated eggs to several countriesof Western Europe and East
Asia, where itemerged to cause severe losses in farmed rain-bow
trout, an introduced species. Similar toother members of the genus
Novirhabdovirusin the family Rhabdoviridae, IHNV contains
anegative-sense, single-stranded RNA genome,approximately 11 000
nucleotides in lengthand encoding six proteins, packaged within
anenveloped, bullet-shaped virion [67]. Isolatesof IHNV from North
America show a strongphylogeographic signature with relatively
lowgenetic diversity among isolates from sock-eye salmon
(Oncorhynchus nerka) inhabitingthe historic geographic range of the
virus[66]. However, isolates from trout in Europe,Japan or Korea,
where the virus is emerging,show evidence of independent
evolutionaryhistories following their initial introduction[29, 64,
106]. The emergence of IHNV in rain-bow trout aquaculture is
accompanied bygenetic changes that appear to be related to ashift
in host specificity and virulence [112].
2.2.2. Viral haemorrhagic septicaemia
Viral haemorrhagic septicaemia (VHS) isanother emerging disease
caused by a fish rhab-dovirus. Similar to IHNV in morphology
andgenome organization, viral haemorrhagic septi-caemia virus
(VHSV) is also a member of thegenus Novirhabdovirus [67]. The virus
wasinitially isolated and characterized in Europewhere it had
become an important cause of lossamong rainbow trout reared in
aquaculture
Vet. Res. (2010) 41:51 P.J. Walker, J.R. Winton
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Table I. Emerging viral pathogens of finfish.
Virus Abbreviation Genome Taxonomic classification1 Known
geographicdistribution
OIE listed2
DNA virusesEpizootic haematopoietic necrosis virusand other
ranaviruses
EHNV dsDNA Iridoviridae, Ranavirus Australia, Europe, Asia,North
America, Africa
Yes
Red sea bream iridovirus RSIV dsDNA Iridoviridae,
Megalocytivirus Asia YesKoi herpesvirus KHV dsDNA
Alloherpesviridae, Cyprinivirus Asia, Europe, North
America, Israel, AfricaYes
RNA VirusesInfectious haematopoietic necrosis virus IHNV (�)
ssRNA Mononegavirales, Rhabdoviridae,
NovirhabdovirusEurope, North America,
AsiaYes
Viral haemorrhagic septicaemia virus VHSV (�) ssRNA
Mononegavirales, Rhabdoviridae,Novirhabdovirus
Europe, North America,Asia
Yes
Spring viraemia of carp virus SVCV (�) ssRNA Mononegavirales,
Rhabdoviridae,Vesiculovirus
Europe, Asia, North andSouth America
Yes
Infectious salmon anaemia virus ISAV (�) ssRNA Orthomyxoviridae,
Isavirus Europe, North and SouthAmerica
Yes
Viral nervous necrosis virus VNNV (+) ssRNA Nodaviridae,
Betanodavirus Australia, Asia, Europe,North America, Africa,
South Pacific
No
1 ICVT, 2009.2 OIE, 2009.
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[123]. Prior to the 1980s, VHSV was assumedto be largely endemic
among native freshwaterspecies of fish in Western Europe where
itspilled-over to the introduced, and presumablymore susceptible,
rainbow trout [156]. Subse-quently, an increasing number of
virologicalsurveys of anadromous and marine fish in theNorth
Pacific and North Atlantic Oceansrevealed a much greater host and
geographicrange than previously recognized [35, 91, 99,121], and
VHSV was shown to cause signifi-cant losses in both cultured and
free-rangingspecies of marine fish [48, 56]. The understand-ing
that VHS appeared to be an emerging dis-ease of marine fish as a
result of both greatersurveillance efforts and the development
ofnovel forms of marine fish aquaculture was fur-ther extended when
VHS emerged for the firsttime in the Great Lakes of North
America.The explosive losses among free-ranging nativespecies
revealed how devastating the diseasecan be when first introduced
into naive popula-tions of freshwater fish [28, 40, 84].
2.2.3. Spring viraemia of carp
Spring viraemia of carp (SVC) is also causedby a fish
rhabdovirus (SVCV). However, unlikeIHNVand VHSV, SVCV is related to
rhabdovi-ruses in the genus Vesiculovirus in having anenveloped,
bullet-shaped virion with somewhatshorter morphology and lacking
the non-viriongene characteristic of novirhabdoviruses
[67].Initially believed to be endemic among com-mon carp (Cyprinus
carpio) in Eastern andWestern Europe, the disease appeared in
thespring to cause large losses among farm-rearedcarp [2, 156].
More recently, SVCV hasemerged in several regions of the world
whereit has been associated with very large lossesin common carp
and its ornamental form, thekoi carp. These outbreaks have occurred
in bothfarmed and wild fish, suggesting a recent rangeexpansion.
The emergence of SVC in NorthAmerica, Asia and in portions of
Europe, for-merly free of the virus, appears to be a resultof both
improved surveillance and the globalshipment of large volumes of
ornamental fish,including koi carp. Genotyping of isolates ofSVCV
and a closely related fish rhabdovirus
from Europe, pike fry rhabdovirus, fromvarious locations have
revealed the isolatesform four major genetic clades [127], and
thatthe isolates of SVCV representing the recentemergence and
geographic range expansionappear to have links to the spread of the
viruswithin China where common carp are rearedin large numbers for
food and koi are rearedfor export [92].
2.2.4. Infectious salmon anaemia
Infectious salmon anaemia (ISA) is anemerging disease of farmed
Atlantic salmon(Salmo salar) caused by a member of the fam-ily
Orthomyxoviridae. The virus (ISAV) haseight independent genome
segments ofnegative-sense, single-stranded RNA pack-aged within a
pleomorphic, enveloped virion,approximately 100–130 nm in diameter,
andis the type species of the genus Isavirus. Ini-tially identified
as the causative agent of out-breaks and high rates of mortality
amongAtlantic salmon reared in sea cages in parts ofNorway [109],
ISAV subsequently emerged tocause losses in other areas of Western
Europewhere Atlantic salmon are farmed [95]. Thevirus was also
confirmed to be the cause ofan emerging hemorrhagic kidney disease
offarmed Atlantic salmon along the Atlantic coastof Canada and the
USA [82]. Isolates of ISAVform two major genotypes containing
isolatesfrom Europe and North America, respectively[62]. More
recently, ISAV has caused veryextensive losses in the Atlantic
salmon farmingindustry in Chile. Genetic analysis has revealedthat
the Chilean isolates group with those fromNorway and that the virus
was likely transferredto Chile sometime around 1996 by the
move-ment of infected eggs [63]. Although princi-pally known as a
pathogen of Atlanticsalmon, ISAV has been isolated from
naturallyinfected marine species that are apparent reser-voirs for
virus spill-over to susceptible Atlanticsalmon in sea cages [115].
Investigation of vir-ulence determinants of ISAV has also
revealedsignificant differences among isolates [88].Thus, the
emergence of ISA appears to be aresponse to the farming of a
susceptible speciesin an endemic area, evolution of the virus
and
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some degree of transmission via the movementof fish or eggs used
in aquaculture.
2.2.5. Koi herpesvirus disease
The disease caused by koi herpesvirus(KHV) is amongst the most
dramatic examplesof an emerging disease of fish. KHV is a mem-ber
of the genus Cyprinivirus in the familyAlloherpesviridae. Koi
herpesvirus disease isrelatively host-specific; although other
cyprinidspecies have been shown to be susceptible, onlycommon carp
(C. carpio) and its ornamentalsubspecies, the koi carp, have been
involvedin the explosive losses that have been reportedglobally in
areas where the virus has been firstintroduced [47]. The enveloped
virion of KHV,formally classified as the species Cyprinid
her-pesvirus 3, has a morphology typical of herpe-sviruses and
contains a double-stranded DNAgenome of approximately 295 kbp [5].
Molecu-lar analysis has shown little variation amongisolates, as
might be expected for a virus thatis being rapidly disseminated by
the globalmovement of infected fish [37]; however, minorvariation
has been reported that may reflect atleast two independent
introductions or emer-gence events of KHV [68]. A significant
prob-lem is that once fish are infected, the viruspersists for some
period of time in a latent orcarrier state without obvious clinical
signs[125]. It appears that the movement of suchcarriers via the
extensive trade in cultured orna-mental fish has resulted in the
rapid appearanceof the disease in many regions of the world[41]. In
addition, the release or stocking ofornamental fish into ponds and
other naturalwaters has resulted in the introduction ofKHV to naive
wild populations, where the ini-tial exposure can result in
substantial mortality.
2.2.6. Epizootic haematopoietic necrosisand other ranavirus
diseases
Epizootic haematopoietic necrosis is causedby a large DNA virus
(EHNV) which is classi-fied in the genus Ranavirus of the family
Irido-viridae [152]. Initially discovered in Australiawhere it was
identified as an important causeof mortality among both cultured
rainbow trout
and a native species, the redfin perch [71], itlater became
clear that EHNV was but one ofa large pool of ranaviruses having a
broad hostand geographic range that included amphibians,fish and
reptiles [53]. Isolated from sub-clinicalinfections as well as
severely diseased fish ineither aquaculture or the wild, the
geneticallydiverse, but related, ranaviruses have beengiven many
names in different locations [86].Although, there is evidence of
spread bythe movement of infected fish, either naturallyor via
trade, an important driver of the emer-gence of ranavirus diseases
in finfish aquacul-ture seems to be the spill-over of virus
fromendemic reservoirs among native fish, amphib-ians or reptiles
[152]. In this regard, ranavirusesrelated to the type species, Frog
Virus 3, havebeen shown to be an important cause of emerg-ing
disease among both cultured and wildamphibian populations and may
be associated,at least in some areas, with their global
decline[19]. Both the large, unregulated global trade inamphibians
and the unintended movement ofranaviruses by humans, including
anglers andbiologists, have been postulated to be importantmethods
of dissemination of these relativelystable viruses to new aquatic
habitats [114].
2.2.7. Red sea bream iridoviral disease and othermegalocytivirus
diseases
Another group of emerging iridovirusescauses disease in marine
as well as freshwaterfish species [19]. Initially identified in
1990 asthe cause of high rate of mortality among cul-tured red sea
bream (Pagrus major) in south-western Japan [54], the causative
agenttermed red sea bream iridovirus (RSIV) wasshown to affect at
least 31 species of marinefish cultured in the region [60, 89].
Antigenicand molecular analyses revealed the causativeagent of
these outbreaks differed from otherknown fish iridoviruses [69,
103]. Soon,reports began to emerge that similar viral dis-eases in
new hosts and other geographic areasof Asia were associated with
novel iridovirusesincluding: infectious spleen and kidney necro-sis
iridovirus (ISKNV) from cultured manda-rinfish (Sinaperca chuatsi)
in southern China,sea bass (Lateolabrax sp.) iridovirus (SBIV)
Emerging viruses of fish and shrimp Vet. Res. (2010) 41:51
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from Hong Kong, rock bream (Oplegnathusfasciatus) iridovirus
(RBIV) from Koreaand the orange-spotted grouper
(Epinepheluscoiodes) iridovirus (OSGIV) from China[27, 45, 83, 94].
Sequence analysis showedthese and several additional, but
related,viruses formed a novel group and have beenassigned to the
genus Megalocytivirus in thefamily Iridoviridae, with ISKNV as the
typespecies [27, 46, 69, 83]. In addition to causingoutbreaks
associated with severe necrosis andhigh mortality in a wide range
of cultured mar-ine fish, these viruses have emerged to
affectfreshwater species such as the African
lampeye(Aplocheilichthys normani) and dwarf gourami(Colisa lalia)
in which they have caused addi-tional losses [132]. Molecular
epidemiologicalstudies have shown that megalocytivirusesform at
least three genetic lineages. There isevidence that some of the
initial outbreaks inmarine species were due to spill-over
fromviruses endemic among free-ranging fishes; inother cases, there
are clear links to the interna-tional movement of both marine and
ornamen-tal fish [132, 150, 152].
2.2.8. Viral nervous necrosis and othernodavirus diseases
Viral nervous necrosis (VNN) has emergedto become a major
problem in the culture of lar-val and juvenile marine fish
worldwide [101].Initially described as a cause of substantial
mor-tality among cultured barramundi (Lates calca-rifer) in
Australia where the disease was termedvacuolating encephalopathy
and retinopathy,the condition was shown to be caused by asmall,
icosahedral virus that resisted cultivationin available cell lines,
but appeared similar topicornaviruses [38, 100]. Around the
sametime, efforts to expand marine fish aquaculturein other regions
of the world revealed diseaseconditions associated with similar
viruses inlarvae or juveniles from a range of speciesincluding
turbot (Scophthalmus maximus) inNorway [8], sea bass (Dicentrarchus
labrax) inMartinique and the French Mediterranean [12],and
parrotfish (Oplegnathus fasciatus) and red-spotted grouper
(Epinephelus akaara) in Japan[97, 163]. In Japan, the disease was
termed ner-
vous necrosis and the virus infecting larvalstriped jack
(Pseudocaranx dentex), nowassigned as the species Striped jack
nervousnecrosis virus (SJNNV), was shown to be aputative member of
the family Nodaviridae[98]. Following isolation in cell culture
[34],sequence analysis of the coat protein genesupported the
creation of a novel genus,Betanodavirus, within the family
Nodaviridaeto include isolates of fish nodaviruses from var-ious
hosts and geographic locations [104, 105].These and other
phylogenetic analyses [23,122, 139] revealed that genetic lineages
of thebetanodaviruses show low host specificity andgenerally
correspond to geographic location,indicating they emerged due to
spill-over fromreservoirs that include a broad range of wildmarine
fish, although some isolates revealedlinks to commercial
movement.
2.3. Emerging viral diseases of shrimp
Shrimp is the largest single seafood com-modity by value,
accounting for 17% of allinternationally traded fishery products.
Approx-imately 75% of production is from aquaculturewhich is now
almost entirely dominated by twospecies – the black tiger shrimp
(Penaeus mon-odon) and the white Pacific shrimp (Penaeusvannamei)
that represent the two most impor-tant invertebrate food animals
[32]. Diseasehas had a major impact on the shrimp farmingindustry.
Since 1981, a succession of new viralpathogens has emerged in Asia
and the Ameri-cas, causing mass mortalities and threateningthe
economic sustainability of the industry[148]. Shrimp are arthropods
and most shrimpviruses are either related to those previouslyknown
to infect insects (e.g., densoviruses, di-cistroviruses,
baculoviruses, nodaviruses, lute-oviruses) or are completely new to
scienceand have been assigned to new taxa (Tab. II).
Several important characteristics are com-mon to shrimp diseases
and distinguish themfrom most viruses of terrestrial or aquatic
verte-brates. Firstly, as invertebrates, shrimp lack thekey
components of adaptive and innate immuneresponse mechanisms (i.e.,
antibodies, lympho-cytes, cytokines, interferon) and,
althoughToll-like receptors have been identified, there
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Table II. Emerging viral pathogens of marine and freshwater
shrimp.
Virus Abbreviation Genome Taxonomicclassification1
Year emerged Known geographicdistribution
OIE listed disease2
DNA virusesMonodon baculovirus MBV dsDNA Baculoviridae 1977
Asia-Pacific, Americas, Africa NoBaculoviral midgut gland necrosis
virus BMNV dsDNA Baculoviridae 1971 Asia, Australia NoWhite spot
syndrome virus WSSV dsDNA Nimaviridae,
Whispovirus1992 Asia, Middle-East,
Mediterranean, AmericasYes
Infectious hypodermal andhaematopoietic necrosis virus
IHHNV ssDNA Parvoviridae,Densovirus
1981 Asia-Pacific, Africa, Madagascar,Middle-East, Americas
Yes
Hepatopancreatic parvovirus HPV ssDNA
Parvoviridae,Densovirus
1983 Asia-Pacific, Africa, Madagascar,Middle-East, Americas
No
RNA virusesYellow head virus YHV (+) ssRNA Nidovirales,
Roniviridae,
Okavirus1990 East and Southeast Asia, Mexico Yes
Taura syndrome virus TSV (+) ssRNA
Picornavirales,Dicistroviridae
1992 Americas, East and SoutheastAsia
Yes
Infectious myonecrosis virus IMNV (+) ssRNA Totivirus
(unclassified) 2002 Brazil, Indonesia, Thailand,China
Yes
Macrobrachium rosenbergii nodavirus MrNV (+) ssRNA Nodavirus
(unclassified) 1995 India, China, Taiwan, Thailand,Australia,
Caribbean
Yes
Laem-Singh virus LSNV (+) dsRNA
Luteovirus-like(unclassified)
2003 South and Southeast Asia No
Mourilyan virus MoV (�) ssRNA Bunyavirus-like(unclassified)
1996 Australia, Asia No
1 ICTV, 2009.2 OIE, 2009.
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is little evidence that they are involved in anti-viral immunity
[70, 160]. RNA interference(RNAi) does appear to have a role in the
anti-viral defensive response of shrimp and there isevidence that
viral proteins can induce a short-lived protective immunity [57,
118]. However,as is the case for insects, the response of shrimpto
viral infection is poorly understood and thesubject of intensive
research. The second distin-guishing feature is that most of the
major patho-genic viruses cause very low level persistentinfections
that can occur at moderate to veryhigh prevalence in apparently
health shrimppopulations [16, 51, 108, 133, 145]. Almostall shrimp
pathogens are transmitted vertically(but usually not
transovarially) and disease isthe result of a massive viral
amplification thatfollows exposure to various forms of environ-ment
or physiological stress [22, 81, 113, 119].Stressors can include
handling, spawning, poorwater quality or abrupt changes in
temperatureor salinity. Shrimp viruses can also commonlybe
transmitted horizontally and, once viral loadsare high and disease
is manifest, horizontaltransmission of infection is accompanied
bytransmission of disease. The third significantcharacteristic is a
logical consequence of the for-mer two in that shrimp commonly can
beinfected simultaneously or sequentially withmultiple viruses
[33], or even different strainsof the same virus [50]. These
characteristicspresent a very different landscape for the
inter-action of pathogen and host and significant chal-lenges for
diagnosis, detection, pathogenexclusion and the use of
prophylactics in healthmanagement. Viruses listed by the OIE as
caus-ing notifiable diseases of marine and freshwatershrimp are
reviewed briefly in this section.
2.3.1. White spot syndrome
White spot syndrome first emerged in FujianProvince of China in
1992 [165]. It was soonafter reported in Taiwan and Japan and
hassince become panzootic throughout shrimpfarming regions of Asia
and the Americas[148]. It is the most devastating disease offarmed
shrimp with social and economicimpacts over 15 years on a scale
that is seldomseen, even for the most important diseases of
terrestrial animals. White spot syndrome virus(WSSV) is a large,
enveloped, ovaloid DNAvirus with a flagellum-like tail and helical
nucle-ocapsid that has been classified as the onlymem-ber of the
new family Nimaviridae, genusWhispovirus [144, 158]. The � 300 kbp
viralgenomecontains at least 181ORF,most ofwhichencode polypeptides
with no detectable homol-ogy to other known proteins [142,
159].Although first emerging in farmed kurumashrimp (Penaeus
japonicus), WSSV has a verybroad host range amongst decapod
crustaceans(e.g., marine and freshwater shrimp, crabs, lob-sters,
crayfish, etc.), all of which appear to besusceptible to infection
[72]. However, suscepti-bility to disease varies and some
crustaceanspecies have been reported to develop very highviral
loads in the absence of clinical signs[162]. All farmed marine
(penaeid) shrimpspecies are highly susceptible to white
spotdisease, with mass mortalities commonly reach-ing 80–100% in
ponds within a period of 3–10days [20, 77]. Persistent, low level
infections inshrimp and other crustaceans occur commonly,sometimes
at levels that are not detectable, evenby nested PCR. The
amplification of viral loadsand onset of disease can be induced by
environ-mental or physiological stress [80, 113], or atambient
temperatures below 30 �C [39, 143].
WSSV was not known prior to its emer-gence in China and the
original source of infec-tion has not been determined. However,
thespread of infection throughout most of Asiaduring the mid-1990s
and subsequently to theAmericas from 2001 was explosive and
wasalmost certainly the consequence of a prolificinternational
trade in live shrimp and other crus-tacean seed and broodstock
[76]. The suscepti-bility of all decapods and absence of evidenceof
replication in other organisms suggests thevirus is of crustacean
origin but it remains amystery why a virus with such broad host
rangeand ease of transmission was not long estab-lished globally in
crustacean populations priorto the advent of aquaculture [148].
2.3.2. Taura syndrome
Taura syndrome first emerged in whitePacific shrimp (P.
vannamei) farms on the
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Taura River near Guayaquil in Ecuador in1992, almost
simultaneously with the emer-gence of WSSV in kuruma shrimp in
China[43]. The disease spread rapidly throughoutmost shrimp farming
regions of Central andSouth America [75]. In 1998, it was
detectedin Taiwan and has now spread throughoutmuch of Asia [140].
Taura syndrome virus(TSV) is a small, naked (+) ssRNA virus thatis
currently classified as an unassigned speciesin the family
Dicistroviridae, order Picornavi-rales [21]. The most closely
related knownviruses include insect viruses in the genusCripavirus
such as cricket paralysis virus anddrosophila C virus [21, 87].
Acute, transitional(recovery) and chronic phases of TSV
infectionhave been described [44]. Mortalities in theacute phase
can be as high as 95% but surviv-ing shrimp remain infected and a
potentialsource of virus transmission. The susceptiblehost range of
TSV is far more restricted thanthat of WSSV but includes most
farmed marineshrimp species. However, susceptibility to dis-ease
varies and virulence varies for differentstrains of the virus.
Other crustaceans includingfreshwater shrimp and crabs appear to be
resis-tant to disease but may be potential carriers[61]. Birds and
water-boatmen (Trichocorixareticulata) have been proposed as
possiblemechanical vectors [14, 36, 126]. The focal ori-gin of the
TSV panzootic and absence of evi-dence of infection prior to the
first outbreaksuggest that, as for WSSV, penaeid shrimpare not the
natural host. The rapid spread ofTSV in the Americas and then to
Asia has alsobeen attributed to the international trade in
liveshrimp.
2.3.3. Yellow head disease
Yellow head virus (YHV) is the most viru-lent of shrimp
pathogens, commonly causingtotal crop loss within several days of
the firstsigns of disease in a pond. It first emerged inblack tiger
shrimp (P. monodon) in CentralThailand in 1990 and has since been
reportedin most major shrimp farming countries inAsia, including
India, Indonesia, Malaysia, thePhilippines, Sri Lanka, Vietnam and
Taiwan[17, 145]. There is also a recent unconfirmed
report that YHV is present in farmed P. vanna-mei and P.
stylirostris in Mexico [25]. YHV isan enveloped, rod-shaped (+)
ssRNA viruswith a helical nucleocapsid and prominent gly-coprotein
projections on the virion surface[157]. The particle morphology and
organisa-tion and expression strategy of the � 26 kbgenome indicate
that it is most closely relatedto vertebrate coronaviruses,
toroviruses andarteriviruses, and it has been classified withinthe
order Nidovirales in the family Ronivirus,genus Okavirus [147]. It
is now known thatYHV is one of a complex of six closelyrelated
viruses infecting P. monodon shrimp[153]. Gill-associated virus
(GAV) is a far lessvirulent virus that emerged to cause
mid-cropmortality syndrome in farmed P. monodon inAustralia in 1996
[124]. However, the preva-lence of GAV infection in healthy P.
monodonbroodstock and farmed shrimp in Australia hasbeen reported
to approach 100% and, althoughdisease can be transmitted by
injection orexposure per os to moribund shrimp, out-breaks in ponds
are most likely the result ofamplification of viral loads as a
consequenceof environmental stress. The other four knowngenotypes
in the complex have been detectedonly in healthy P. monodon in Asia
and,although they occur at high prevalence inmany locations, they
are not known to beassociated with disease [153]. Many other
pen-aeid and palemonid shrimp species have beenshown to be
susceptible to experimental infec-tion with YHV or GAV, but
yellow-head-complex viruses are detected rarely in otherpenaeid
shrimp species and P. monodonappears to be the natural host [148].
Neverthe-less, the very high virulence of YHV for pen-aeid shrimp
does suggest that this genotypemay enter ponds via an alternative
reservoirhost. Homologous genetic recombination isalso a feature of
the yellow head complex.A recent study has indicated that � 30%
ofyellow-head-complex viruses detected inP. monodon from across the
Asia-Pacificregion are recombinants [154]. The prevalenceand
geographic distribution of these recombi-nant viruses suggests that
aquaculture and theinternational trade in live shrimp are the
sourceof rapidly increasing viral genetic diversity.
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2.3.4. Infectious hypodermal and haematopoieticnecrosis
Infectious hypodermal and haematopoieticnecrosis was first
detected in Hawaii in 1981,causing mass mortalities in blue
shrimp(Penaeus stylirostris) farmed in super-intensiveraceways
[74]. Infectious hypodermal and hae-matopoietic necrosis virus
(IHHNV) is a small,naked, ssDNA virus that has been classifiedwith
several insect viruses in the family Parvo-viridae, genus
Brevidensovirus [21]. Followingits initial detection in Hawaii,
IHHNV wasfound to be widely distributed in both P. styliros-tris
and P. vannamei shrimp throughout farmingregions of the Americas
and in the wild shrimppopulation of the Gulf of California
wheresome reports suggest that it may have contrib-uted to the
collapse of the capture fishery[96, 111]. Although it does not
cause mortalitiesin P. vannamei, IHHNV has been shown toreduce
growth by up to 30% and cause deformi-ties of the rostrum and
anterior appendages in acondition called ‘‘runt deformity
syndrome’’[59]. In Asia, IHHNV is endemic and occurscommonly in P.
monodon shrimp which appearsto be the natural host and in which it
does notcause disease and has no impact on growth orfecundity [18,
155]. Four genotypes of IHHNVhave been identified of which two have
beenshown to be integrated into host genomicDNA and experimental
transmission studiessuggest they may not be infectious for P.
mon-odon or P. vannamei shrimp [65, 135, 136].The other two
genotypes can be transmitted hor-izontally by injection, ingestion
or exposure toinfected water, or vertically from infectedfemales
[73]. Genetic evidence suggests thatP. monodon imported from the
Philippines werethe source of the epizootic in the Americas,
indi-cating that disease emergence has been the con-sequence of an
expanded host range providingopportunities for pathogenicity and a
vastlyexpanded geographic distribution [134].
2.3.5. Infectious myonecrosis
Infectious myonecrosis is the most recentlyemerging of the major
viral diseases of marineshrimp. It first appeared in farmed P.
vannamei
shrimp at Pernambuco in Brazil in 2002 andhas subsequently
spread throughout coastalregions of north-east Brazil and to
Indonesia,Thailand and Hainan Province in China[4, 79, 120]. The
original source of infectionis unknown but the trans-continental
spreadhas almost certainly been due to the volumi-nous trade in P.
vannamei broodstock. Shrimpwith the acute form of the disease
display vari-ous degrees of skeletal muscle necrosis, visibleas an
opaque, whitish discolouration of theabdomen [137]. Surviving
shrimp progress toa chronic phase with persistent low-level
mor-talities. Infectious myonecrosis virus (IMNV)is a small, naked,
icosahedral, dsRNAvirus thatis most closely related to members of
the familyTotiviridae, genus Giardiavirus [116]. The onlyother
known members of this family infectyeasts and protozoa. Several
farmed marineshrimp species have been reported to besusceptible to
infection but disease has onlybeen reported in white Pacific shrimp
[137].The increasingly common practice in parts ofAsia of
co-cultivation of white Pacific shrimpand black tiger shrimp is
likely to presentopportunities for adaptation and further spreadof
the disease.
2.3.6. White tail disease
White tail disease is an emerging infectionof the giant
freshwater shrimp Macrobrachiumrosenbergii. It was first reported
in 1995 fromthe island of Guadeloupe and then nearbyMartinique in
the French West Indies, and hassince been reported from China,
Taiwan,Thailand, India and Australia [6, 110, 117,141, 161]. The
disease can affect larvae, post-larvae and early juvenile stages,
causing up to100% mortalities within 5–7 days of the firstgross
signs which include a white or milkyappearance of abdominal muscle
[42, 117].Adults are resistant to the disease but can
bepersistently infected and transmit the infectionvertically.
Marine shrimp (Penaeus monodon,P. japonicus and P. indicus) have
been shownto be susceptible to infection but did notdevelop
disease, and artemia and some spe-cies of aquatic insects appear to
be vectors[130, 131]. White tail disease is caused by a
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small, naked (+) ssRNA virus that has beennamed Macrobrachium
rosenbergii nodavirus(MrNV). Sequence alignments indicate that itis
related to but distinct from nodaviruses ofinsects (genus
Alphanodavirus) and nodavirus-es of fish (genus Betanodavirus) [9].
A verysmall satellite virus (extra small virus, XSV)appears to be
universally associated with natu-ral MrNV infections but is not the
direct causeof disease [117]. As the native endemic range
ofMacrobrachium rosenbergii is restricted tosouth and south-east
Asia, the wide geographicdistribution of the disease most likely
has beendue to the movement of stock for aquaculturepurposes.
Nevertheless, the detection in 2007of a distinct strain of MrNV in
Macrobrachiumrosenbergii broodstock captured from theremote
Flinders River in western Queensland,Australia [110], where there
is a long-standingenforced prohibition on the importation of
livecrustaceans, suggests that the virus is a naturalinfection of
freshwater shrimp. Penaeus vanna-mei nodavirus (PvNV) is a distinct
but relatedvirus that was detected in 2004 in cultured mar-ine
shrimp in Belize displaying the gross signsof white tail disease
[138].
3. IMPACTS OF EMERGING DISEASESOF FISH AND SHRIMP
3.1. Economic and social impacts
The impacts of emerging diseases of aquaticanimals have been
substantial; all have affectedlivelihoods locally and many have
impacted onregional or national economies. The most dev-astating
economic and social impacts have beenin shrimp aquaculture for
which it was esti-mated in 1996 that the global direct and
indirectcosts of emerging diseases had reached $US 3billion
annually or 40% of the total productioncapacity of the industry
[55, 85]. The most sig-nificant production losses have immediately
fol-lowed the emergence of each of the majorpathogens, with ensuing
periods of poor pro-ductivity and reduced rates of industry
expan-sion during which pathogens have beenidentified and
characterised, diagnosis anddetection methods developed, and
improved
biosecurity measures implemented [10, 148].In many cases,
impacts have continued formany years, particularly for small
low-incomefarmers in developing countries who lack theknowledge,
skill and resources to respondeffectively. WSSV has been by far the
mostdevastating of the shrimp pathogens. It has beenestimated that
the impact of WSSV in Asiaalone during the 10 years after its
emergencein 1992 was $US 4–6 billion [78]. In the Amer-icas, the
emergence of WSSV in 1999–2000resulted in immediate losses
estimated at $US1 billion. The combined impacts of TSV andIHHNVon
aquaculture and wild shrimp fisher-ies in the Americas have been
estimated at $US1.5–3 billion [44, 78]. The consequences of
dis-ease emergence for some countries have beenso severe that
shrimp production has never fullyrecovered. Beyond the direct
effects on produc-tion and profitability, disease impacts on
theincome and food-security of small-holdershrimp farmers and the
job security of workerson larger farms and in feed mills and
processingplants, with a flow-on effect to the sustaininglocal
communities [148].
The global economic losses in fish aquacul-ture due to
infectious diseases are of a lessermagnitude, but still highly
important in severalways and can be crippling for farmers. Not
onlyare many individual animals of greater commer-cial value (e.g.,
koi carp) but the disruption ofconsistent production schedules by
companiesengaged in intensive aquaculture can result inloss of
market share. The emergence of ISAVin Scotland in 1998–1999 is
estimated to havecost the industry � $US 35 million andresulted in
an ongoing annual loss of $US 25million to the industries in Norway
and Canada.The estimated cost of the emergence of KHV inIndonesia
was in excess of $US 15 million dur-ing the first 3 years [10],
with ongoing socio-economic impacts on low-income,
small-holderfarmers.
3.2. Environmental impacts
Environmental impacts of emerging diseasesof aquatic animals
have been both direct andindirect. Disease can impact directly on
wildpopulations and the ecosystem by changing
Emerging viruses of fish and shrimp Vet. Res. (2010) 41:51
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host abundance and predator/prey populations,reducing genetic
diversity and causing localextinctions [7]. The emergence of
pilchard her-pesvirus in Australasia during the 1990s wasone of the
most dramatic examples of large-scale impact on ecosystems.
Commencing inMarch 1995, mass mortalities occurred in wildpilchard
(Sardinops sagax neopilchardus) pop-ulations across 5 000 km of the
Australiancoastline and 500 km of the coastline ofNew Zealand [58].
The epizootic subsided inSeptember 1995 but a second more severe
waveof mortalities occurred between October 1998and April 1999 with
vast numbers of pilchardswashed onto southern Australian beaches
andmortality rates in pilchard populations as highas 75% [151]. The
causative agent was identi-fied as a previously unknown fish
herpesvirus,but the source of the epidemic has never beenidentified
[52]. Beyond the direct impact on pil-chard populations, wider
secondary impacts onpiscivorous species were observed.
Penguinssuffered increased mortalities and failed tobreed due to
food shortage [24]. The contribu-tion of pilchards to the diet of
the Australiangannet (Morus serrator) declined from 60%to 5%
following the mortality event and wascompensated by feeding on
species with lowercalorific value [15]. As pilchards are
importantprey for seabirds, fish and marine mammals,other secondary
impacts were likely. The recentintroduction of VHSV to the Great
Lakes Basinhas also resulted in large-scale mortalities andspread
to at least 25 native freshwater fish spe-cies with potential for
similar broader environ-mental impacts [1].
Despite their panzoootic distribution in aqua-culture systems
and wide crustacean host range,direct environmental impacts of
shrimp viruseshave not been commonly observed. It has beenreported
that IHHNV impacted on wildP. stylirostris fisheries in the Gulf of
Mexico fol-lowing its introduction in 1987 [96] but
rigorousenvironmental assessments of the impact of thisor other
shrimp pathogens have not been con-ducted. Indirect environmental
impacts of dis-ease in shrimp aquaculture are more clearlyevident.
These include the destruction of man-grove habitats due to pond
abandonment andrelocation to new sites, soil salinisation in
inland
areas due to avoidance of disease-prone coastalzones, and use of
antibiotics, disinfectants andother chemicals to prevent or treat
disease inponds [3, 93, 148]. Difficulties in managing dis-ease in
native Asian marine shrimp species havealso led to an extraordinary
shift in productionsince 2001 to imported P. vannamei for whichSPF
stock are readily available [13]. The naturalhabitat of this
species is the west coast of CentralAmerica but it now accounts for
67.1% of totalfarmed shrimp production in Asia [32], repre-senting
a massive species translocation forwhich the impacts on local
biodiversity remainuncertain.
4. FACTORS CONTRIBUTING TO DISEASEEMERGENCE IN AQUATIC
ANIMALS
The increasing rate of emergence of diseasesof fish and shrimp
has been driven primarily byanthropogenic influences, the most
profound ofwhich have been associated with the globalexpansion of
aquaculture. Farming of aquaticanimals commonly involves
displacement fromtheir natural habitat to an environment that isnew
and sometimes stressful, the use of feedsthat are sometimes live
and often unnatural orartificial, and culture in stocking densities
thatare much higher than occur naturally. This hasprovided
opportunities for exposure to newpathogens and conditions that can
compromisedefensive responses and facilitate pathogen rep-lication
and disease transmission [146, 148].Most importantly, the growth in
aquacultureand increasing international trade in seafoodhas
resulted in the rapid movement of aquaticanimals and their
products, with associated risksof the trans-boundary movement of
pathogens[129]. Other diseases have been spread by nat-ural or
unintentional movement of infectedhosts or amplified by invasive
species, whileanthropogenic environmental pressures havecaused
changes in the severity of several ende-mic diseases. Better
surveillance activitiesbased upon novel and more sensitive toolsand
their application in new species and geo-graphic areas have also
contributed to an appar-ent expansion of host or geographic
range,sometimes dramatically.
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4.1. Activities related to the global expansionof
aquaculture
Emerging viral diseases of fish or shrimpare usually caused
either by (i) viruses that nat-urally infect the target species but
are unob-served or not normally pathogenic in wild orunstressed
populations, or (ii) the spill-over ofviruses from other species
that may not beencountered naturally. Virus infections
occurcommonly in apparently healthy populationsof wild fish and
shrimp and, although diseaseoutbreaks may occasionally occur, these
oftenpass undetected and are not essential to sustainthe natural
cycle of transmission [149]. Inshrimp, IHHNV, yellow-head-complex
virusesand possibly MrNVappear to be naturally ende-mic in healthy
wild populations and haveemergedas significantpathogensonly asa
conse-quence of aquaculture practices. In the case ofIHHNV, disease
emergence has been due to thetranslocation of the natural host, P.
monodon,from the Philippines to Hawaii and theAmericasfor use in
aquaculture breeding programs,allowing spill-over into susceptible
westernhemisphere shrimp species [134]. For virusesin the yellow
head complex, the natural preva-lence can approach 100% in some
healthy wildP. monodon populations but stressful cultureconditions,
in combination with yet uncharac-terised virulence determinants,
appear to triggerdisease outbreaks [26, 145, 153]. Similarly,
theemerging fish pathogen ISAV is endemic at rel-atively high
prevalence in wild salmonid popu-lations in Norway and Canada but
has beenassociated with disease only in farmed Atlanticsalmon. It
has been suggested that intensive cul-ture serves to provide
concentrations of suscep-tible animals in which virulent strains of
ISAVemerge due to a combination of high mutationrate and increased
opportunity for virus replica-tion [63]. Other major emerging
pathogens areclearly not naturally endemic in aquaculturespecies
but have spilled-over into both farmedand wild populations as a
consequence of theexposure opportunities provided by the
rapidgrowth of a large and diverse industry. WSSV,TSV and IMNV each
appear to have beeninitially introduced to shrimp populations
fromunidentified sources that could potentially
include experimental live or frozen feeds orco-inhabitants of
terrestrial pond environmentssuch as insects or aquatic
invertebrates. Never-theless, each of these viruses now occurs
com-monly as low-level persistent infections inhealthy shrimp
populations and disease out-breaks are precipitated by
environmental stres-ses associated with aquaculture. In the case
ofWSSV, aquaculture has also provided opportu-nities for spread of
infection to a very widerange of new wild crustacean hosts in
whichthe virus has now become endemic across avast coastal area of
Asia and the Americas.
Amongst finfish pathogens, the ranavirusesand nodaviruses
provide good examples ofthe emergence of disease due to
spill-overfrom wild reservoirs. Prior to the availabilityof large
populations of susceptible speciesreared in aquaculture, the
betanodavi-ruses were endemic but undetected amongfree-ranging
populations of marine fish andvarious ranaviruses were present in a
broadrange of native species that included fish,amphibians and
reptiles. The introduction ofthese viruses to commercial
aquaculture andthe ensuing emergence of disease were likelydue to
the use of open water supplies andwild-caught broodstock.
The intentional or unintentional movementof infected hosts or
pathogens by individualsor companies involved in global
aquacultureor the ornamental fish trade has also been animportant
driver of viral disease emergence inaquatic animals [150]. Exotic
viruses translo-cated into new geographic areas have spreadto cause
major disease outbreaks in populationsof both native and cultured
species and thetrans-boundary movement of aquatic animalscontinues
to be one of the greatest threats tothe productivity and
profitability of aquacultureworldwide. For finfish, this is
exemplified bythe spread of IHNV to Europe and Asia viathe shipment
of contaminated eggs of troutand salmon, the global spread of SVCV
andKHV via the ornamental fish trade and theintroduction of the
pilchard herpesvirus intonative populations of pilchards in
Australiavia baitfish. For shrimp, the prolific interna-tional
trade in live broodstock has been themajor driver of the explosive
trans-boundary
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spread of emerging viral pathogens. The rapidspread of WSSV
throughout Asia and then tothe Americas has been attributed to the
move-ment of live crustaceans [78]. The magnitudeof this problem is
most clearly exemplified bythe mass translocation of many hundreds
ofthousands of white Pacific shrimp broodstockfrom the Americas to
Asia, accompanied bythe introduction of TSV, IMNV and possiblyother
exotic pathogens [13]. The internationaltrade in frozen commodity
shrimp and shrimpproducts has also been recognised as a
potentialmechanism of trans-boundary spread of disease[76]. Several
reports have indicated the pres-ence of infectious WSSV and YHV in
frozencommodity shrimp imported to the USA andAustralia [90, 107].
However, it is yet to beestablished that the trade in infected
frozenproduct has contributed to disease outbreaksin wild or
cultivated shrimp [33b].
4.2. Improved surveillance
Apparent changes in the prevalence and dis-tribution of viral
diseases of fish and shrimp canalso be attributed to improved
surveillance as aresult of the availability of new cell lines
forvirus isolation and characterization, the devel-opment of more
sensitive molecular diagnosticmethods, enhanced testing activity in
naturalecosystems and greatly improved aquatic ani-mal health
diagnostic capability in some devel-oping countries. For some viral
pathogens, theavailability of improved detection and surveil-lance
capabilities has resulted in reports of agreater host or geographic
range than previ-ously known; in other cases, diseases in
differ-ent species or geographic regions have beenshown to be due
to the same or similar viruses.For fish diseases, this is
exemplified by devel-opment of the salmon head kidney (SHK)
cellline to detect and characterize ISAV in Norwaywhich
subsequently led to the identification ofpotential carriers and the
observation thatemerging diseases of Atlantic salmon in Canadaand
Chile were due to isolates of the same virus[82]. Enhanced
surveillance activities alsoresulted in the detection and isolation
of VHSVfrom normal returning adult salmon on the westcoast of North
America in 1988. While initially
appearing as a large geographic range expan-sion, increased
surveillance activities showedthat VHSV is naturally endemic in the
NorthPacific and North Atlantic Oceans among awide range of marine
species [121]. Similarly,investigations in Australia have
identified thatseveral viruses that were previously assumedto be
exotic, occur commonly in healthy shrimppopulations [110]. The
increasing number ofpreviously unknown viruses that have
beenidentified through enhanced surveillance ofhealthy wild fish
and shrimp populations illus-trates how little is currently known
of the aqua-tic virosphere.
4.3. Natural movement of carriers
The emergence of some viral diseases of fishand shrimp has
occurred through expansion ofthe known geographic range via the
naturalmovement of infected hosts, vectors or carrierswith
subsequent exposure of naive, and oftenhighly susceptible, species.
While the mecha-nism is not known with certainty, it is consid-ered
plausible that VHSV was introduced tothe Great Lakes Basin of North
America viathe natural movement of fish up the SaintLawrence River
from the near shore areas oftheAtlantic coast ofCanada. The initial
introduc-tion of the virus into the Great Lakes precededthe
emergence of massive epidemics amongseveral species by at least two
years. This hasgiven rise to speculation that a single
introduc-tion of VHSV resulted in infection of the mostsusceptible
species such as the native muskel-lunge (Esox masquinongy) or the
invasive roundgobi (Neogobius melanostomus) which couldamplify the
virus sufficiently to increase theinfection pressure on a broad
range of naivespecies within the larger ecosystem [40].
4.4. Other anthropogenic factors
The emergence of viral disease in aquaticsystems can also been
driven by anthropogenicfactors unrelated to aquaculture such as
themovement of pathogens or hosts via ballastwater in ships,
movement of bait by anglersand unintentional movement in other
biotic orabiotic vectors. The environmental impacts of
Vet. Res. (2010) 41:51 P.J. Walker, J.R. Winton
Page 16 of 24 (page number not for citation purpose)
-
increasing global population such as increasingloads of
pollutants, contaminants and toxins inaquatic habitats also
threaten the health anddisease-resistance of both native and
farmedfish populations. Finally, water diversions,impoundments,
cooling water inputs and otherwater-use conflicts can result in
environmentalchanges that may be detrimental to the healthof
aquatic species.
5. FUTURE DISEASE EMERGENCE RISKS
The increasing global population, increasingdemand for seafood
and limitations on produc-tion from capture fisheries will
inevitably leadthe continued global expansion of aquaculturewith
associated risks of disease emergence andspread. Africa, in
particular, which currentlycontributes less than 1.3% of global
aquacultureproduction [32], offers significant
developmentopportunities for aquaculture but also presentsa rich
biodiversity that may be the source ofemergence of new aquatic
animal pathogens.There are also disease emergence risks associ-ated
with the increasing diversity of farmed spe-cies, the introduction
of species into newfarming areas and the increasing trend
amongstsmall-holder farmers in some countries towardspolyculture or
alternate cropping of several fishand crustacean species to improve
productivity.
As is the case for terrestrial pathogens, cli-mate change also
looms as a likely future driverof disease emergence in aquatic
animals. Cli-mate change and variability are likely to
bringecological disturbance on a global scale thatwill influence
the suitability of aquaculturefarming sites and has potential to
influencethe growth rate of pathogens and the hostimmune response
to infection, generate thermalstress that will increase
susceptibility to disease,change the distribution of vectors,
carriers andreservoirs and the density or distribution of
sus-ceptible wild species, and alter the physical hab-itat and
farming practices in ways that affectdisease ecology. Nevertheless,
there is a grow-ing awareness of the importance of emergingdiseases
of aquatic animals and it is likely thatthe risks of future disease
emergence will bemitigated somewhat by the development of
improved diagnostic methods and surveillanceefforts, increased
regulatory oversight of aqua-culture with greater levels of health
inspectionfor fish, shrimp and their products involved
ininternational trade, and the development ofnovel vaccines and
therapeutics.
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