A Review Of The Impact Of Diseases On And

Jeffrey D. Shields

Virginia Institute of Marine Science, The College of William and Mary, Gloucester Point, VA 23062

Abstract

Diseases are a natural component of populations. Background levels of various agents are expected in fished populations, and there is good reason to establish baseline levels of pathogens in exploited fisheries before they become a problem. Such baselines are often difficult to fund or publish; nonetheless, outbreaks are an integral feature of heavily exploited populations. Mortalities or other problems can arise when an outbreak occurs, and all too often the underlying causes of an outbreak are poorly understood. A variety of stressors can lead to outbreaks of disease or contribute to their severity. Pollution, poor water quality, hypoxia, temperature extremes, overexploitation have all been implicated in various outbreaks. This review focuses on epidemic diseases of commercially important and as well as a few examples of other disease issues in that are ecologically important, but not of commercial significance.

Key words: pathogens, crustaceans, mortality, Carcinonemertes, PaV1, , Rhizo- cephala, Paramoeba

Introduction

Pathogens cause direct and indirect losses to were thought to contain presumptive crustacean fisheries. Direct losses are obvi- toxins (Magnien 2001). At the time, the ous, resulting in morbidity or mortality to scare threatened the in- the fished , but they can be difficult dustry of because consum- to assess. However, mortality events can be ers did not purchase fish from the region. widespread and can even damage the socio- economics of impacted fishing communities, Direct losses are most visible to the such as the lobster mortality event in Long because the outcome is usually morbidity or Island Sound during 1999 (Pearce and mortality to the targeted component of the Balcom 2005). Direct losses may also occur population. However, direct losses may also at the market where certain pathogens or occur in the recruiting stock, the unfished syndromes, such as shell disease (Pearce and segment of the population, which is Balcom 2005), cause unappealing lesions on typically include juvenile or female seg- the carapace of lobsters rendering them less ments of the population. Outbreaks with marketable in the live trade. Affected lob- resultant mortality to juveniles have been sters are processed in the lower-valued documented in at least three different canned meat ; hence they represent a fisheries that include the blue crab Callinec- direct loss to the higher grade live trade tes sapidus, the snow crab industry. Such losses can negatively influ- opilio, C. bairdi, and the Caribbean spiny ence public opinion as happened to the fin- lobster (Messick and fish industry during the Pfiesteria scare in Shields 2000, Shields and Behringer 2004, 1997-1998, when presumably “exposed” Shields et al. 2005).

Indirect losses or indirect effects can be dif- Nemertean worms, overfishing, and the ficult to assess, because they are often cryp- collapse of tic and require long-term censuses of popu- lation trends. Basically, infected by The (Cancer magister) one pathogen may become more susceptible supports several targeted fisheries off the to other diseases or to , or they western seaboard of the . The may undergo loss of vigour or castration fishery off central plummeted in with the concomitant loss of egg or sperm the late 1950’s. The once thriving fishery production. Widespread castration and egg declined by 80-90% (Heiman and Carlisle mortality resulting from parasites may 1970) and has never fully recovered. In potentially limit larval populations (Brattey 1976, three studies implicated egg mortality et al. 1985, Wickham 1986), but these as a possible cause of the decline (Fisher effects are difficult to establish at the 1976, Fisher and Wickham 1976). Egg population level. Nonetheless, mathematical clutches from crabs near had models indicate that parasitic castrators can high mortalities, with most clutches sustain- potentially regulate the impacted crustacean ing 10 to 50% egg mortality (Fisher and population (Blower and Roughgarden 1989 Wickham 1976). The clutches of crabs from a,b). Rhizocephalan barnacles, which are Bodega Bay north to had much known castrators, can be very prevalent in less egg mortality. Fouling organisms, fila- some crab populations. The castration that mentous bacteria (e.g., Leucothrix mucor), they inflict upon their hosts can also produce and the fungus Lagenidium sp., were stunting and aberrant behaviors (Shields and originally thought to have caused these Wood 1993). This review discusses mortalities, but the primary agent was later examples of how outbreaks of parasites and shown to be a nemertean worm, Carcino- diseases have impacted several crustacean nemertes errans (Wickham 1979, Shields fisheries. De-tails on outbreaks in cultured and Kuris 1988a). The intensities of worm populations, such as , have been infestations were highly correlated with egg reviewed recently by Lightner (2005), Flegel mortalities; the latter often reached 100% on (2006) and Walk-er and Mohan (2009). individual females from central California Simply defined, an outbreak is the and nearly all ovigerous female crabs were occurrence of a pathogen at greater than infested (Wickham 1979, 1986). Moreover, background levels in a host population. In the high prevalence of the worm and many cases, outbreaks of pathogens in resultant egg mortalities correlated with the crustacean fisheries were un-known or non-recovery of the central California stock unreported from their hosts until the onset of of the crab (Fisher and Wickham 1976, an epizootic. This highlights the fact that Wickham 1979, 1980, 1986). baseline data has not been established on those diseases that affect many crustacean Correlations between worm prevalence, in- species. It also indicates that the causative tensity and egg mortality over time led agents may be newly emergent pathogens, Wickham (1979, 1986) to speculate that or they are simply cryptic and remain three factors contributed to the outbreak of unnoticed by fishers who might otherwise C. errans. The exploitation of the central report sick or dying ani-mals. California crab stock was extraordinarily

high in the late 1950’s, with record landings 1980s. Because egg mortalities were in 1957. The intense fishing pressure and generally lower in more northerly waters, large of landed crabs essentially led and the fishery has only marginally recov- to mass settlement of worms on the few ered, continued surveillance of the worms remaining crabs. The worm population was and their related fouling agents would be so large that every female crab became integral to sound management of that fish- infected, but more importantly, high inten- ery. Unfortunately, review of the published sity infestations caused wide-scale egg literature does not indicate that any such mortality (c.f., population-wide castration), databases are under development. which was further exacerbated by fouling agents. With fewer crabs and increased ex- Outbreaks of nemertean egg predators have ploitation, crab recruitment decreased, with occurred in other fisheries. In the early the positive feedback of higher intensity 1980’s, the red fishery (Parali- worm infestations and additional egg pre- thodes camtschaticus) off southern dation fueling the decline in recruitment. collapsed. The collapse occurred directly Interestingly, in terms of fishing, central after a peak in crab abundance, which co- California is the southern-most part of the occurred with a peak in fishing pressure range for Dungeness crab, and this stock (Blau 1986, see also http://www.nmfs.noaa. may be subject to large variations in gov/fishwatch/species/red_king_crab.htm). recruitment. If this is the case, then the Interestingly, a herpes-like viral infection outbreak of C. errans would represent a new was reported from blue king crabs, Parali- lower ecologically stable state, non-recovery thodes platypus, and it was conjectured to of the stocks continuing into the future, as have contributed to the decline of the red has happened, albeit the fishery has in- king crabs (Sparks and Morado 1986), but creased to about one quarter of its landings infections were not reported from the red compared to its peak periods. king crab host. As with the outbreak in Dungeness crabs, egg mortalities were quite Given the possibility that nemerteans were high in ovigerous red king crabs, reaching contributing to the non-recovery of the an average 90% egg mortality in all of the fishery, worm infestations were included in females within certain fjord or coastal areas a model to examine abundance of Dunge- (Kuris et al. 1991). Egg mortalities were ness crabs in a simulated population from caused by high intensity infestations of northern California. Worm density did not Carcinonemertes regicides and several other cause destabilization of the crab population undescribed species of Carcinonemertes in the model, but worm density contributed (Shields et al. 1989, 1990, Kuris et al. 1991). to depressed population levels (Botsford and The infestations were seasonal and peaked Wickham 1979). Later, an age- and sex- in intensity during the early summer (Kuris structured model of the crab population indi- et al. 1991). Interestingly, egg mortality was cated that worms as a single factor could not only correlated with worm intensity over the destabilize the population model, but in summer months because the worms did not combination with density-dependent re- remain on their hosts at high levels in other cruitment, the parasites could have a desta- months (Shields et al. 1990). Fjord systems bilizing effect (Hobbs and Botsford 1989). may trap or entrain the parasitic larvae into the more enclosed “closed system” of the Infestations of C. errans on the Dungeness fjord. Thus, the loss of eggs negatively af- crab have not been studied since the mid- fects larval recruitment into “closed” fjords

that have high worm abundances. The over time ranged from 38% to 43% of the landings of red king crabs have not since clutch with complete brood loss reported returned to their former levels. among heavily infested lobsters (Aiken et al. 1985, Brattey et al. 1985). It is interesting to speculate that fishing pressure has somehow contributed to the The ecological effects of P. homari on the outbreaks of nemertean worms on Dunge- fisheries for the do not ness and red king crabs. That is, removal of appear to be as severe as those for C. errans one segment of the fished population some- and C. regicides; and it is interesting to how served to amplify infestations on the speculate on why this may be the case. remaining hosts. Fishing pressure was cer- Certain life history characteristics play a role tainly high on these crab hosts, and the in the outbreaks of both C. errans and C. reduction of females, or the loss of males, regicides, and these may not be the case for might have led to amplified parasite in- P. homari. For C. errans, the juveniles ap- tensities on remaining brood stock. How- parently survive for long periods on the ever, fishing activity is not necessarily re- sternum, abdomen, and axillae of their non- quired for this amplification. An outbreak ovigerous hosts (Kuris 1993). Over time, a of C. epialti was reported from an unfished crab may accumulate a heavy infestation. or lightly fished population of Hemigrapsus Worms are also transmitted sexually from oregonensis (Shields and Kuris 1988b). The males to females (Wickham et al. 1984), a fishing pressure on H. oregonensis was light feature which may serve to amplify prior to the outbreak, as they are used as bait infections onto female crabs. For C. regici- by the recreational fishers and little else. des, newly hatched larvae can reinvade the host from which they hatched (i.e., auto- Pseudocarcinonemertes homari is a nemer- infection); therefore, worm populations can tean that infects the American lobster, Ho- reach extremely high levels (>600,000 marus americanus. This worm is usually worms per clutch) over a short summer per- found at low intensities on its host, but high iod (Kuris et al. 1991). Contributing to the intensity infestations have been reported amplification of C. regicides is the fact that (Aiken et al. 1985). Grooming activity by prevalence was highest in fjords, particularly the female reduces the burden of the worms, those with shallow sills, and these fjord but some lobsters are not fastidious groom- systems have limited water exchange with ers and have heavy infestations with result- the open ocean; thus infectious larvae may ant egg mortality. Prevalences of P. homari be retained within the fjord system (Kuris et are usually quite low (Aiken et al. 1983), but al. 1991). Interestingly, egg mortality was one apparent outbreak was reported from only correlated with worm intensity over the lobsters off Grand Manaan Island, Nova summer months namely because the worms Scotia, Canada (Brattey et al. 1985). In that did not remain on their hosts at high levels instance, the prevalence among ovigerous over other months (Shields et al. 1990). For females was 78.7% with a mean intensity of P. homari, perhaps epidemics do not occur 102.4 worms per infected host. Egg mor- because most lobsters preen their clutches, tality due to P. homari correlated with the reducing their infestations, or perhaps intensity of infection (Campbell and Brattey, lobsters do not inhabit areas with restricted 1986). More than 16% of the clutches of water circulation, or mortality occurs over a lobsters from off Grand Manaan Island had shorter time span than when the worms are >50% egg mortality. Mean egg mortality present.

Stressors in Long Island Sound effects of eutrophication (Pearce and Bal- com 2005), and intoxication from anthropo- The American lobster supports a large fish- genic substances (Zulkowsky et al. 2005). ery in Long Island Sound, USA. Prior to Virtually all of these stressors can lead to an 1999, the lobster industry in New York and immunologically compromised (Pat- Connecticut had annual harvests of 10-11 erson and Stewart 1974, DeGuise et al. million pounds, valued at over $40 million 2004), with weakened host defenses, which (Pearce and Balcom 2005). Several diseases can lead to secondary infection. What made have recently impacted the fisheries and these situations especially problematic was management of the American lobster in that the observed decline in lobster health these waters. In 1999, the pathogenic amoe- and viability may have causes that were ba Neoparamoeba pemaquidensis emerged linked to a convergence of more than one in concert with other stressors to decimate factor. Moreover, these diseases are indica- the commercially important population in tors of environmental change and anthropo- western Long Island Sound (Mullen et al. genic degradation, and their emergence may 2004, 2005, Pearce and Balcom 2005). have implications for additional regulation Mortalities also occurred in many other spe- of industrial chemical discharges into cies such as the blue crab ( sapi- marine and estuarine environments. dus), spider crabs (Libinia spp.), rock crab () and the horseshoe crab For example, from 1997 to the present, epi- (Limulus polyphemus). However, the path- zootic shell disease has affected lobsters ogenic amoeba was not linked to mortalities from Naragansett Bay and Block Island in any species other than H. americanus Sound off Rhode Island (Castro and Angell although it must be noted that other host 2000, Castro et al. 2005, Landers 2005, species were not examined. At about the Powell et al. 2005), and from Buzzards Bay same time, lobsters from eastern Long Is- north to Cape Bay off Massachusetts land Sound and Block Island Sound were (Glenn and Pugh 2005). In addition, the in- experiencing an outbreak of epizootic shell cidence of epizootic shell disease has mark- disease (Castro and Angell 2000). In 2002, edly increased, with prevalence ranging lobsters suffering from calcinosis, a physio- from 25-65% of the lobster population, logical response to temperature stress, were particularly in ovigerous females (Castro et also evident within central areas of Long al. 2005, Glenn and Pugh 2005, Howell et Island Sound (Dove et al. 2004); and at al. 2005, Landers 2005). Epizootic shell about the same time, ~50% of the lobsters in disease appears to reduce both the quantity western portions of the sound were and quality of commercial lobster landings diagnosed with blindness (Maniscalco and (Cobb and Castro 2006). Heavily infected Shields 2006, Magel et al. 2009). In animals are not marketable due to gross addition, another emergent pathogen, Vibrio external pathology, which in severe cases fluvialis was implicated in lobster presents as the nearly complete erosion of mortalities off the coast of Maine (Tall et al. the dorsal carapace and claws of the lobster. 2003). The etiology and pathogenicity of the dis- The emergent disease issues in Long Island ease remains to be determined. However, it Sound appeared to be related to environ- is partially non-infectious, caused by envi- mental changes, such as increased bottom ronmental changes, and partly an infectious temperatures during summers, the general one, caused by chitinoclastic bacteria

(Chistoserdov et al. 2005). The dynamics of phenols related to Bisphenol A have been infection are partly known, in that infected found in lobster tissues, some at relatively lobsters can molt successfully, but they can high levels. The alkylphenols (2-t-butyl-4- become rapidly reinfected (Castro and An- (dimethylbenzyl)phenol; 2,4-bis-(dimethyl- gell 2000). The disease syndrome is more benzyl)phenol; 2,6-bis-(t-butyl)-4-(dimeth- abundant in the fall, after animals have ylbenzyl)phenol; and 2,4-bis-(dimethylben- molted. zyl)-6-t-butylphenol) have been used as antioxidants and surfactants in industrial ap- Epizootic disease has not been shown to be plications, and one (2,6-bis-(t-butyl)-4-(di- horizontally transmitted to healthy lobsters methylbenzyl)phenol-MON-0585) has been in laboratory experiments (Chistoserdov et tested as a pesticide because of it is a al. 2005a, b). It is associated with bacterial Juvenile Hormone analog. Bisphenol A is a species other than Vibrio spp., such as known endocrine disruptor and the alkyl- members of the Flavobacteriaceae, but there phenols found in lobsters are known analogs is no apparent relationship with bacteria for Juvenile Hormone that can disrupt molt- other than with chitinoclastic forms (Chisto- ing activity (Biggers and Laufer 2004). serdov et al. 2005a, b). It is histologically Lobsters from Long Island Sound had over different from classical shell disease because 21.0 µg/ml of 2,6-bis-(t-butyl)-4-(dimethyl- of the formation of pseudomembranes under benzyl)phenol in their hemolymph com- the large friable areas of necrotic cuticle pared to <0.5 µg/ml in lobsters from nearby (Smolowitz et al. 2005a, b). Classical shell Vineyard Sound (Biggers and Laufers disease can be transmitted horizontally to 2004). Ovigerous lobsters with epizootic healthy lobsters (Bullis 1989), as observed shell disease also have increased ecdysone in many lobster holding facilities (Getchell levels, >10 times higher than unaffected ovi- 1987, Geddes et al. 2003). gerous animals, and the increased ecdysone may induce abnormal molting activity in Long Island Sound and Buzzards Bay have these animals during a sensitive period high levels of environmental contaminants, (Laufer et al. 2005b). Much remains to be including PCBs, pesticides, metals, and done to identify the stressors involved in this PAHs (e.g., http://www.longislandsound- syndrome, but the relatively narrow confine- study.net/pubs/facts/fact10.pdf, http://www. ment of diseased animals to Rhode Island, buzzardsbay.org/toxicact.htm). Indeed, a eastern Connecticut and southern Massa- major oil spill off Naragansett Bay, Rhode chussetts suggests a pivotal role for a con- Island, killed an estimated 7 million lobsters, taminant. immediately prior to occurrence of epizootic shell disease from that region (North Cape Paramoeba outbreaks in the blue crab oil spill fact sheet, http://www.dem.ri.gov/ news/2006/cape/factsgen.pdf). Paramoeba perniciosa causes “gray crab” disease in the blue crab. The sternums of Further, Biggers and Laufer (2004) and Lau- heavily infected and dead crabs become dis- fer et al. (2005a) found that lobsters with colored with a characteristic gray color epizootic shell disease had higher levels of (Sprague and Beckett 1966, Johnson 1977). alkylphenols than did healthy lobsters, and Outbreaks of P. perniciosa are focal and are that bottom sediments had higher than nor- typically noticed in shedding facilities when mal levels of these compounds in areas a large number of crabs become moribund where diseased lobsters resided. Four alkyl- and die. Around Chesapeake Bay, mortal-

ities occur in shedding facilities from May Because mortalities peak in late spring, to June and in the dredge fishery from Newman and Ward (1973) and Couch October to February (Couch 1983). During (1983) speculated that transmission may epizootics, prevalence ranged from 17 to occur during ecdysis or in post molt when 35% in premolt juvenile crabs at shedding the carapace is soft. facilities on Chincoteague Bay (Sawyer Paramoeba perniciosa infects blue crabs 1969, Sprague et al. 1969). Newman and from Long Island Sound south to the Ward (1973) assessed mortality at 30% per Atlantic coast of (Newman and month from Chincoteague Bay. Prevalence Ward 1973, Johnson 1977) and the ameba is reached >20% during winter dredge samples relatively common in the coastal bays of the from Chincoteague Bay and prevalence Delmarva Peninsula in Delaware, , ranged from 3 to 13% in lower Chesapeake Virginia and south to Georgia (Sprague and Bay (Couch 1983). After peak mortality Beckett 1966, Sawyer 1969, Messick 2002). events, prevalence dropped to 8% in trawled It has not been reported from the Gulf of crabs (Sawyer 1969). Such declines in prev- Mexico (Overstreet 1978, Messick 2002). alence probably reflect host mortality and The disease exhibits a strong summer peak not a seasonal reduction of disease or any in prevalence (Newman and Ward 1973, increase in host resistance. Johnson 1977), but infections can persist in- to winter (Couch 1983). Amebae apparently Heavily infected crabs are sluggish and die overwinter in crabs (Johnson 1977), but a shortly after capture (Johnson 1977). Crabs histological study of overwintering crabs is with light and moderate infections often needed to confirm this. Temperature and exhibit no overt sign of disease. Infected seasonality play important roles in outbreaks premolt crabs die shortly after molting, of amebic infections in other species. presumably because the increased meta- Paramoeba invadens occurs in epizootics in bolic demands of molting, causes additional green sea urchins, Strongylocentrotus droe- stress to the diseased animal. bachiensis, which have been correlated with increased water temperatures (Scheibling The mode of transmission of P. perniciosa and Hennigar 1997, Scheibling et al. 2010), remains unknown. Transmission experi- and P. pemaquidensis (now Neoparamoeba ments with the amoeba have been incon- pemaquidensis) causes disease in cultured clusive (Johnson 1977, Couch 1983). Can- salmonids (Kent et al. 1988, Roubal et al. nibalism may spread the disease when 1989) as well as lobsters (Mullen et al. infected lethargic and moribund crabs are 2004). eaten by conspecifics (Johnson 1977). In- fections, however, have not been experi- The blue crab is the primary host for P. mentally established by feeding infected perniciosa, but the green crab (Carcinus tissues to naïve hosts nor by inoculating maenas), (Cancer borealis), the them with infected hemolymph (Newman lesser blue crab (), and and Ward 1973, Johnson 1977, Couch American lobster have also been reported as 1983). The fact that infected crabs are hosts (Sawyer 1976 as cited in Sawyer and found in high salinity waters, coupled with MacLean 1978, Campbell 1984, Messick the fact that blue crabs are osmoregulators, 2002). The paucity of reports of disease suggest that cannibalism plays little role in from these hosts suggest that they are not transmission; otherwise, infections would be important reservoirs for the ameba Para- sustained at low and moderate salinities. moeba perniciosa infections in blue crabs

appear to have a strong association with Lazaro-Chaves et al. 1996). Sacculina car- seaside coastal bays and lagoons. This type cini can reach a prevalence over 90% in the of “landscape” association with a disease green crab, C. maenas (Stentiford and Feist has been noted for other parasitic diseases of 2005), and local patchiness in prevalence is crustaceans, namely infec- a relatively common phenomenon with this tions in snow crabs and blue crabs (Meyers species (Heath 1971, Stentiford and Feist et al. 1987, Shields 1994, Messick and 2005) as well as other species (Tolley et al. Shields 2000, Shields et al. 2005), and rhizo- 2006, Sloan et al. 2010). Sylon hippolytes cephalan infections in king crabs (Sloan occurs on a variety of shrimp and can reach 1984). high prevalences, but these parasites have received comparatively little attention Insidious effects of rhizocephalans (Bower and Boutillier 1988).

Rhizocephalans are bizarre, highly modified Many rhizocephalan infections stunt the barnacles that cause interesting pathologies growth and molting of their hosts. This is to their hosts, including castration, femin- typically the result of interference with the ization, anecdysis, or a cessation of molting, hormonal regulation of molting in the hosts, stunting, and mortality. They are cryptic causing anecdysis. When the prevalence is and masquerade as the egg mass of their high, a large proportion of the host popu- host. While their effects can be insidious to lation can become stunted, including blue individuals, the range in prevalence of some crabs (C. sapidus) and lithodid crabs species is elevated enough to cause direct (Overstreet 1978, Over-street et al. 1983, effects on the population biology of their Hawkes et al. 1986, Höeg 1995). Stunted hosts. animals do not enter the fishery and they may accumu-late in the fishing grounds as Several species of commercially important “shorts” (Hawkes et al. 1986, Meyers 1990). crustaceans are infected by rhizocephalans. Re-turned “shorts” may artificially increase Briarosaccus callosus infects lithodid king the prevalence of the parasite and serve as crabs in boreal, Antarctic and Arctic waters. foci for transmission to new hosts (Hawkes High prevalences, 50% to 75%, have been et al. 1986, Meyers, 1990). The potential for reported in king crabs in fjords off British ac-cumulation of shorts in a fished Columbia (Sloan et al. 1984) and south- population has led to the suggestion to eastern Alaska (Hawkes et al. 1986). Preva- actively overfish isolated populations, which lence was about 20% in Paralomis granu- would remove the parasites (Hawkes et al. losus in the deepwater canyons around 1986, Kuris and Lafferty 1992, Shukalyuk et South Georgia Island (Watters 1998). Infec- al. 2005), but this practice has not been tions of Sacculina granifera in Portunus implemented. pelagicus can reach prevalences of 40% or more (Phillips and Cannon 1978, Weng Rhizocephalan infections can have other in- 1987, Shields and Wood 1993). Infections sidious, indirect effects on their hosts and of Loxothylacus texanus in the American host populations. Indirect effects of infest- blue crab, C. sapidus, range in prevalence ation at the population level may include from 30 to 70% in lagoons and embayments castration, sterile matings, loss of fecundity, around the (Christmas 1969, homosexual matings, and competition with Ragan and Matherne 1974, Wardle and Tir- phenotypically identical parasites (Shields pak 1991, Alvarez and Calderon 1996, and Wood 1993). The potential for compe-

tition between castrated crabs (phenotyp- hydrodynamic or demographic closed ically crabs, but genetically reproductive systems (Sloan et al. 1984, Kuris and parasites) and uninfected crabs has not been Lafferty 1992). These models indicate that explored and could prove interesting in rhizocephalans can reach a high prevalence terms of the ecology of the parasite as well in their host populations when the model as the behavioral ecology of the host- conditions simulate a closed circulation sys- parasite association. tem with internal recruitment. Therefore, an outbreak of rhizocephalans in a commercial- Several environmental factors facilitate out- ly fished population of crabs or breaks of rhizocephalans. High prevalences could have significant potential to damage of Briarosaccus callosus have been associ- the fishery by altering the population struc- ated with turbid fjords in British Columbia ture of the fished population. and Alaska, particularly those with shallow sills (Sloan et al. 1984, Hawkes et al. 1986). Bitter crab disease by Hematodinium The fjord water either has a long residence time within the system or it becomes en- In the early 1980s, large numbers of Tanner trained allowing the transmissive cyprid crabs () from fjords in larva of the parasite to more readily find and southeastern Alaska developed an unusual infect new hosts than in more open oceanic condition which made them taste bitter and systems. Higher prevalences may co-occur unmarketable. The condition was called bit- with turbid waters, which may reduce the ter crab syndrome or bitter crab disease and ability of crabs to clean their gills, which are was caused by a parasitic , He- the initial sites of infection (Hawkes et al. matodinium sp. (Meyers et al. 1987, 1990). 1986). Shallow lagoons and embayments At that time, estimated losses to the industry with long residence times are also thought to were >$250,000, and these losses were facilitate high prevalences of rhizocephalans centered in the fjords of southeastern Alaska and Hematodinium infections in portunid (Meyers et al. 1987). Infected crabs repre- crabs (Alvarez and Calderon 1995, Shields sented up to a third of the commercial fish- and Overstreet 2007). Confined habitats ery in southeastern Alaska (Meyers et al. may limit the dispersal of the parasite larvae, 1990). Outbreaks of Hematodinium spp. limit their dilution, and lead to high preva- have since been reported from a number of lences (Kuris and Lafferty 1992). Other commercially important crabs and lobsters environmental factors such as temperature, (Stentiford and Shields 2005). seasonality, salinity, depth and turbulence are known to influence the prevalences of Two outbreaks of Hematodinium sp. have rhizocephalans in non-commercial species been documented in snow crabs, C. opilio, (Ritchie and Høeg 1981, Høeg 1995, Høeg from . Taylor and Khan et al. 2006). (1995) initially reported the parasite at low levels during the early 1990’s; however, in A model of the parasitic castrator Hemio- later surveys its prevalence increased signif- niscus balani and its barnacle hosts suggest icantly in the coastal bays (Pestal et al. 2003, that rhizocephalans can regulate their host Shields et al. 2005, 2007). The first populations (Blower and Roughgarden 1989 outbreak in snow crabs occurred in a,b). Other models have examined how Bonavista and Conception Bays in 1999 and castrators can affect their host populations 2000 and mostly affected female and when their ecological connections are within juvenile crabs (Shields et al. 2005). From

2003 through 2005, another epidemic disease occurred in and around the Scottish occurred, but it primarily affected large- fjords (Field et al. 1992, 1998, Stentiford et clawed mature males, with a prevalence of al. 2001). As with snow crabs, up to 35% (Shields et al. 2007). This latter lobsters are apparently in-fected after epidemic was associated with a 1ºC increase molting (Stentiford et al. 2001). In years in bottom temperature, which caused an that there is synchrony in the molting apparent five-fold increase in molting activity of males and females, prevalences activity in larger crabs. Because crabs are show a peak in infections. In years when infected shortly after molting, the large molting is asynchronous between males and number of newly molted, susceptible females, there is a lower ‘plateau’ in animals fueled the epidemic over the three prevalence. year period (Shields et al. 2007). Interestingly, female and juvenile crabs had Outbreaks of Hematodinium are common in similar prevalences to those in the earlier the American blue crab and show a distinct outbreak. There was no outbreak in Bona- autumnal periodicity (Messick and Shields vista Bay during 2003 through 2005 and that 2000). In Virginia and Maryland, periodic bay apparently has a shorter residence time summer and autumn mortalities are cryptic, compared to Conception Bay, which has a but losses may exceed $500,000 per year in shallower sill and a longer residence time nonepidemic years (Stentiford and Shields (DeYoung and Sanderson 1995). 2005). An outbreak in the early 1990’s reached a prevalence of 100% and was pri- In the late 1980’s, an outbreak of Hemat- marily centered on juvenile crabs (Messick odinium sp. was partially documented in the 1994). Similar outbreaks have been (Necora puber) fishery off Brit- reported off the coast of Georgia (USA), tany, (Wilhelm and Mialhe 1996). particularly in relation to drought (Lee and The relatively small fishery suffered a cata- Frischer 2004). Along the Delmarva strophic loss due to the parasite. Infections Peninsula, out-breaks occur in the shallow of the same or a related parasite have coastal bays and lagoons (Messick 1994, occurred in Maia squinado and C. pagurus Shields 1994, Messick and Shields 2000). from Brittany and the English Channel, but Prevalences are generally much lower at the the prevalence in these hosts remains mouth of Chesapeake Bay, which is a more undetermined (Latrouite et al. 1988, Stenti- open physiographic environment. ford et al. 2002). Virtually all outbreaks of Hematodinium are In the late 1980’s and early 1990’s, out- associated with distinct physiographic fea- breaks of Hematodinium were also docu- tures (Stentiford and Shields 2005), such as mented in the Norway lobster fishery off fjords or shallow poorly drained bays and western Scotland (Field et al. 1992). Losses lagoons, but key spatial features of these to the fishery were estimated at £2-4 million outbreaks have not been adequately de- annually (Field et al. 1992). Outbreaks scribed. For example, deep “confined” areas occur seasonally in the fishery and and certain habitat types (mud, sand, gravel, prevalences can reach 70% during the height shell) are associated with infections in snow of the outbreaks, which occur in winter crabs, but the nature of the association re- months (Field et al. 1998, Stentiford et al. mains to be determined (Shields et al. 2005). 2001). As with other Hematodinium The fjords of Alaska, British Columbia and infections, the highest prevalences of the Scotland and the shallow bays of the east

coast of America are ideal for the growth implications for production in these ecolog- and spread of pathogens. These regions pos- ically important host populations. The latter sesses several features that facilitate epi- ay have repercussions to pelagic food webs. demics of Hematodinium and other patho- There is an expansive literature on gens: (1) relatively “closed” host popula- plague, or krebspest and its effects on the tions (i.e., those with little immigration and European crayfish, or noble crayfish (Asta- emigration of juveniles and adults; but not cus astacus). is caused by necessarily closed to larvae), (2) restricted the pathogenic oomycete, Aphanomyces exchange with the open ocean (i.e., narrow astaci. The pathogen fulminated into a wide- channels with shallow sills, deep confined spread pandemic in Europe during the areas, entrained water masses), (3) stressful 1860’s, and it was the first disease outbreak conditions for the crab population (i.e., sum- that was documented in a crustacean. The mer and winter thermal stress, high salinity, pathogen was introduced to northern Italy in seasonal hypoxia, intense fishing pressure), the early 1860’s, probably from contam- and, of course, (4) a pathogen that can inated ballast water in ships sailing from amplify rapidly within a population (Shields ports in the U.S.A. or Canada (Edgerton et 1994). Several of the other parasites dis- al. 2002). From there, the plague rapidly cussed in other sections of this paper have spread northward and was reported within similar associations: e.g., Briarosaccus cal- France in 1875, Germany in 1880, Russia in losus (Sloan et al. 1984), Loxothylacus tex- 1890, Finland in 1893, and then Sweden and anus (Alvarez and Calderon 1995), Saccu- Norway. In Europe, A. astaci decimated na- lina granifera (Shields and Wood 1993), tive stocks of crayfish, particularly Astacus Carcinonemertes regicides (Kuris et al. astacus, which is a delicacy in Northern 1991) as well as infections of Hematodinium Europe. The disease has since been reported (see above). from in 1958, Greece in 1982, the in 1981, and Turkey in Other emerging diseases 1984 as well as in 1987 (Holdich and Reeve 1991, Edgerton et al. 2002). It has This review has focused on a few salient also spread through the introduction of in- diseases of fished crabs and lobsters. How- fected , Pacifastacus leniu- ever, several epidemics of viruses have sculus, from the U.S.A. during attempts to occurred in shrimp farms and these have revive the crayfish industry in Northern spread to become catastrophic pandemics in Europe (Edgerton et al. 2002). Many of the shrimp fisheries. The viruses responsible studies on this pathogen have focused on for these outbreaks (e.g., white spot host immunology or control of the infection. syndrome virus, yellow head virus, Taura For recent reviews of crayfish diseases, see virus, gill associated virus, baculoviruses) Edgerton et al. (2004) and Oidtmann et al. have been well reviewed (Lightner 2005, (2002). Flegel 2006, Walker and Mohan 2009). I will not review them here. There are also Conclusions. documented epi-zootics of oomycete pathogens in freshwater and marine This review has concentrated on significant copepods (Redfield and Vincent 1979, diseases that principally affect commercial Burns 1985) and parasitic ciliates in fisheries of crabs and lobsters. Because of euphausiids (Capriulo et al. 1991, Gomez- the nature of commercial fisheries, i.e., har- Guiterrez et al. 2003) that may have serious vest as opposed to culture, there is the

perception that little can be done to limit the veniles (Shields and Behringer 2004, Flegel effects of pathogens on fished populations. 2006). Juvenile crustaceans molt more Actually, that perception may be false. Few frequently than adults, and those disease if any models use disease data (e.g. – prev- agents that are transmitted via molting alence, distribution) to estimate effects or would have an increased opportunity to in- otherwise manage a fishery. Early modeling fect juvenile hosts during this stressful time. attempts have asked whether diseases could However, not all of these pathogens use be managed in fished populations by “fish- molting as the portal of entry. Some such as ing out” the affected population through WSSV are spread via cannibalism (Lightner increased fishing activity (Kuris and Laf- and Redman 1998, Lighnter 2005) and ferty 1994). The model indicated that in others such as PaV1 and WSSV can be systems with closed recruitment, such as spread via waterborne transmission (Butler might be expected in fjords or entrained et al. 2008). The reason for their increased water masses, such an approach might work. prevalence in juvenile hosts is not clear. Other models have indicated that pathogens, However, what is clear is that the industries such as parasitic castrators, may exert sig- for these crustaceans focus on the adults and nificant population level effects on their not on the juveniles; hence, the agents of hosts, i.e., regulation or declines of their disease are often ignored or not thought to crustacean host populations (Blower and be important to recruitment. Nonetheless, Roughgarden 1989a, b). The development pathogens such as PaV1, Hematodinium sp., of spatial models for systems with disease Aerococcus viridans and Anophryoides has great potential because such models can haemophila may seriously affect their hosts incorporate biological data and integrate it and may play a role in the population over different spatial scales. With such dynamics of host stocks. They will become mod-els, ‘at risk’ populations can be increasingly important pathogens with the identified, especially where the structure advent of increased climatic variability asso- (e.g. sex- or size-bias) of a population makes ciated with global warming (Shields et al. it susceptible to epizootics, or the impact(s) 2007); hence, it is important that we of the disease can be examined in relation to understand basic elements of their life changes in fishing practices. Spatial models history, transmission and pathogenicity prior of disease have not been applied to crusta- to their emergence in larger outbreaks and cean fisheries, but they may be very useful epidemics. in future studies of transmission and population-level effects on both the host and Acknowledgments: the pathogen. I thank the Living Oceans Foundation for In several instances, disease issues are more their generous sponsorship and support of common in juveniles rather than adults. For travel. Partial funding for this work was example, species of Hematodinium have a provided by EID Program Grant, NSF OCE predilection for juvenile hosts (Stentiford BE-UF #0723662. This is contribution and Shields 2005). While adult hosts be- #3103 from the Virginia Institute of Marine come infected, they generally have lower Science. prevalences than juveniles except during epidemics. Other pathogens such as Panu- References lirus argus Virus 1 and White Spot Syn- drome Virus also have a predilection for ju- Aiken, D. E., S. L. Waddy, and L. S. Uhazy. 1985. Aspects of the biology of Pseudocarcinonemertes

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