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Journal of Invertebrate Pathology 110 (2012) 211–224
Contents lists available at SciVerse ScienceDirect
Journal of Invertebrate Pathology
journal homepage: www.elsevier.com/locate/jip
Minireview
The impact of pathogens on exploited populations of decapod crustaceans
Jeffrey D. Shields ⇑
Virginia Institute of Marine Science, The College of William and Mary, Gloucester Point, VA 23062, USA
a r t i c l e
i n f o
Article history:
Available online 14 March 2012
Keywords:
Lobster
Crab
Fishery
Fisheries
Disease
Outbreak
Epidemic
a b s t r a c t
Several crustacean fisheries have experienced significant outbreaks of disease that have damaged their
industries. Not only do fisheries suffer from direct losses to pathogens, such as disease-induced mortalities or reduced product value, but they can also incur indirect losses such as stunting, castration, and
increased risk of predation. In some cases, the indirect losses can be substantial, yet they are often overlooked by the fishing industry as their primary focus is on recruits to the fishery, and not on the affected
juvenile pre-recruits. Low levels of pathogens are to be expected in natural populations of commercial
species, but baseline data on the prevalence and intensity of even the most common agents is often lacking. It is important to establish baselines for two reasons. First, it is important to know what pathogens
exist in heavily exploited populations so as to gauge their potential to damage the industry; and second,
during outbreaks, it is important to know whether an outbreak is a newly emergent event or whether it is
a component of a cyclical phenomenon. Pathogens frequently act in concert with environmental stressors, and a variety of stressors have contributed to outbreaks of emerging agents in crustacean fisheries.
Pollution, poor water quality, hypoxia, temperature extremes, and overexploitation have all been implicated as stressors in various outbreaks. This review focuses on epidemic diseases of commercially fished
crustaceans. Outbreaks in cultured stocks are not covered. Disease epizootics have occurred in fished
populations of crayfish and shrimp but they are less well known than the issues arising from extensive
aquaculture of these species.
Ó 2012 Elsevier Inc. All rights reserved.
Contents
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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Emergent diseases in lobsters off southern New England .
Bitter crab disease and Hematodinium . . . . . . . . . . . . . . . .
Crayfish plague . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
PaV1 in spiny lobsters . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Egg predation, fishing, and the collapse of crab fisheries .
The indirect effects of rhizocephalans . . . . . . . . . . . . . . . .
Focal outbreaks of other pathogens . . . . . . . . . . . . . . . . . .
Modeling diseases for fisheries management . . . . . . . . . . .
Concluding remarks: diseases in juveniles . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
Crustacean fisheries suffer direct and indirect losses to several
pathogens. Direct losses are mortalities induced by pathogens,
⇑ Fax: +1 804 684 7186.
E-mail address: [email protected]
0022-2011/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.jip.2012.03.011
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but they can be difficult to estimate. Nonetheless, mortalities can
be widespread, causing extensive damage to impacted fishing
communities. For example, the lobster mortality in Long Island
Sound, 1999, devastated the industry in western Long Island Sound
(Pearce and Balcom, 2005). That fishery sustained significant longterm damage due to the extent of the mortality. In addition, some
pathogens can result in a direct loss of individuals by causing the
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J.D. Shields / Journal of Invertebrate Pathology 110 (2012) 211–224
formation of unappealing lesions rendering the crab or lobster
unmarketable. Such animals cannot be marketed whole; hence,
there is a loss in value for downgraded product. For example,
clawed lobsters with epizootic shell disease are either culled
or processed into the lower-valued canned meat industry. Unesthetically appealing seafood can impact public opinion, which
happened to the finfish industry during the Pfiesteria scare in
1997–1998, when fish thought to contain presumptive toxins
depressed the seafood industry (Magnien, 2001). The resulting
hysteria threatened the commercial fishing industry of Chesapeake
Bay because consumers were reluctant to purchase fish from the
region. Most fishermen and their agents strive to sell a quality
product so damage to public opinion can be difficult to repair.
Direct losses from pathogens can also impact unfished segments of the population, typically the juvenile or female subpopulations. Outbreaks in juveniles arguably cause more damage to
fisheries because early life history stages are more sensitive or susceptible to pathogens and environmental stressors. Disease-related
mortalities in juveniles have been documented in at least three
important fisheries that include the blue crab (Callinectes sapidus),
the snow crab (Chionoecetes opilio, Chionoecetes bairdi), and the
Caribbean spiny lobster (Panulirus argus) (e.g., Messick and Shields,
2000; Shields and Behringer, 2004; Shields et al., 2005).
Indirect losses to pathogens can be difficult to assess because
they are cryptic and require ongoing estimation techniques to census populations. However, stunting, castration, and morbidity
leading to increased predation risk are outcomes associated with
several pathogens of crustaceans. In some cases, the indirect losses
can be substantial, yet they are often overlooked by the fishing
industry because their primary focus is on recruits to the fishery,
and not on the affected juvenile pre-recruits. For example, indirect
effects can result from widespread egg mortality which in turn
may limit larval supply (e.g., Wickham, 1986; Brattey et al.,
1985), but this relationship can be difficult to establish at the population level. Nonetheless, mathematical models indicate that parasitic castrators can potentially regulate impacted crustacean
populations (Blower and Roughgarden, 1989a,b). Given that several commercially important crab species harbor parasitic castrators (rhizocephalan barnacles, bopyrid isopods) and egg
predators (nemerteans and amphipods), there is some validity to
the larger impact caused by pathogens which cause indirect effects
on their host populations.
As is often the case in crustacean diseases, the causative
agent in an outbreak is rarely known or unreported until the onset of the initial epizootic. By definition, an outbreak is the
occurrence of a pathogen at greater than baseline levels in a host
population (Center for Disease Control and Prevention, 2007);
thus it is important to know the baseline before one can ascertain the scale or effect of an outbreak. Baseline surveys are critical but often lacking. They can indicate the presence of a
pathogen and give clues as to whether it has the potential to
damage a fishery. Moreover, baselines can indicate whether an
outbreak is a newly emergent event or whether it is a regular
feature in the host population. If a pathogen is an emergent phenomenon, then the underlying (proximate) causes can be examined in more detail.
The scope of this review is to examine how outbreaks of parasites and diseases have impacted several crustacean fisheries. The
primary focus will be on marine species because data and reporting systems are in place due to the use of logbooks and monitoring
efforts of resource agencies. I have not provided an exhaustive review; rather I focus on a few examples to highlight what we know
about how epidemics fulminate in crustacean fisheries and what
effects they can have on fisheries. Disease issues in cultured species, such as shrimp and crayfish, have been reviewed by Edgerton
et al. (2002), Lightner (2005), Flegel (2006) and Walker and Mohan
(2009). They will not be covered here.
2. Emergent diseases in lobsters off southern New England
Several disease issues have recently emerged in the fishery for
the American lobster, Homarus americanus in Long Island Sound
and other sounds off southern New England. In 1999, the pathogenic amoeba Neoparamoeba pemaquidensis emerged in concert
with environmental stressors to decimate the lobster population
in western Long Island Sound (Mullen et al., 2004, 2005; Pearce
and Balcom, 2005). Mortalities were observed in many crustaceans, including the blue crab (Callinectes sapidus), spider crabs
(Libinia spp.), and the rock crab (Cancer irroratus) as well as the
horseshoe crab (Limulus polyphemus). High temperature stress, increased use of pesticides in response to the introduction of West
Nile Virus, and benthic hypoxia appeared to act in synergy with
the ameba to cause a catastrophic mortality (Pearce and Balcom,
2005). The mortality subsided in 2000, but the lobster population
in Long Island Sound has not recovered (Fig. 1) (Long Island Sound
Study, 2011a,b).
Three other disease issues have also emerged in lobsters from
the region. In 2002, lobsters from central Long Island Sound were
diagnosed with calcinosis, a physiological disorder due to temperature stress (Dove, 2005; Dove et al., 2004, 2005). It was thought to
be responsible for smaller mortality events in Long Island Sound.
More recently, lobsters in Long Island Sound have been shown to
have varying degrees of idiopathic blindness, with prevalence hovering around 50%, and many lobsters having a complete loss of vision (Maniscalco and Shields, 2006; Magel et al., 2009; Shields
et al., in press). The causes of the idiopathic blindness were thought
to be associated with environmental issues. A more pressing disease issue has emerged in the form of epizootic shell disease. Prior
to the mass mortality event in western Long Island Sound and
coincidentally after a major oil spill, lobsters from eastern Long
Island Sound and Block Island Sound experienced an unusual outbreak of shell disease (Castro and Angell, 2000). The syndrome,
now termed epizootic shell disease, continues to be a problem in
the region (see below). In addition, in 2000, lobsters from off Maine
began dying from ‘‘limp lobster’’ syndrome, a condition caused by
infection of Vibrio fluvialis (Tall et al., 2003). What made these
emerging diseases problematical was the potential for multiple
stressors to coincide to cause declines in lobster health and viability on a scale not seen before. These emergent diseases appear related to anthropogenically-induced environmental changes, such
as increased bottom temperatures during summers, the general effects of eutrophication (Pearce and Balcom, 2005), and intoxication
from contaminants (Zulkosky et al., 2005). Many of these stressors
can lead to an immunologically compromised animal (Paterson
and Stewart, 1974; DeGuise et al., 2004), that is more susceptible
to secondary infections. That is, the emergent disease issues in lobsters in Long Island Sound are indicators of environmental change
and anthropogenic degradation of the lobsters’ habitat.
Of the disease syndromes mentioned above, epizootic shell disease has received recent attention because of its potential longterm effect on the fishery. Unlike classical shell disease, epizootic
disease has not been shown to be horizontally transmitted to
healthy lobsters in laboratory experiments (Chistoserdov et al.,
2005a,b). It is associated with changes to the bacterial flora, notably
by the presence of Aquimarina homari, a newly described chitinoclastic bacterium in the Flavobacteriaceae (Chistoserdov et al., in
press). Heavily affected animals are not marketable due to gross
external pathology (Fig. 2), which in severe cases presents as the
nearly complete erosion of the dorsal carapace and claws. The etiology of the syndrome remains to be determined, but it appears to be
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(A) Cancer magister
6.00
100
A
B
C
D
90
80
70
4.00
60
3.00
50
40
2.00
30
Egg mortality (%)
Landings (millions lbs)
5.00
20
1.00
10
0.00
1962-63
1964-65
1966-67
1968-69
1970-71
1972-73
1974-75
1976-77
1978-79
1980-81
1982-83
1984-85
1986-87
1988-89
1990-91
1992-93
1994-95
1996-97
1998-99
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2002-03
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0
Fishing Season
100
40
90
35
80
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30
60
25
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15
30
10
20
5
10
0
0
m
m
Fig. 2. Epizootic shell disease in Homarus americanus from Narragansett Bay, RI. (A)
Moderate infection of epizootic shell disease (Lobster RI008), and (B) a heavy
infection of epizootic shell disease (Lobster RI012). The cuticle is friable and can
easily lacerated by routine handling. (C) Oblique section through a lesion from a
lobster with epizootic shell disease. Note the nodulation around the membraneous
layer (arrows) and hemocytic infiltration. Melanization (m) in the endocuticle is
also apparent. Bar = 100 lm. (D) Severe erosion of the cuticle in a lobster (Lobster
RI069) with epizootic shell disease. Melanization of the endocuticle (m) with
remnants of the overlying epicuticle () and nodulation of the membranous layer
(arrows). Bar = 300 lm. (D) Adapted from Shields et al., in press.
Fishing year
(C) Homarus americanus
10
9
Landings (million lbs)
*
*
Egg mortality (%)
45
1954
1956
1958
1960
1962
1964
1966
1968
1970
1972
1974
1976
1978
1980
1982
1984
1986
1988
1990
1992
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1996
Landings (mt)
(B) Paralithodes camtschatica
8
7
CT
NY
6
5
4
3
2
1
2007
2009
2003
2005
2001
1999
1997
1995
1993
1989
1991
1987
1985
1983
1981
0
Fishing year
Fig. 1. Declines in landings of several important crab and lobster species. (A)
Landings for the Dungeness crab, Cancer magister, from Central California (solid)
and egg mortality (dashed) due to Carcinonemertes errans and other fouling agents
on female crabs during the nadir in landings. Data from Pacific States Marine
Fisheries Commission (2011) and Wickham (1986). (B) Landings for the red king
crab, Paralithodes camtschatica, from the Kodiak Fisheries Management Area (solid)
and egg mortality (dashed) due to Carcinonemertes regicides and other fouling
agents on female crabs from Uganik Bay, Kodiak Island. Data from Bechtol and
Kruse (2009) and Kuris et al. (1991). (C) Landings for lobster, Homarus americanus,
from Long Island Sound (New York – solid, Connecticut – dashed) showing the nonrecovery of the stock after the mortality event in western Long Island Sound in
2000, and the emergence of epizootic shell disease in eastern Long Island Sound
since 2000. Data from the Long Island Sound Study (2011a,b).
a complex interplay between environmental changes, contaminants (Biggers and Laufer, 2004; Laufer et al., 2005a,b; Laufer
et al., in press; LeBlanc and Prince, in press), and changes to the bacterial flora on the surface of the lobster that act in concert to weaken
and erode the cuticle (Chistoserdov et al., 2005a,b). Infected lobsters can molt out of the condition, but they can also develop the
syndrome shortly after molting (Castro and Angell, 2000).
The environmental stressors that have contributed to epizootic
shell disease have not been fully elucidated. The high prevalence in
lobsters off Rhode Island, eastern Connecticut and southern Massachussetts suggests that a contaminant may be involved. Indeed, the
largest oil spill in Long Island Sound, the North Cape spill, killed an
estimated 7 million lobsters off Rhode Island in winter 1996–1997
(NOAA, 2009a,b). However, the fuel oil that spilled was highly volatile and unlikely to remain present for several years. The coincidental occurrence of shell disease in summer, 1997, is hard to
ignore, but there are high levels of other contaminants, such as
polycyclic biphenyls (PCBs), pesticides, metals, and polycyclic aromatic hydrocarbons (PAHs), in the sediments of Long Island Sound
and Buzzards Bay (e.g., Long Island Sound Study, 2011b; Buzzards
Bay National Estuaries Program, 2011). However, one group of contaminants in particular, the alkylphenols, have been found in lobsters and sediments from Long Island Sound (Biggers and Laufer,
2004; Laufer et al., 2005a). The alkylphenols are used as antioxidants and surfactants in industrial applications. Those found in
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lobsters are known analogs for Juvenile Hormone and can disrupt
molting activity (Biggers and Laufer, 2004; Jacobs et al., in press;
Laufer et al., in press). Thus, while there is no single etiology resolved for epizootic shell disease, there is evidence that environmental contaminants may weaken the cuticle of lobsters making
it more susceptible to a dysbiotic bacterial community with increased prevalence of chitinoclastic invaders (Chistoserdov et al.,
in press).
Epizootic shell disease has primarily impacted the lobster fishery off Southern New England. The quantity and quality of commercial lobster landings have declined over time (Cobb and
Castro, 2006). Affected lobsters have been found in Narragansett
Bay, Block Island Sound off Rhode Island, and eastern portions of
central Long Island Sound (Castro and Angell, 2000; Castro et al.,
2005; Landers, 2005; Powell et al., 2005), but diseased lobsters
have also been reported from Buzzards Bay north to Cape Cod
Bay off Massachusetts (Glenn and Pugh, 2005). The incidence of
the syndrome has increased, with prevalence ranging from 25%
to 30% of the lobster population, and as high as 65% in ovigerous
females (Castro et al., 2005; Glenn and Pugh, 2005; Howell et al.,
2005; Landers, 2005). Mortality in laboratory-held animals can
be high (Stevens, 2009); moreover, the impact on the ovigerous females, with their reduced molting frequency, appears to have affected the number of larvae in the ecosystem as well as the
number of new recruits to the fishery (Wahle et al., 2009). Consequently, there has been serious discussion of imposing a moratorium on this once valuable fishery off southern New England
(Atlantic States Marine Fisheries Commission, 2010).
3. Bitter crab disease and Hematodinium
Several important crab fisheries and a lobster fishery have been
seriously impacted by parasitic dinoflagellates in the genus Hematodinium (Fig. 3). Bitter crab disease, or bitter crab syndrome, affects Tanner and snow crabs in the fjords of southeastern Alaska
in the Pacific (Meyers et al., 1987, 1990), and the bays of northern
Newfoundland in the Atlantic (Taylor and Khan, 1995; Dawe, 2002;
Shields et al., 2005). Infected crabs develop an unusual condition
which renders them bitter when cooked and unmarketable. In
the first recognized outbreak in southeastern Alaska, infected crabs
represented up to a third of the commercial landings (Meyers et al.,
1990). An outbreak in the velvet crab (Necora puber) fishery off
Brittany, France, resulted in a catastrophic loss of crabs (Wilhelm
and Mialhe, 1996). Recurrent epizootics have damaged the Norway
lobster fishery off Scotland (Field et al., 1992, 1998; Stentiford
et al., 2001), and the blue crab fishery off the western Atlantic,
USA (Messick, 1994; Messick and Shields, 2000).
There is evidence that the recent epizootics of the pathogen in
colder boreal waters are emergent phenomena and not simply a result of better reporting or increased scientific awareness. Two outbreaks of Hematodinium sp. have been documented in snow crabs,
C. opilio, from Newfoundland. Surveys of the snow crab in the
coastal bays reported very low levels of the parasite in the early
1990s (Taylor and Khan, 1995), but in later surveys prevalence increased significantly (Pestal et al., 2003; Shields et al., 2005, 2007).
The first outbreak occurred from 1999 to 2000 and mostly affected
female and juvenile crabs (Shields et al., 2005). From 2003 to 2005,
another epidemic occurred, but it affected primarily the largeclawed mature males, with a prevalence of up to 35% (Shields
et al., 2007). This latter epidemic was associated with a 1 °C increase in bottom temperature, which caused an apparent fivefold
increase in molting activity in larger crabs. Because crabs may become infected shortly after molting, the large number of newly
molted, susceptible animals may have fueled the epidemic over
the three-year period. Female and juvenile crabs had a prevalence
A
B
C
D
E
F
Fig. 3. Hematodinium infections in crabs. (A) Ameboid trophonts or sporonts of
Hematodinum sp. from the snow crab, Chionoecetes opilio, from Conception Bay,
Newfoundland, showing marked uptake of the vital stain, 0.3% neutral red. (B)
Similar uptake of 0.3% neutral red in an ameboid trophont of Hematodinium sp. from
the blue crab, Callinectes sapidus from Virginia, USA. Note the lack of uptake in the
adjacent host hemocytes. Inset: hemolymph from a blue crab showing discoloration
from a late-stage infection of Hematodinium. (Photo credit, C. Li.) (C) Unstained
ameboid trophonts (arrows) can be mistaken for host hyalinocytes. (D) An
arachnoid trophont isolated from Hematodinium sp. from the blue crab and
cultured as in Li et al. (in press). (Photo credit, T. Miller.) (E) Ameboid trophonts
(H, arrows) in the lumen of the heart, and (F) gills of a blue crab. An arteriole in the
heart shows the normal architecture of the fixed phagocytes (P). (Photo credit, K.
Wheeler).
that was similar to that seen in the earlier outbreak. Both epidemics occurred in Conception Bay, a large bay with a shallow sill that
entrains water within it. Epidemics do not appear to occur in open
ocean areas (Meyers et al., 1996; Mullowney et al., 2011).
Outbreaks of Hematodinium in the Norway lobster fishery off
western Scotland cost an estimated £2–4 million annually (Field
et al., 1992). Outbreaks occur seasonally in the fishery and prevalence can reach 70% during the height of the outbreaks, which occur in winter months (Field et al., 1998; Stentiford et al., 2001). As
with other Hematodinium infections, the highest prevalence of disease occurs in and around the Scottish fjords (Field et al., 1992,
1998; Stentiford et al., 2001). Outbreaks of Hematodinium are common in the American blue crab, particularly in coastal bays and lagoons with high salinities (Messick and Shields, 2000). In Virginia
and Maryland, periodic summer and autumn mortalities are cryptic, but losses to the fishery may exceed $500,000 per year in
nonepidemic years (Stentiford and Shields, 2005). An outbreak in
the early 1990s reached a prevalence of 100% in juvenile crabs
(Messick, 1994). Infections are usually fatal (Shields and Squyars,
2000). Similar outbreaks have been reported off the coast of Georgia (USA), particularly in relation to drought (Lee and Frischer,
2004). Losses due to Hematodinium in the Tanner crab fishery of
southeastern Alaska were estimated to exceed $250,000 in landings (Meyers et al., 1987), but the actual cost in terms of losses
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to females and juveniles, which are more heavily impacted, was
not assessed.
Outbreaks of Hematodinium are associated with distinct physiographic features, such as fjords or shallow, poorly drained bays,
and lagoons (Shields, 1994; Stentiford and Shields, 2005). Such features are ideal for the growth and spread of pathogens as they serve
to focus transmissive stages or retain them within the system. These
regions possesses four features that may facilitate epidemics of
Hematodinium and other pathogens: (1) relatively ‘‘closed’’ host
populations (i.e., those with little immigration and emigration of
juveniles and adults; but not necessarily closed to larvae), (2) restricted exchange with the open ocean which retains transmissive
stages (i.e., narrow channels with shallow sills, deep confined areas,
entrained water masses), (3) stressful conditions for the host population (i.e., summer and winter thermal stress, high salinity, seasonal
hypoxia, intense fishing pressure), and (4) a pathogen that can amplify rapidly within a population. This pattern has been reported in
several other pathogens that affect commercial fisheries, e.g., Briarosaccus callosus (Sloan, 1984), Loxothylacus texanus (Alvarez and
Calderon, 1995), Sacculina granifera (Shields and Wood, 1993), Carcinonemertes regicides (Kuris et al., 1991).
Management of Hematodinium in diseased hosts remains challenging. Bitter crab disease is unpalatable, and a single infected
crab can ruin an entire batch of cooked crabs; hence, fishers cull infected crabs. Resource managers have warned fishers to destroy
their infected, culled crabs or dispose of them in landfills rather
than return them to the sea (David Taylor, Resource Biologist,
Department of Fisheries and Oceans, Canada, personal communication). This can present a problem in outbreak years when large
numbers of overtly infected crabs require disposal. Infected Norway lobsters and blue crabs do not have an altered flavor per se,
but their flesh is pasty and unappetizing (Shields personal observation). Fishers can recognize heavily infected Norway lobsters and
blue crabs by their altered coloration and separate them from their
catches. In the blue crab fishery, some fishers go to great lengths to
insure a high quality product by separating discolored crabs and
changing their fishing locations to areas where they see less
disease.
4. Crayfish plague
Crayfish plague, or krebspest, has an extensive literature due to
its epidemic outbreaks and resulting mortalities in European crayfishes, particularly the noble crayfish (Astacus astacus). Crayfish plague is caused by the pathogenic oomycete, Aphanomyces astaci. It is
probably the first epidemic disease reported from a crustacean. In
the 1850s, the pathogen was introduced into Europe and rapidly
fulminated into a widespread pandemic. It was most likely introduced to northern Italy; probably on crayfish in ballast in ships
from the USA or Canada (see Alderman and Polglase, 1988). From
its first report in Italy (Cornalia, 1860 in Aquiloni et al., 2011), it
spread rapidly to France, 1875, Germany, 1880, Russia, 1890, Finland, 1893, and then into Sweden and Norway (for review see
Alderman and Polglase, 1988; Edgerton et al., 2002). In the 1960s
and 1970s, the pathogen was re-introduced to Europe, primarily
into Sweden, through the importation of infected crayfish, Pacifastacus leniusculus and Procambarus clarkii, from the USA during attempts to revive the crayfish industry (Alderman, 1996; Holdich,
2003). It has since been reported from the United Kingdom,
1981, Turkey, 1984 and Ireland, 1987 (see Holdich, 2003; Edgerton
et al., 2004). This pathogen is a serious pest and is listed by the Office International des Epizooties (OIE 2011). It is also highly invasive, and is listed in the Global Invasive Species Database in their
list of the top 100 Worst Invasive Species (http://issg.org/database/welcome/).
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A. astaci has a relatively simple life history. Zoospores are released from sporangia that protrude through the cuticle of the infected crayfish. The zoospores are motile for up to 3 days, then
encyst, but they are capable of excysting and re-encysting several
times (Unestam, 1969; Svensson and Unestam, 1975; Cerenius
and Söderhäll, 1992). The zoospores will encyst on a susceptible
crayfish then germinate, with the germ tube forming a hypha that
penetrates into and through the cuticle of the host (Nyhlén and
Unestam, 1975). Melanization of the portal of entry and hyphae
can occur in resistant hosts (Unestam and Weiss, 1970). Sporangia
can develop in crayfish cadavers up to 5 days after their death, and
infected cuticle can pass through fish guts and still develop sporangia (Oidtmann et al., 2002).
As its common name implies, crayfish plague has decimated
stocks of European crayfishes. All five of the native crayfish in Europe, as well as many species in Australia and Asia, appear highly
susceptible to the pathogen whereas species of North American
crayfish are mostly resistant to it (Unestam, 1969, 1972). However,
only three North American species, Orconectes limosus, P. leniusculus and P. clarkii, are known vectors to European species (Unestam,
1972). Outbreaks can be sustained and very severe. Native stocks
of A. astacus, which is a delicacy in Northern Europe, have suffered
dramatic declines due introductions of the pathogen. For example,
prior to outbreaks, harvests in Scandinavian and Baltic countries
totaled more than 2000 tons annually; however, they fell to 200
tons afterwards, a 90% decrease in production (Skurdal et al.,
1999).
Epidemics of crayfish plague in native European stocks cause
significant mortalities, but they eventually subside, or burn out,
typically with a local loss of the host species in an affected lake
or stream. Because the pathogen can only survive a few weeks
without a host, control efforts have focused around management
of affected areas by letting them remain fallow, then reseeding
them with unaffected stock (e.g., Taugbøl et al., 1993; Spink and
Frayling, 2000). However, fallowing may not work in complex lake
systems where the pathogen may subsist at low levels (Fürst, 1990
cited in Taugbøl et al., 1993). Re-introducing uninfected crayfish
requires excellent diagnostic tools, which have been developed
(Oidtmann et al., 2004, 2006), as well as disinfection protocols
(e.g., Alderman et al., 1987; Jussila et al., 2011), but quarantine
and fallowing are still primary tools in rehabilitating stocks
(Diéguez-Uribeondo, 2006). Unfortunately, efforts to re-establish
the native species have been hindered by the introduction of the
non-indigenous species, and their removal can be problematic
(Cerenius et al., 2002).
The European species of crayfish have come under serious
threat with significant population declines due primarily to habitat
fragmentation and degradation, overfishing, degraded water quality, competition from introduced crayfish, and disease, primarily in
the form of crayfish plague. Indeed, A. astaci and environmental
degradation were thought responsible for the extirpation of the
white-clawed crayfish, Austropotamobius pallipes, from Portugal
(Bernardo et al., 1997; Holdich et al., 2006). Legislation to protect
the native species has been established in various European countries (see reviews by Holdich, 2003; Holdich et al., 2009), but the
losses in populations and collapsed ranges have been notable. Human influences are largely responsible for the introduction of crayfish plague and for the ongoing impacts to native crayfish species.
The extensive literature on crayfish plague has focused on host
immunology, control of the infection, and more recently on documenting the occurrence of plague in different populations. For indepth reviews of crayfish plague, see Alderman and Polglase
(1988), Alderman (1996), Holdich (2003), Edgerton et al. (2002),
Diéguez-Uribeondo (2006), and an extensive review of the crayfish
populations under threat of disease by Holdich et al. (2009).
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5. PaV1 in spiny lobsters
Panulirus argus Virus 1 (PaV1) is a pathogenic virus in the Caribbean spiny lobster (Fig. 4). It has been implicated as a possible contributor to the decline in spiny lobster landings from the Florida
Keys (Shields and Behringer, 2004). It is an unenveloped, icosahedral, DNA virus that infects host hemocytes, spongy connective tissues, and other mesodermally derived cells (Shields and Behringer,
2004; Li et al., 2006). Lobsters heavily infected with PaV1 are often
lethargic with milky hemolymph that does not clot. The mode of
transmission is via contact with diseased lobsters or from waterborne sources (Butler et al., 2008), but vertical transmission has
not been ruled out as infections have been reported in adults
(Shields and Behringer, 2004; Huchin-Mian et al., 2009) and postlarvae (Moss et al., 2012). Infectivity of the virus is negatively correlated with lobster size. In contact transmission trials, 63% of early
benthic juveniles (<25 mm carapace length, CL) became infected
versus 33% of larger juveniles (30–40 mm CL), and only 11% in
the largest juveniles (>40–50 mm CL) (Butler et al., 2008).
PaV1 appears to have different outcomes in different life history
stages. In field studies that examined visual signs of infection,
prevalence was highest, 16%, among small juveniles (<20 mm
CL), 5% among larger juveniles (>40 mm CL), and lowest, <1%, in
adults (Shields and Behringer, 2004). Mortality can be very high
in small juvenile lobsters, approaching 100% in early benthic juveniles, but larger juveniles and adults can apparently develop
chronic, possibly life-long infections (Shields and Behringer,
2004; Butler et al., 2008; Moss et al., 2012). Short-term mark-recapture studies indicate that overtly diseased lobsters have lower
recapture rates than animals without overt disease (Behringer
et al., 2008).
The decline in landings in the spiny lobster fishery in the Florida
Keys coincided with the finding of PaV1 (Shields and Behringer,
2004). The virus is widespread in the shallow nurseries for juvenile
lobsters in the Florida Keys. Overall prevalence in the Keys was 7%,
B
A
C
*
D
*
Fig. 4. PaV1 in spiny lobsters. (A) Taking hemolymph from a juvenile lobster in the
laboratory. The syringe is inserted between the basis and ischium of one of the
walking legs. (B) Infected fixed phagocytes (arrows) in the hepatopancreas.
Bar = 20 lm. (C) Transmission electron micrograph of an infected hemocyte
showing the condensed, emarginated chromatin (arrows) in the hypertrophied
nucleus with clumps of virions () within. Bar = 2 lm. (D) Rosette of infected fixed
phagocytes (arrows) surrounding an arteriole in the heart. Bar = 40 lm. (C) adapted
with permission from Li et al., 2006.
with 30% prevalence in focal areas (Shields and Behringer, 2004).
Prevalence in the Keys has remained 6–10% over several years
(Behringer et al., 2011; Moss et al., 2012), which suggests that
background levels are relatively stable. The prevalence of PaV1 in
lobsters off Puerto Morelos and Chinchorro Bank, Mexico, was
2.5–10.9% (Lozano-Álvarez et al., 2008). The virus has been reported from several places around the Caribbean Sea, including
the Florida Keys, US Virgin Islands, Mexico, Cuba, and Belize (Butler
et al., 2008; Huchin-Mian et al., 2008, 2009; Quintana et al., 2010).
Additional studies will no doubt reveal a more widespread distribution of the virus in the Caribbean.
In the Florida Keys, the fishing practices for the Caribbean spiny
lobster entail using pots baited with live juvenile lobsters. Lobsters
are socially gregarious and are attracted to pots containing live animals. Unfortunately, this practice may facilitate the transmission
of PaV1 (Behringer et al., 2012). The close proximity of lobsters
confined in traps and the confinement of juveniles by the hundreds
in live-wells, along with the physiological stress induced by such
practices, may enhance transmission of the disease. Transport of
juvenile lobsters throughout the fishing grounds may also facilitate
the spread of the pathogen. PaV1 and its potential effect on the
spiny lobster fishery in the Florida Keys is cause for some concern.
Moreover, live lobsters and lobster tails are increasingly shipped
widely from Caribbean ports. Huchin-Mian et al. (2009) reported
PaV1 from frozen lobster tails bound for international markets. Given the possibility of transshipment to new areas, it would be wise
to quarantine or screen lobsters for the virus as well as other
microbial infections to prevent their potential introduction into
other areas.
6. Egg predation, fishing, and the collapse of crab fisheries
Egg mortality due to pathogens has been implicated in the
decline or non-recovery of two important fisheries, the Dungeness and the red king crabs. The Dungeness crab (Cancer magister) supports important fisheries off the western USA and
Canada. In the late 1950s, the stock off Central California declined by 80–90% (Heimann and Carlisle, 1970), but it has shown
substantial recovery from 1986 to the present (Fig. 1) (Pacific
States Marine Fisheries Commission, 2011). In the 1970s, egg
mortality due to microbial agents was implicated as a possible
cause of the decline. Egg mortalities were 10–50% of the clutch
in crabs near San Francisco, but mortality was significantly less
in Northern California through Washington (Fisher, 1976; Fisher
and Wickham, 1976). Filamentous bacteria (Leucothrix mucor)
and the oomycete Lagenidium sp., were thought to cause these
mortalities (Fisher, 1976), but a nemertean worm, Carcinonemertes errans, was later implicated as the primary agent of mortality
(Wickham, 1979; Shields and Kuris, 1988). In Central California,
prevalence was nearly 100% on ovigerous females and worm
intensities were highly correlated with egg mortalities (Wickham,
1979, 1986). The high prevalence of the worm and consequent
egg mortality appeared to suppress the recovery of the Central
California stock of the Dungeness crab (Fisher and Wickham,
1976; Wickham, 1979, 1980, 1986). Stocks further north were
not impacted.
Three factors were thought to facilitate the outbreaks of the
nemertean (Wickham, 1979, 1986). In the late 1950s the exploitation of the Central California crab stock was extraordinarily high,
with record landings in 1957. The intense fishing pressure led to
the removal of a large segment of the crab population which fueled
the mass settlement of worms on the few remaining crabs. The
worm densities increased such that wide-spread egg mortality
(analogous to population-wide castration) ensued, which was further exacerbated by the colonization of secondary pathogens into
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the affected clutches. Increased exploitation and egg mortality
resulted in a feedback of higher intensity worm infestations and
additional egg predation which continued to affect recruitment.
Central California represents the southern-most range of the fishery for the Dungeness crab; hence, this portion of the stock may
be prone to large variations in highly variable wind- and currentdriven recruitment events. Models of this system indicate that
worm density alone could not destabilize the crab population,
but it could depress the recovery of the stock (Botsford and Wickham, 1979), particularly when coupled with density-dependent
recruitment (Hobbs and Botsford, 1989).
The red king crab fishery (Paralithodes camtschaticus) off Kodiak
Island, Alaska declined precipitously in the late 1960s and again in
the early 1980s. The collapse occurred directly after a peak in crab
abundance, which co-occurred with intense fishing pressure
(Fig. 1) (Blau, 1986; Bechtol and Kruse, 2009). Coincidental with
the collapse in the 1980s, egg mortalities were quite high in ovigerous crabs, reaching an average 90% egg mortality in areas with
outbreaks (Kuris et al., 1991). The primary culprit was C. regicides,
but several undescribed species were also found (Shields et al.,
1989, 1990; Kuris et al., 1991). Newly hatched larvae can autoinfect their hosts, and therefore reach explosively high intensities
(>600,000 worms per clutch) over a short period (Fig. 5) (Kuris
et al., 1991). Egg mortality was correlated with worm intensity
only during summer months because the worms did not remain
at high intensities in other months.
Several factors may have contributed to the decline and nonrecovery of the red king stock. Again, intense fishing pressure led
to the removal of a huge biomass of crabs which may have led
to the mass settlement of worms on the few remaining crabs.
The resulting egg predation was widespread and further reduced
A
C
B
D
Fig. 5. Nemertean infestation within the egg clutch of an ovigerous red king crab.
(A) A single pleopod removed for processing in a large petri dish. (B) Thousands of
nemerteans along with a few crab eggs found on the pleopod in (A) after processing.
(C) A live specimen of Carcinonemertes regicidens showing the stylet (arrow) in the
proboscis chamber. A scale is shown in (D). (D) Composite drawing of the female
and male of C. regicides (redrawn with permission from Shields et al. (1989). Note
the small size of these worms.
217
the production of recruits into the system. Moreover, fjord systems may entrain larvae of the host crab as well as the infectious stages of their parasites, thereby enhancing transmission
to new hosts (Sloan, 1984; Hawkes et al., 1986; Kuris et al.,
1991). Coupled with the limited exchange that occurs in fjord
systems, autoinfection of hosts and explosive transmission to
new hosts led to very high prevalences and intensities over a
short period (Kuris et al., 1991). The resulting egg mortality negatively affected larval recruitment of crabs in these ‘‘closed’’ systems. It is not clear if these systems continue to have high
intensities infections, but landings of red king crab have not returned to their former levels (Fig. 1) (Bechtol and Kruse, 2009;
NOAA, 2011).
The American lobster, H. americanus, is also infested with a
nemertean, Pseudocarcinonemertes homari. High intensity infections have been reported but the worm is typically found at low
intensities on its host (Aiken et al., 1985). Fisheries for the American lobster do not appear to be damaged by the worm and it may
be because lobsters preen their clutches to reduce their infestations. While some crab species preen their clutches, their worms
are much smaller than those on the lobster and are unlikely to
be removed by preening.
Infestations of nemertean egg predators have not been studied
since the early 1990s. For those fisheries that have been impacted
by these parasites, continued surveillance would be prudent. Monitoring can be as simple as sampling and preserving a pleopod from
egg clutches from a resource survey for later assessment. Storage of
samples and their proper curation requires planning, but the information gained could be useful in assessing the effects of these
interesting egg predators as well as providing data on host fecundity for recruitment models.
7. The indirect effects of rhizocephalans
Rhizocephalan barnacles can be found at high levels of prevalence in crab and shrimp populations. These barnacles are
highly modified parasites that castrate, feminize, stunt, cause
anecdysis, and in some cases even kill their hosts. The external
sac of the parasite masquerades as the egg mass of their host
(Fig. 6) and the parasite often changes the behavior of male
hosts to make them less aggressive and more like pre-ovigerous
females. Their high prevalence in a population may potentially
lead to regulation of their host populations (e.g., Blower and
Roughgarden, 1989a,b).
Several commercially important crabs are infected by rhizocephalan barnacles. Lithodid crabs from boreal and arctic waters
are often infected by B. callosus. This parasite reaches a prevalence
of up to 75% in king crabs in fjords off British Columbia (Sloan,
1984) and southeastern Alaska (Hawkes et al., 1985, 1986) and
up to 20% in the southern king crab from South Georgia Island near
Antarctica (Watters, 1998). In temperate waters, portunid crabs often have a high prevalence of rhizocephalans. The prevalence of S.
granifera in Portunus pelagicus can reach 40% or more (Phillips and
Cannon, 1978; Weng, 1987; Shields and Wood, 1993). The prevalence of L. texanus in the American blue crab, C. sapidus, ranges
from 30 to 70% in lagoons and embayments around the Gulf of
Mexico (Christmas, 1969; Ragan and Matherne, 1974; Wardle
and Tirpak, 1991; Alvarez and Calderon, 1996; Lázaro-Chávez
et al., 1996; Alvarez et al., 1999). The prevalence of Sacculina carcini
can reach 90% in the green crab, C. maenas (Stentiford and Feist,
2005), and locally high prevalence is a common phenomenon with
this species (Heath, 1971; Stentiford and Feist, 2005). A rhizocephalan, Sylon hippolytes, can reach fairly high levels on commercially
fished shrimp, but it has otherwise received little attention (Bower
and Boutillier, 1988).
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A
C
B
D
E
identical parasites (Shields and Wood, 1993). At high prevalence,
sterile matings and lost fecundity can be quantified.
Outbreaks of rhizocephalans are facilitated by several environmental factors. As with the nemertean infestations, fjords
with their limited water exchange and shallow sills serve as foci
for B. callosus in king crabs (Sloan, 1984, Hawkes et al., 1986).
Fjords frequently possess entrained water masses with long residence times (age of water) that enhance transmission of the
infectious cyprid larva. Similarly, other physiographically confined habitats such as shallow lagoons and embayments with
long residence times can also facilitate outbreaks of rhizocephalans, Paramoeba, and Hematodinium infections in portunid crabs
(Sprague et al., 1969; Alvarez and Calderón, 1996; Messick and
Shields, 2000; Shields and Overstreet, 2007). In basic models,
rhizocephalan castrators can affect their host populations when
present in ecologically closed systems (Kuris and Lafferty,
1992). Confined habitats limit dispersal of transmissive stages,
limit their dilution, and lead to high prevalence (Kuris and Lafferty, 1992). Therefore, an outbreak of rhizocephalans in a commercially fished population of crabs or shrimps could
potentially damage the fishery by altering the population structure of the fished population. Stunting, lost fecundity, and increased mortality could all impose costs to the fishery.
8. Focal outbreaks of other pathogens
Fig. 6. Rhizocephalan infections in crabs. (A, B, E) Briarosaccus callosus on the
golden king crab, Lithodes aequispina, from fjords in British Columbia. Note how the
external sac of the parasite resembles the color and granularity of the egg clutch of
the female. (Photos from Sloan, 1984) (C and D) Loxothylacus texanus infections in
the blue crab, Callinectes sapidus. Note the ovigerous female in (C) is nearly three
times the size of the infected female. Those in (D) are infected with the parasite
(with permission from Overstreet, 1978).
Rhizocephalans typically cause stunting of their hosts and anecdysis, or a cessation of molting. Stunting can reach noticeably high
levels in some populations, including blue crabs (C. sapidus) and
lithodid crabs (Overstreet, 1978; Overstreet et al., 1983; Hawkes
et al., 1985, 1986; Høeg, 1995). Stunted animals do not enter the
fishery and they are often culled back and so may accumulate in
the fishing grounds as ‘‘shorts’’ (Hawkes et al., 1986; Meyers,
1990). This can artificially increase the prevalence of the parasite
due to fishing, but no studies have quantified the effect. Moreover,
the culled returns can serve as foci for transmission to new hosts
(Hawkes et al., 1986; Meyers, 1990). The potential for accumulation of shorts in a fished population has led to the suggestion that
fisheries should actively overfish isolated populations to remove
the parasites (Hawkes et al., 1986; Kuris and Lafferty, 1992; Shukalyuk et al., 2005), or kill stunted ‘‘shorts’’ to remove them from
the fishery (Lester et al., 1978), but these practices have not been
implemented because of management issues with killing undersized animals. Rhizocephalans have other insidious effects on their
hosts, although they have been difficult to document at the population level. They include castration, sterile matings, loss of fecundity, homosexual matings, and competition with phenotypically
Focal outbreaks of various pathogens have been reported from
disparate commercial fisheries (Table 1). The agents range from
typical microbial pathogens (viruses, bacteria, fungi) to more unusual parasitic agents (protistans, bopyrid isopods). The effects of
the pathogens are as diverse as their systematic range, with some
causing outright mortality and others reducing marketability
through overt pathologies. A few of the better documented pathogens are highlighted below.
Viral pathogens cause significant morbidity and mortality in
shrimp aquaculture, but few have been reported to damaged fisheries. Infectious Hypodermal and Hematopoietic Necrosis Virus,
IHHNV, was introduced into the Gulf of California from transshipment of infected postlarvae of Penaeus vannamei in or around 1987
(Lightner et al., 1992, Morales-Covarrubias et al., 1999). By 1990, it
was widely distributed in the Gulf of California in several shrimp, P.
stylirostris, as well as P. vannamei and P. californiensis (Pantoja et al.,
1999). At the time, infections of IHHNV in P. stylirostris in aquaculture facilities were severe, leading to mortalities, with subsequent
closure of facilities. The virus was also associated with major declines in the landings in the fishery for P. stylirostris in the early
1990s (Pantoja et al., 1999). A later study found very high prevalence of IHHNV in P. stylirostris, but the fishery appeared to be
recovering (Morales-Covarrubias et al., 1999). Thus, while IHHNV
may have contributed to the decline in the fishery for P. stylirostris,
the impact of the initial epizootic has apparently subsided.
In the late 1990s, the mangrove land crab, Ucides cordatus, of
northern Brazil experienced a series of mass mortalities (Boeger
et al., 2005). The crab supports a significant artisanal fishery with
many households reliant on the crab for income (Glaser, 2003).
Several anthropogenic activities, such as sugar-cane culture,
shrimp farming, oil extraction, and lumbering, were thought to directly account for the mortalities, but a pathogenic fungus had the
strongest association with disease. Fishing yields were reduced by
84–98% in some localities (Nóbrega and Nishida, 2003). While
Koch’s postulates have not been fulfilled for the agent, histopathology and molecular genetics point to a black yeast, Exophiala sp., as
the etiological agent (Boeger et al., 2007).
Gaffkemia, or red-tail disease, is a disease of the American
lobster, H. americanus. It is caused by Aerococcus viridans, a
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Table 1
Pathogens that have potentially impacted commercially important fished crustaceans, by host species, pathogen of concern, primary effect of the pathogen, and key references
selected by the author.
Fishery
Pathogen/condition
Primary effect
Key references
Lobsters
Homarus americanus
Homarus americanus
Homarus americanus
Homarus americanus
Homarus americanus
Homarus americanus
Nephrops norvegicus
Panulirus argus
Aerococcus viridans
Epizootic shell disease
Vibrio fluvialis
Anophryoides haemophila
Neoparamoeba pemaquidensis
Pseudocarcinonemertes homari
Hematodinium sp.
PaV1
Mortality
Mortality?
Mortality
Mortality
Mortality
Egg mortality?
Mortality
Juvenile mortality
Stewart et al. (1966)
Wahle et al. (2009)
Tall et al. (2003)
Aiken et al. (1973) and Cawthorn et al. (1996)
Mullen et al. (2004, 2005)
Brattey et al. (1985)
Field et al. (1992) and Stentiford et al. (2001)
Shields and Behringer (2004) and Behringer et al. (2012)
Crabs
Callinectes sapidus
Callinectes sapidus
Callinectes sapidus
Callinectes sapidus
Callinectes sapidus
Callinectes sapidus
Cancer magister
Cancer magister
Cancer pagurus
Chionoecetes bairdi
Chionoecetes opilio
Lithodes aequispina
Paralithodes platypus
Paralithodes platypus
Paralithodes camtschatica
Paralomis granulosa
Lithodes santolla
Ucides cordatus
Various viruses
Reovirus
Vibrio spp.
Paramoeba perniciosa
Hematodinium sp.
Loxothylacus texanus
Nadelspora canceri
Carcinonemertes errans
Hematodinium sp.
Hematodinium sp.
Hematodinium sp.
Briarosaccus callosus
Briarosaccus callosus
Herpes-like virus
Carcinonemertes regicides
Pseudione tuberculata
Pseudione tuberculata
Fungus
Mortality?
Mortality?
Mortality?
Mortality
Mortality
Castration, stunting
Mortality?
Egg predation
Mortality?
Mortality
Mortality
Castration, stunting
Castration, stunting
Mortality?
Egg predation
Mortality? Stunting?
Stunting?
Mortality
Johnson (1983)
Bowers et al. (2010) and Tang et al. (2011)
Tubiash et al. (1975) and Welsh and Sizemore (1985)
Sprague and Beckett (1966)
Messick and Shields (2000)
Ragan and Matherne (1974)
Childers et al. (1996)
Wickham (1979)
Stentiford (2008)
Meyers et al. (1987)
Shields et al. (2005, 2007)
Sloan (1984)
Hawkes et al. (1986)
Sparks and Morado (1986)
Kuris et al. (1991)
Lovrich and Vinuesa (1993)
Cañete et al. (2008)
Boeger et al. (2005, 2007)
Aphanomyces astaci
Thelohania spp.
Mortality
Mortality
Alderman and Polglase (1988)
Edgerton et al. (2002)
Epipenaeon ingens
IHHNV
Castration
Mortality
Owens (1990, 1993)
Morales-Covarrubias et al. (1999) and Pantoja et al. (1999)
Crayfish
Astacus astacus
Shrimp
Penaeus semisulcatus P. esculentus
Penaeus stylirostris
tetrad-forming, gram-positive bacterium. A mortality event in
1893 may have been caused by gaffkemia, but signs of disease
were not well described (Herrick, 1909). Gaffkemia is primarily a
disease of confined lobsters, capable of causing significant mortalities in holding facilities, but focal outbreaks have occurred in natural populations (Rabin, 1965; Stewart et al., 1966; Keith et al.,
1992; Lavallée et al., 2001). Infected lobsters occur throughout
much of the Canadian Atlantic (Stewart et al., 1966) and Gulf of
Maine (Vachon et al., 1981). It has also been reported in wild European lobsters, H. gammarus, from the Orkney Islands and Norway,
but at very low levels (Wiik et al., 1987; Nilsen et al., 2002). The
pathogen may have been introduced to Europe via the shipment
of American lobsters to Norway (Alderman, 1996; Jørstad et al.,
1999a,b), but, there is some controversy about its introduction
and whether it has become established in natural populations
(Egidius, 1972). There is continued concern regarding reintroductions of this pathogen into European stocks. For more extensive
reviews of gaffkemia and other diseases in clawed lobsters, see
Stewart (1980), Shields et al. (2006), and Cawthorn (2011).
Bumper car disease is a disease in American lobsters that is
caused by a scuticociliate, Anophyroides haemophila. Infections of
this pathogen were first noticed in the early 1970s in lobsters held
in impoundments (Aiken et al., 1973), but the agent was not described until later (Cawthorn et al., 1996). Outbreaks of the ciliate
can cause considerable losses to impounded lobsters (Greenwood
et al., 2005). Prevalence has been reported in wild stocks of 17–
20% (Aiken et al., 1973; Cawthorn et al., 1996), potentially ranging
to 100% (Sherburne and Bean, 1991), but the pathogen is usually
found at very low levels in wild populations (Brattey and Campbell,
1985; Aiken and Waddy, 1986; Lavallée et al., 2001). Impounded
lobsters showing signs of the disease are often downgraded because of poor muscle mass and quality, and often have an unpleasant flavor (Cawthorn, 1997). This parasite may have considerable
potential to damage the lobster industry; thus, it is surprising that
there are so few studies on its epidemiology.
Paramoeba perniciosa occurs in focal outbreaks in the blue crab
industry along the eastern seaboard of the USA. Outbreaks are often noticed in shedding facilities for soft-shell crabs when large
numbers of crabs become moribund and die (Sawyer, 1969; Sprague et al., 1969; Couch, 1983). Crabs often have a dark sternum,
hence the moniker ‘‘gray crab disease’’. Epizootics ranged in prevalence from 17 to 35% in crabs held at shedding facilities (Sawyer,
1969; Sprague et al., 1969). Mortality was estimated at 30% per
month in crabs from Chincoteague Bay (Newman and Ward,
1973; Johnson, 1977). As with several pathogens reviewed here,
P. perniciosa has a strong association with physiographic features,
namely seaside coastal bays and lagoons (Sprague and Beckett,
1966; Sawyer, 1969; Messick, 2002). Little is known of this pathogen, and in some cases, it is possible that it has been confused with
the ameboid trophonts of Hematodinium sp. from the same region.
The false king crab in Paralomis granulosa can have very high
parasitization by a bopyrid isopod, Pseudione tuberculata (Lovrich
and Vinuesa, 1993; Roccatagliata and Lovrich, 1999). The isopod
has a predilection for small juvenile crabs, with up to 46% infected.
Some juveniles survive the infection and molt to show no signs of
it. Bopyrids are known castrators and infections can result in
Author's personal copy
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J.D. Shields / Journal of Invertebrate Pathology 110 (2012) 211–224
stunting, selective mortality, or altered behaviors of infected hosts
(O’Brien and Van Wyk, 1985). While the prevalence of P. tuberculata is low in the reproductive population of crabs (1.2%) (Roccatagliata and Lovrich, 1999), there is some evidence of stunting in
infected juveniles (Cañete et al., 2008).
In Australia, the bopyrid Epipenaeon ingens can infect up to 30%
of its host prawns Penaeus semisulcatus, and P. esculentis, both of
which are castrated by the infection (Owens and Glazebrook,
1985; Owens, 1990). Because of the relatively high prevalence of
the parasite, losses to the industry have been estimated at up to
$A5 million due to lost production from castration as well as increased processing costs (Owens, 1993). Interestingly, the bopyrid,
as well as two other bopyrid species on related prawns, are themselves infected by a castrator, a cryptoniscid isopod, Cabirops orbionei, and the presence of the hyperparasite is correlated with
reduced prevalences of the bopyrids (Owens, 1993). Thus, Owens
(1993) posited that the hyperparasite might make a useful biological control agent in shrimp fisheries with high levels of bopyrids.
9. Modeling diseases for fisheries management
Diseases can have serious effects on commercial fisheries. Yet,
there is a perception among resource managers and fishers that
diseases are not important to the industries or that little can be
done to manage around the disease issues. Few existing fishery
models use disease data (e.g. prevalence, distribution) in fisheries
management. While it is true that management of disease can be
difficult, estimates of disease-induced effects such as mortality or
negative marketability can be incorporated into existing models
to improve stock assessment or management. For example, using
a statistical model, Wahle et al. (2009) used changes in estimates
of settlement and recruitment to model consequences of epizootic
shell disease in their model of lobster recruitment. The lobster
industry off southern New England may be closed or limited because their findings show the effect of the continuing epidemic
of epizootic shell disease on recruitment. Using an individual spatial model, Dolan et al. (in preparation) modeled the effect of host
behavior and the dispersal of PaV1 in juvenile spiny lobsters in the
Florida Keys. Host avoidance was a strong negative influence on
the spread of the virus that largely outweighed water-borne transmission in the dispersal of the virus (Behringer et al., 2006), but the
virus may persist through recurrent colonization of postlarvae.
Kuris and Lafferty (1992) examined the effects of diseases in crustacean fisheries subject to open vs. closed recruitment. In systems
with closed recruitment, such as might be expected in fjords or entrained water masses, intensive fishing pressure to ‘‘fish out’’ a
pathogen could potentially control it.
Other models have examined questions regarding the effects of
pathogens on crustacean populations or on harvested wildlife
stocks. Most models have relied on the classic mass balance approach with susceptible-infectious-recovered (SIR) individuals.
For example, Murray (2009) used SIR models to examine transmission pathways in aquatic pathogens. Different disease features,
such as culling, open vs. local pathways, density-dependent vs.
density-independent pathways, were modeled for several aquatic
pathogens. Choisy and Rohani (2006) examined the effect of harvesting on disease severity and dispersal in harvested wildlife
and livestock. Harvesting markedly increased the prevalence of
disease by altering the density dependence in favor of the pathogen. This is likely the case with nemertean outbreaks in Cancer
and king crabs. Lotz and Soto (2002) and Lotz et al. (2003) used
SIR models to determine the force of transmission (transmission
efficiency) of two important shrimp viruses, WSSV and taura
syndrome virus, respectively. Blower and Roughgarden (1989a,b)
modeled the effects of parasitic castrators in a crustacean
population. Their model indicated that castrators may exert significant population level effects on their hosts.
10. Concluding remarks: diseases in juveniles
The fishing industries for crustaceans tend to focus solely on
adults, and in some cases only on adult males. However, with some
notable exceptions, many disease issues appear to affect juveniles
more than adults. For example, species of Hematodinium have a
predilection for juvenile hosts (Stentiford and Shields, 2005).
Adults can become infected, but they generally have a lower prevalence than juveniles. During epidemics, both juveniles and adults
appear to obtain a high prevalence, but the epidemics likely originate in the juvenile segment of the population. Many viruses,
including PaV1, WSSV, IHHNV and taura syndrome virus, also have
a predilection for juveniles (Shields and Behringer, 2004; Flegel,
2006), and in many cases, previously exposed adults serve as carriers. For Hematodinium and many rhizocephalan infections, juveniles are at more risk of infection because these agents may be
transmitted to the postmolt host. However, other pathogens, such
as several of the shrimp viruses, are spread via cannibalism (Flegel,
1997; Lightner and Redman, 1998; Lightner, 2005), or as in PaV1,
through water-borne transmission (Butler et al., 2008). In these
systems it is not clear why juveniles are more susceptible. Nonetheless, given that many pathogens in fished species affect juvenile
pre-recruits, it is important that we understand basic elements of
etiology, ecology and prevalence and their importance to disease
emergence in our fisheries.
Acknowledgments
I thank Grant Stentiford for organizing the OECD workshop and
the Organisation for Economic Cooperation and Development for
their sponsorship and generous support for travel. Partial funding
for this work was provided by EID Program Grant, NSF OCE BEUF #0723662. This is contribution #3206 from the Virginia Institute of Marine Science.
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