ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on September 1, 2008
ICES Journal of Marine Science: Journal du Conseil 2008 65(9):1578-1592; doi:10.1093/icesjms/fsn134
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Diseases of the European edible crab (Cancer pagurus): a review
European Community Reference Laboratory for Crustacean Diseases, Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth Laboratory, Weymouth, Dorset DT4 8UB, UK
tel: +44 1305 206600; fax: +44 1305 206601; e-mail: grant.stentiford{at}cefas.co.uk.
Stentiford, G. D. 2008. Diseases of the European edible crab (Cancer pagurus): a review. – ICES Journal of Marine Science, 65: 1578–1592.The edible crab (Cancer pagurus) supports an important fishery in European waters. The fishery is increasing in size and in relative importance as stocks of marine finfish decline. Despite its importance, though, studies on the pathogens and parasites of this crab species are relatively lacking compared with studies of commercially exploited finfish and molluscan hosts. Recent basic surveys of C. pagurus stocks from the English Channel carried out by the Cefas laboratory at Weymouth have identified a new viral infection (C. pagurus bacilliform virus, CpBV) in juvenile crabs, and several new species of protistan parasite (Hematodinium sp., Paramarteilia canceri, and Enterospora canceri) in the adult population. The histopathology and prevalence of each of these pathogens suggests that each can induce host mortality and, further, that specific pathogens are differentially prevalent in juvenile and adult cohorts from similar geographic locations and at different times of the year. In this review, these newly discovered pathogens are placed in context with previously described bacterial, fungal, protistan, and metazoan pathogens of C. pagurus, and the potential for these pathogens to impact on the health of individuals and populations within the English Channel fishery is discussed.
Keywords: biosecurity, Crustacea, disease, fishery, Hematodinium, live transport, population, risk assessment
Received 18 January 2008; accepted 18 July 2008; advance access publication 1 September 2008.
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Introduction |
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In recent years, scientists at the Cefas Weymouth Laboratory have described several pathogens of Cancer pagurus collected from the English Channel fishery. These have included the causative agent of pink crab disease (the dinoflagellate parasite Hematodinium sp.; Stentiford et al., 2002), the type species of a new genus of intranuclear microsporidian infecting the hepatopancreas (Enterospora canceri; Stentiford et al., 2007), a systemic infection caused by a new species of Paramarteilia, a systemic yeast-like pathogen (Stentiford et al., 2003), and most recently, a non-occluded bacilliform virus infecting the hepatopancreas of juvenile crabs [C. pagurus bacilliform virus (CpBV); Bateman and Stentiford, 2008]. Given the importance of the fishery and the relatively replete biological literature concerning the species, it is perhaps surprising that descriptions of this kind are possible. It also highlights how even fairly rudimentary surveys of exploited decapods continue to discover new pathogens with the potential to impact upon the size and structure of their host populations and, further, how little is known about the pathogen fauna of even our most important commercial decapods. With increasing pressure on global, commercial, decapod stocks, and a growing requirement to manage these stocks carefully to ensure sustainability, it is pertinent to consider the effects of disease as a mortality driver in such populations. To this end, improved understanding of the pathogen profile of commercially exploited species is crucial. Here, I provide a review of pathogens and parasites of C. pagurus with commentary on the likelihood for these diseases to impart a detrimental effect on their hosts at an individual and a population level. Further, I provide recommendations for future surveillance work for commercially important decapods along with an overview of ways in which this type of data may be applicable to future stock management.
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Viruses |
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Johnson (1984) noted the distinct lack of descriptions of viral pathogens in the Cancer genus compared with other commercially exploited crab genera. Although the absence of viral pathogens may denote a relative lack of attention afforded to crustacean hosts by pathologists, compared with molluscs and finfish, it may also indicate that viruses are most likely to be observed in juveniles, these rarely forming the basis of disease surveys. Since this observation, two viruses have been described from C. pagurus. Cancer pagurus systemic bunya-like virus (CpSBV) was described by Corbel et al. (2003) from experimental transmission trials of white spot syndrome virus (WSSV) to potential hosts. Abnormal mortalities were recorded in a WSSV negative control group, following which unknown virus-like particles were discovered in the haemolymph. Purified virus isolates were negatively stained and shown to be 60–70 nm enveloped particles with a tail-like structure. Ultrastructural analyses identified viral particles in the cytoplasm of connective tissue cells and also free within the haemolymph. Genetic analysis of purified virus revealed its ssRNA composition, and passage to naïve crab hosts resulted in mortality within 7–12 d, with no gross signs of disease. Corbel et al. (2003) noted that the virus is distinct from the S virus described from crabs (Carcinus maenas, Carcinus mediterraneus, and Liocarcinus depurator) from the French coast. As the C. pagurus for that study were obtained from storage tanks ("viviers"), the prevalence and manifestation of this virus in wild populations is currently unknown. It seems likely, however, that Corbel et al. (2003) are correct in suggesting that CpSBV may play an important role in mortalities occurring in post-capture storage and transportation of C. pagurus. Further work is now required to assess the prevalence of CpSBV in wild populations of edible crab, and to investigate its potential role in post-capture mortality. Moreover, cross-species transmission trials may elucidate whether the pathogen can transfer to other commercially exploited decapods held within the same storage systems as infected C. pagurus.
Recently, my laboratory has described a second virus of C. pagurus. CpBV is a non-occluded, bacilliform virus infecting the hepatopancreatocytes of crabs collected along the shores of the English Channel (Bateman and Stentiford, 2008). The virus was only observed in juvenile C. pagurus with carapace widths (CWs) ranging between 20 and 70 mm. Apparent prevalence was estimated at 5%. Although viral infection was not observed in crabs above the minimum landing size (MLS) of 140 mm CW, infection has since been observed in one crab with a CW above the MLS, sampled as part of a separate study on effects of post-capture storage on C. pagurus (unpublished personal data; Figure 1). Infected crabs exhibit no external symptoms, but histology of the hepatopancreas reveals hypertrophic nuclei with eosinophilic nucleoplasm and marginalized chromatin. Transmission electron microscopy allows visualization of rod-shaped virions within these enlarged nuclei. Virions contain an electron-dense nucleocapsid possessing relatively electron-lucent ends. The nucleocapsid is surrounded by a trilaminar envelope, expanded at one end to form a lateral protuberance containing a fine tail-like structure emerging from the proximal end of the nucleocapsid. Virions are 
210 nm long with a diameter of 60 nm. The apparently greater prevalence of infection in juvenile C. pagurus highlights a requirement to consider age and size when carrying out disease surveys in wild crustacean hosts. In particular, it demonstrates how pathogens specifically present in juvenile life stages may act as silent mortality drivers within a fishery for commercially important species. Further work is now required to assess the relative pathogenicity of the virus and to assess its prevalence in juveniles throughout the season and across the geographic range of C. pagurus (Bateman and Stentiford, 2008).
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Bacteria |
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Bacterial diseases of Cancer species (including C. pagurus) can be separated into those associated with the carapace and those that appear as either specific infections of particular organ systems, as for Rickettsia-like and Chlamydia-like organisms, or as systemic infections.
Diseases of the carapace of C. pagurus have been reported repeatedly from across its natural range. The first published report, by Pearson (1908), noted how "granny crabs" (old C. pagurus) displaying signs of shell necrosis had a bitter-tasting flesh, were unsightly, and were often rejected by the fishery. McIntosh (1963) carried out microbiological analyses of lesions in affected crabs. A later review by Getchell (1989) reported bacteria belonging to the genera Vibrio, Aeromonas, Pseudomonas, Alteromonas, Flavobacterium, Spirillum, Moraxella, Pasteurella, and Photobacterium associated with shell-disease lesions. Ayres and Edwards (1982) recorded the condition as "black spot" owing to the black lesions presenting on the exoskeleton of affected crabs. They noted that the prevalence of the condition was greatest in populations of older crabs, whose moult frequency is relatively low, i.e. typically in new or developing fisheries where fishing effort has yet to reduce the average size of animals within the population. Later studies by Austin and Alderman (1987) co-associated the bacterial shell diseases of crustaceans under the heading of "burn-spot disease", and as being caused by chitinolytic, gram-negative bacteria predominantly of the genera Pseudomonas and Vibrio. In a survey of crabs from the west coast of Scotland, Comely and Ansell (1989) recorded shell disease in almost 100% of C. pagurus, significantly higher than in other crab species analysed in the same survey, with no apparent relationship with depth of capture or season. A considerable body of work was subsequently carried out on C. pagurus collected from the Welsh coastline starting in the late 1990s. Vogan et al. (1999) reported an overall prevalence of >50% in crabs from the South Wales fishery, male crabs showing a higher prevalence and intensity of infection. A propensity for lesions to be concentrated towards the posterior dorsal surface of the carapace was interpreted in light of the tendency for C. pagurus to "back burrow", with resultant surface shell abrasions leading to infection, particularly in areas where sediments contained bacteria with higher chitinase activity (Vogan and Rowley, 2002a). However, studies of other species have also implicated mechanical or chemical injury as a catalyst for the condition (Cipriani et al., 1980; Dyrynda, 1998).
Further studies by Vogan et al. (2001) have shown that crabs with more severe levels of shell disease also display histopathological alterations to several organ and tissue systems, including systemic melanized haemocyte nodules, with a significant proportion of haemolymph-derived isolated bacteria exhibiting chitinolytic activity. Despite this bacteraemia and a decrease in haemolymph protein concomitant with symptoms of shell-disease syndrome, no dramatic alteration in various immune parameters were observed (Vogan and Rowley, 2002b). Further characterization of the bacterial species responsible for shell disease and apparently associated internal effects of the disease was carried out by Vogan et al. (2002). Here, injection of particular isolates led to systemic infections, some of which led to rapid mortality of host animals. Further studies by Costa-Ramos and Rowley (2004) demonstrated that injection of a purified lipopolysaccharide of Pseudoalteromonas atlantica, isolated from shell-diseased crabs, caused rapid death in naïve hosts. However, how this mode of infection (and action) relates to shell-disease syndrome in naturally infected C. pagurus in the field remains unclear. Powell and Rowley (2005) noted an apparent dissociation between the prevalence of shell disease and organic load (related to sewage pollution) in C. pagurus. This study perhaps reinforced the earlier interpretation by Ayres and Edwards (1982) that the prevalence and severity of the condition depends on moult frequency, and hence age, of the crab population. Whether shell-disease syndrome provides a direct barometer of growth rate and extent of exploitation within a particular population remains to be shown.
Although haemolymph bacteraemia appears to be a pathological outcome of shell-disease syndrome, systemic bacterial infections per se have not been reported from C. pagurus. In the co-generic Cancer irroratus, Vibrio spp. infections have been reported in wild crabs and caused high mortalities during experimental infections. Interestingly, in the same study, this Cancer species was also shown to be susceptible to the lobster disease Gaffkaemia when inoculated with Aerococcus viridans var. homari (Newman and Feng, 1981). Although no studies have demonstrated similar susceptibility to A. viridans in C. pagurus, commercial practices that hold this crab species with lobsters (Homarus spp.) may identify this as a high-risk activity.
Obligate intracellular bacteria of the order Chlamydiales have been reported from the co-generic Cancer species Cancer magister, C. irroratus, and C. borealis. Infection in C. magister is systemic with a pathogen affinity for connective tissues. Between 6 and 13% of wild-caught C. magister were infected, with prevalence highest during winter. The pathogen is thought to be responsible for a period of high-mortality experienced in crab pots and commercial holding facilities in embayments in Washington in 1979 (Sparks et al., 1985). In C. irroratus and C. borealis, infection was observed in laboratory-maintained crabs, where it elicited high mortality. Infection of the haemopoietic tissues, blood cells, and connective tissues suggests a similar pathogenesis to that observed in C. magister (Leibovitz, 1988). No similar pathogens have been reported from C. pagurus.
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Fungi |
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Fungal infections (Phycomycetes, Ascomycetes, and Fungi Imperfecti) have been implicated in catastrophic epizootics and mortality events in decapod crustaceans (Unestam, 1973). However, despite the existence of a relatively extensive, crustacean-related literature concerning this pathogen group, only one fungal pathogen has been described from C. pagurus. The yeast-like pathogen was discovered in C. pagurus (and Necora puber) from the English Channel. All crabs were co-infected with the dinoflagellate parasite Hematodinium (Stentiford et al., 2003). Infected crabs displayed large numbers of haemocytic encapsulations that surrounded viable (budding) yeast-like cells. Although the taxonomic position of the yeast-like pathogen was not defined, previous studies identified a number of yeasts that infect crustaceans, including Metschnikowia, Cryptococcus, Candida, Pichia, Endomyces, and Debaryomyces (Metschnikoff, 1884; Pixell-Goodrich, 1928; Spencer et al., 1964; Unestam, 1973; Codreanu and Codreanu-Balcescu, 1981; Hryniewiecka-Szyfter et al., 1994; Hsu and Liu, 1994; Hryniewiecka-Szyfter and Babula 1996, 1997a, b; Lu et al., 1998). Many yeasts have also been isolated from fresh, raw, seafood products. Of these, the proteolytic Candida lipolytica, Trichosporon pullulans, and Trichosporon cutaneum have been isolated post-mortem from C. pagurus (Kobatake et al., 1992). Stentiford et al. (2003) suggested that these species are perhaps native inhabitants of the tissues and haemolymph of C. pagurus. Under conditions of host immunosuppression, such as that caused by primary disease or by environmental factors, their opportunistic proliferation leads to disease in their hosts.
Epizootic larval mycosis of the co-generic C. magister attributable to a Lagenidium-like pathogen has been reported from experimental culture systems in the USA (Armstrong et al., 1976). Infection was apparently acquired within 48 h of hatching and implicated more than 40% of the larval stock within 7 days. Owing to the low aquaculture potential for C. pagurus, and despite the use of larval surveys as indicators for estimates of the stock size of adult crabs in European waters, there are no published studies on larval pathogens of this species. Moreover, reports on egg mortalities in wild populations of C. magister caused by a Lagenidium-like pathogen (Fisher and Wickham, 1975) demonstrate the potential for disease agents to induce "silent" mortalities in crustacean fisheries by reducing year-class recruitment, rather than by causing direct mortality to host animals.
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Protistans |
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Although viral, bacterial, and fungal pathogens appear to exert the most significant constraints on the growth and survival of crustaceans under culture conditions, the available literature appears to indicate that it is the protistan parasites that elicit the greatest detrimental effect on wild crustacean populations. Hence, it is these diseases that may additionally negate the marketability of commercial products harvested from these hosts. Whether this is a true reflection of the situation in host populations, or whether it is an artefact of how pathologists sample diseased animals, is debatable. As such, "silent mortalities" attributable to viral (or other) pathogens may occur in field scenarios, but owing to their rapid onset or their low prevalence or absence in the fished (adult) population, they are not detected in routine surveys or during commercial fishing seasons. In this respect, the apparent absence of viral diseases in nephropid lobsters and in several commercially important crab genera, including until recently, Cancer, may reflect insufficient field-sampling design rather than some refractory nature of these groups to viral pathogens. Nevertheless, several protistan parasites known to cause direct and indirect mortality, and as such having a detrimental effect on commercial exploitation, have been described from C. pagurus and its co-generics.
Microsporidians
Many microsporidian parasites, several of which are responsible for economic and ecological impacts in commercial hosts, have been described as infecting decapod crustaceans (see reviews by Sprague and Couch, 1971; Sprague, 1977; Couch, 1983). As for microsporidian parasites of other host groups, those infecting crustaceans are obligate, intracellular parasites that infect cells by discharging their infective sporoplasm through a spore-derived polar filament into the cytoplasm of the host cell. Parasite development proceeds via merogony and sporogony wholly within the confines of the host cell (Lom and Dyková, 1992). The first microsporidian described from C. pagurus was Ameson atlanticum, found infecting the musculature of crabs captured off northern France (Vivarès and Azevedo, 1988). Merogony advanced from a single-celled meront to a bi- and tetra-nucleate stage, all stages in direct contact with the muscle-cell cytoplasm. Tetra-nucleate sporont stages apparently divided into four sporoblasts that contained precursors of the spore apparatus (polar filament, anchoring disc, and polaroplast), these maturing to mature spores that possessed distinctive hair-like projections and the presence of 11–12 turns of the polar filament. The parasite caused whitening and destruction of up to 80% of the host musculature, but no host reaction was observed (Vivarès and Azevedo, 1988). Ameson atlanticum has not been observed in any of the surveys carried out by the Cefas Weymouth laboratory, and in the absence of prevalence data in the study of Vivarès and Azevedo (1988), it may be assumed that it is a relatively infrequent pathogen of C. pagurus, at least in British waters.
Recently, the Cefas laboratory described a second microsporidian infecting C. pagurus. The pathogen is the type species of a new genus (Enterospora) within the family Enterocytozoonidae. The family is distinctive within the Microsporidia in that it contains two genera with unique developmental features, one of these genera (Nucleospora) residing solely within the nucleus of host cells. The parasite from C. pagurus, named E. canceri (Stentiford et al., 2007), also develops within the nucleus of host cells and, as such, it is the first example of an intranuclear microsporidian pathogen in invertebrates. Nuclei of host hepatopancreatocytes infected with E. canceri are hypertrophic, and contain an eosinophilic and granular nucleoplasm that displaces host chromatin to the periphery of the nucleus. Presumed auto-infection of adjacent hepatopancreas cells can lead to severe infections and eventual tubular degeneration. Transmission electron microscopy of infected cells reveals a development sequence characteristic of the family Enterocytozoonidae. Uninucleate meronts progress to multinucleate plasmodia containing precursors of the spore-extrusion apparatus (e.g. polar filament, anchoring disc) and eventually to mature spores that are in direct contact with the host-cell nucleoplasm. As seen in the fish-infecting genus Nucleospora, the complete developmental cycle of E. canceri takes place within the nucleus of host cells, with eventual liberation from the nucleus into the cytoplasm coinciding with nuclear degeneration (Figure 2). Transmission of the parasite is assumed to occur via passage in the faeces, though this has not been investigated or proved. Interestingly, a second member of the genus Enterospora has also been discovered infecting the hepatopancreas of the European hermit crab Eupagurus bernhardus (Stentiford and Bateman, 2007). As that discovery occurred as part of routine surveys, it is possible that intranuclear microsporidians may be relatively common in crustaceans. Molecular taxonomy of other members of the Enterocytozoonidae (the genera Nucleospora and Enterocytozoon) has placed this family as basal members within the Microsporidia (Lom and Nilsen, 2003). Moreover, molecular-phylogenetic studies of a microsporidian infecting crustacean sea lice and another from daphnids have shown that, although these forms are not intranuclear, they nevertheless closely align with existing members of the family Enterocytozoonidae (Refardt et al., 2002; Freeman et al., 2003). Because the genus Enterocytozoon is an important human pathogen in immunosuppressed patients with acquired immune deficiency syndrome (AIDS) (Desportes et al., 1985), it is important first to understand how humans obtain these (presumably zoonotic) infections, and second to investigate the significance of mammalian (Enterocytozoon), fish (Nucleospora), and invertebrate (Enterospora) pathogens coexisting within the family Enterocytozoonidae. Further work is required to elucidate the molecular-taxonomic features of Enterospora relative to these genera and to other hepatopancreatic microsporidians in crustaceans.
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Only one other microsporidian parasite has been described from the genus Cancer. Nadelspora canceri infects the skeletal musculature of C. magister from the Pacific coast of the USA. The parasite is a member of the family Nadelsporidae and is characterized by the presence of needle-shaped spores that impart opacity to infected muscle fibres, leading to mortality in heavily infected host crabs (Olson et al., 1994). Field surveys have shown that the prevalence of the parasite can reach 40% and is highest in male crabs at least 2 years old (Childers et al., 1996). Laboratory trials have demonstrated transmission of the lethal parasite via ingestion of infected tissues by naïve crabs (Reno et al., 1994).
Systemic dinoflagellates
Dinoflagellates of the genus Hematodinium and Hematodinium-like dinoflagellates have been described from a wide range of crustacean hosts (Stentiford and Shields, 2005). A Hematodinium-like dinoflagellate, hereafter referred to as Hematodinium, was first described in C. pagurus by Latrouite et al. (1988), following surveys in the English Channel, the Irish Sea, along the west coast of Scotland, and in the Bay of Biscay off France. Further studies were carried out at the Cefas laboratory following reports by fishers of mortalities and poor condition of C. pagurus captured from the Cornish and Guernsey fisheries during 2000 and 2001. Anecdotal information provided by fishers indicated unusually poor survival during transportation and holding, with dead and morbid crabs even present in fishing traps left on the seabed for more than one day. Affected crabs were listless and emitted creamy or pink haemolymph from breaches in the carapace, which was the basis of the term "pink crab disease" coined by fishers. Analysis of affected crabs led to the re-discovery of Hematodinium in the Cornish and Guernsey fishery (Stentiford et al., 2002). As is widely reported for infections with Hematodinium, the haemolymph of infected crabs contained masses of uni-, bi-, and multicellular parasites that penetrated tissues via haemal sinuses and haemolymph vessels. Normal connective-tissue cells and reserve-inclusion cells were displaced or absent in crabs with advanced infections, and hepatopancreatic and muscular tissues displayed changes consistent with infection in other species. Muscular degeneration, particularly in the chelipeds, is probably related to the loss of integrity following the cooking of infected crabs (Stentiford et al., 2002). A later study by the Cefas laboratory revealed the presence of a yeast-like pathogen in Hematodinium-infected C. pagurus. Interestingly, the cellular immune response towards this pathogen was pronounced, whereas the response to Hematodinium was minimal or absent, suggesting a lack of "visibility" of Hematodinium to the immune system of C. pagurus (Stentiford et al., 2003).
Preliminary histological surveys on the prevalence of Hematodinium (and other pathogens) in the Weymouth C. pagurus fishery in the English Channel during 2003 indicated a seasonal peak of infection in spring/early summer (May/June), with apparent infection prevalence of the total catch of 45% and a prevalence in female crabs of almost 60% (unpublished data). Surveys at other locations in the English Channel and elsewhere within the European fishery have not been reported to date (Figure 3). The global presence of Hematodinium within commercially exploited marine decapods and its direct and indirect effects on mortality and marketability of affected hosts classify it as perhaps the most significant pathogen affecting the UK’s commercial crustacean stocks. Dedicated research and monitoring have been recommended to assess the risk of the infection spreading via commercial activities and to ascertain the apparent mode of transmission to naïve target and non-target hosts (Stentiford and Shields, 2005). In this context, taxonomic diversity among members of the genus Hematodinium and its role in pathogen virulence and transmission is still an issue that remains relatively unresolved. Further genomic assessment of commercially significant isolates would assist with accurate field diagnostics for these pathogens, and would provide information on the likelihood of past and future translocations of this disease via the international trade in live crustaceans (Stentiford and Shields, 2005; Small et al., 2007).
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Although not causing disease per se in C. pagurus, predation on mussels contaminated with diarrhetic shellfish poison (DSP) can lead to accumulation of DSP within the tissues (Castberg et al., 2004). In some instances, DSP contamination of shore-collected C. pagurus has led to episodes of human intoxication and sickness, so demonstrating the potential for these toxins to accumulate within the food chain (Torgersen et al., 2005). To date, the effect of toxin exposure on the organs and tissues of these crabs has not been reported.
Paramyxeans
During periodic surveys of the English Channel C. pagurus fishery, the Cefas laboratory discovered a new species of parasite within the genus Paramarteilia (family Marteiliidae). Paramarteilia sp. is the second species to be described, following the type Paramarteilia orchestiae from the amphipod Orchestia gammarellus (Ginsburger-Vogel and Desportes, 1979). Parasites within the genus, and indeed those of the sister genera Marteilia and Paramyxa, are characterized by the formation of "propagules" comprising several cells enclosed within each other that arise via endogenous budding of the original stem cell (Desportes and Perkins, 1989). The cells also contain haplosporosome-like structures similar to those in haplosporidians, but the cell-within-cell arrangement distinguishes these three genera from this group (Desportes and Perkins, 1989). Infected crabs appeared lethargic and unresponsive, but did not contain discoloured haemolymph typical of infections with Hematodinium. The histology of the infected crabs revealed a systemic invasion of most organs and tissues, and a pronounced encapsulation response. Careful observation of the congested haemal sinuses within the hepatopancreas revealed small, apparently multicellular bodies. In heavily infected crabs, these were also present within the epithelial cells of the hepatopancreas, gut, epidermis and gill, the muscle fibres of the heart and body, the pericardium of the heart, the nerves, the tegmental glands, and, significantly, within viable oocytes and even spermatocysts (Figure 4). Transmission electron microscopy of parasite stages revealed the typical cell-within-cell formations and elongated haplosporosome-like structures described for P. orchestiae. Preliminary surveys suggested a relatively low prevalence (<4%) of Paramarteilia sp. in the English Channel fishery, although no surveys have been carried out elsewhere within the host range. Infection of viable and mature oocytes intriguingly proposes a vertical transmission route for Paramarteilia sp., though this cannot be confirmed from field surveys. The severe pathological outcome when coupled with the systemic nature of severe Paramarteilia sp. infections suggests that the parasite may be responsible for at least some element of mortality of this host in the wild. Because of the similarities between Paramarteilia sp. and its sister genus Marteilia (an OIE-listed notifiable pathogen of molluscs), further surveys, encompassing a wider geographic range and including juvenile C. pagurus, are required.
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Systemic ciliates
The first description of a ciliate infection of crustaceans was made by Cattaneo (1888). Since then, ciliate infections have been described in a range of crustacean hosts (see Morado and Small, 1995, for a review). Usually, ciliate infections are associated with stressful conditions and, as such, they have been considered as opportunistic pathogens that are, in fact, rarely observed in samples collected directly from the field (Meyers, 1990; Small et al., 2005). It is under such conditions that a ciliate parasite was found infecting C. pagurus. A high prevalence of an Anophrys sp. (= Mesanophrys, Paranophrys) ciliate was found in crabs held in post-capture "vivier" tanks in France, with the infection leading to elevated mortalities in the captive stock (Bang et al., 1972). It caused opacity of the haemolymph as a consequence of the large numbers of ciliates, and death ensued within a few days of crabs entering the holding facilities. The infection could be passaged by the injection of infected haemolymph into naïve crabs. Other ciliate infections have been described in co-generic species within the genus Cancer. Armstrong et al. (1981) and Sparks et al. (1982) described Paranophrys (= Mesanophrys) infections of C. magister collected from holding tanks. Later studies by Morado et al. (1999) recorded dead and dying wild populations of C. magister from the coast of Washington state. Analysis of affected specimens revealed infections by the ciliate Mesanophrys pugettensis (Morado and Small, 1994) and a particular association with the moult status of affected hosts. This report is the first instance of a ciliate pathogen implicated in mass mortalities under natural conditions and demonstrates how ciliates may act as mortality drivers, particularly in association with stressful life-history events such as moulting. Despite these reports of ciliate infection in wild C. magister and in commercially held C. pagurus, surveys of wild C. pagurus carried out by the Cefas Weymouth laboratory have not observed ciliates in crabs collected directly from the wild.
Systemic amoebae
Amoebic infections have not been widely reported as infectious agents of crustaceans. The most significant, Paramoeba perniciosa has been implicated in the so-called "grey crab disease" of blue crabs (Callinectes sapidus), as a consequence of the clinical signs of infection—grey colouration of infected haemolymph that pervades the ventral carapace (Johnson, 1977). The same parasite has also been discovered infecting lobsters (Homarus americanus) and rock crabs (C. irroratus) on the Atlantic coast of the US (Sawyer, 1976). The parasite proliferates to massive numbers within the haemolymph, and causes tissue and organ damage that leads to lethargy and eventual death (Johnson, 1977). Shields (2003) suggested that efforts are required to develop molecular diagnostic tools for this pathogen, particularly to identify infected animals entering blue-crab shedding facilities, but also potentially to discriminate the pathogens described from the genera Callinectes, Homarus, and Cancer. Paramoebiasis has not been discovered in surveys of C. pagurus carried out in UK waters by the Cefas laboratory, and no reports of this parasite in other European stocks of C. pagurus have been published yet.
Apicomplexans
A single rather convoluted reference to a gregarine infection in C. pagurus was highlighted by Sprague and Couch (1971). The parasite, nominally assigned as Cephaloidophora praemorsa by Kamm (1922), was observed in the gut and in "vesicles adhering to the ovary" of C. pagurus by Redi in 1684; referred to in Kamm (1922) and Sprague and Couch (1971). The original reference suggested an organism that "might have been a gregarine". No more examples of gregarine infections have been reported from C. pagurus or other Cancer species, although systematic surveys have not been carried out.
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Metazoans |
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In the context of this review, metazoan parasites refer to multicellular organisms that reside within or between tissues and organs of C. pagurus and which may or may not cause a negative impact on the health of the host. Relative to the studies reported above for viral, bacterial, fungal, and protistan pathogens, most studies on metazoan infections were carried out between the late 19th and mid-20th centuries. Few recent disease surveys of this or other host species appear systematically to include metazoan parasites, so it is difficult to ascertain their prevalence in commercial stocks or to assess the role that they play in defining the health of C. pagurus populations.
Trematodes
As described in several other marine crustaceans, encysted, metacercarial stages of digenetic trematodes have been discovered in the tissues of C. pagurus. Microphallus similis, a parasite generally found infecting tissues of the shore crab C. maenas, has been found at very low prevalence in C. pagurus from British waters (Crothers, 1966). In this case, C. maenas and C. pagurus fulfil the role of second intermediate host, with intertidal, prosobranch molluscs such as Littorina saxatilis acting as primary hosts by producing motile cercarial stages that penetrate the gills of the host crab and thereafter encyst as metacercaria within various organs and tissues (Stunkard, 1957; James, 1967). The encysted metacercaria of a second species (Cercaria esmasculans), also primarily hosted within intertidal littorinid molluscs, has also been found in C. pagurus collected from the UK (James, 1967). A third example is Spelotrema excellens (= feriatum), another common parasite of C. maenas that occasionally infects C. pagurus (Hansson, 1998). Previous studies on rock crabs (C. irroratus) from Canada have demonstrated that encysted microphallid digeneans are the most commonly encountered metazoan parasites, but that their prevalence in the host species is considerably lower than in C. maenas because of the littoral habit of the latter. In these zones, cercaria-shedding, littorinid molluscs are more common (Brattey et al., 1985). Dungeness crabs (C. magister) also play host to an unidentified digenean parasite that in some cases has caused severe disruption to nervous tissues and led to host lethargy (Sparks and Hibbits, 1981). The absence of adult C. pagurus from the European littoral zone probably precludes a high prevalence of encysted digeneans in adult populations. As described above, the differential prevalence of these and other pathogens in juvenile C. pagurus may be demonstrated by better design of disease surveys to include crabs of different ages and size.
Cestodes
There are few reports of larval cestode infections in the genus Cancer. McIntosh (1875, cited by Ingle, 1996) provided an initial record of a Tetrarhynchus sp. in C. pagurus. A second record, Eutetrarhynchus ruficollis, the type species of the genus with a definitive host in elasmobranch fish of the genera Mustelus and Squalus, has been reported from C. pagurus in the Atlantic and Mediterranean (Hansson, 1998). No prevalence data or information on pathological outcome is available, however, though reports of cestode infections in other crustacean hosts suggest that prevalence may reach 90%, with large numbers of parasites per individual. Despite this, even heavily parasitized hosts may display no obvious symptoms of infection (Sindermann, 1990).
Acanthocephalans, nemerteans, and turbellarians
As for digeneans and cestodes, reports of the infection of C. pagurus and its co-generics by other helminth parasite groups are rare. McIntosh (1875, cited in Ingle, 1996) reported the acanthocephalan Echinorhynchus sp. in C. pagurus, whereas other acanthocephalans of the genus Polymorphus have been observed in up to 37% of C. irroratus from Canadian waters (Stunkard, 1957; Schmidt and MacLean, 1978; Brattey et al., 1985). A recent review of nemertean predators has suggested that most prey on live invertebrates and have the potential to impact upon the population size and structure of their prey organism (Thiel and Kruse, 2004). Nemertean infestations have not been reported from C. pagurus, but Carcinonemertes errans infects egg masses of Dungeness crab C. magister: infected egg masses contained up to 100 000 worms with an estimated egg mortality of 55% in Californian C. magister populations over a five-year period (Wickham, 1979, 1980, 1986). Another species, Carcinonemertes epialti, has a high infection prevalence of Cancer anthonyi in southern California, causing an egg mortality of up to 30% (Shields, 1990; Shields et al., 1993).
Turbellarians have been reported rarely from crustaceans, but one species, Fecampia erythrocephala, has been described as infecting C. maenas and C. pagurus from around the UK and in the Mediterranean (Brun, 1967; Kuris et al., 2002, 2005). Kuris and co-authors consider this species to be a parasitoid, because the completion of its life cycle depends on the death of its host. Cocoons of the parasite are fixed to the underside of rocks in the littoral zone and, at such sites, infection prevalence, decreasing sharply with size, reached 11% in crabs <11 mm. Kuris et al. (2002) suggested that this parasitoid is a major mortality driver of juvenile C. maenas and C. pagurus that inhabit these zones. In juvenile C. pagurus collected from the English Channel, crabs infected with F. erythrocephala are significantly lighter in colour than their uninfected counterparts, and on dissection are found to contain a single, large turbellarian that appears to replace the major organ masses contained within the cephalothorax (Figure 5).
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Crustaceans
Crustacean pathogens of C. pagurus and its co-generics have been reported rarely. The rhizocephalans Sacculina triangularis (Anderson, 1862) and Sacculina carcini (Malm, 1881) were found to infect C. pagurus from the Firth of Forth in Scotland, and in the North Sea, respectively. Renouf (1932) reported infection by a third species, S. carcini, in Irish populations of C. pagurus. Both these infections of C. pagurus were later reassigned as Sacculina inflata by Boschma (1931, 1933, 1955), who found further examples of infection in the Firth of Forth and in the English Channel. Stephenson (1933) also described S. inflata infecting Danish populations of C. pagurus. Boschma (1955) notes that most species of the Sacculinidae are inhabitants of shallow water and that S. inflata has not been recorded at depths >50 m. This life-history feature may explain the relative absence of infections in adult crabs sampled during our surveys of the English Channel, and highlights once again a requirement to survey juveniles in addition to crabs above MLS (Figure 6).
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Other crustacean parasites have been described infecting members of the genus Cancer. The copepod Choniosphaera cancrorum infects the egg clutch of both C. borealis and C. irroratus (Connolly, 1929, in Sindermann, 1990). Copepods of this genus extract the yolk from eggs and mimic the colour and shape of eggs held externally on the host abdomen (Gotto, 2004). No similar infections have been reported for C. pagurus.
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Carapace-fouling organisms |
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Many organisms have been observed fouling the exoskeleton of C. pagurus. In this review, these fouling organisms are only discussed briefly, because most of them are more likely indicators of host moult status rather than sentinels for underlying health status. The first report of carapace fouling was by Holt (1890), who reported the anemone Actinia mesembryanthemum (= equina) as "not uncommon" on the carapace of C. pagurus and stressed that, because young crabs and anemones are common in the diet of cod (Gadus morhua), it is unlikely that the anemone affords the crab any protection from predation.
Several species of spirorbid polychaete (Janua pagenstecheri, Spirorbis rupestris, and S. tridentatus) have also been described as inhabiting the external carapace of C. pagurus (Knight-Jones and Knight-Jones, 1977). Janua pagenstecheri is the most common spirorbid globally, and is especially abundant in British waters. Its distribution extends from the littoral zone to a depth of at least 120 m, and its larvae appear preferentially to colonize dark or red subtrata, perhaps explaining their propensity to inhabit the carapace of C. pagurus rather than marine alga or inanimate surfaces (Knight-Jones and Knight-Jones, 1977; Figure 7). Similarly, several cirripede crustacean species (barnacles) inhabit the carapace of intermoult C. pagurus. These include Balanus balanus, Balanus crenatus, Chelonibia patula, Chirona hameri, Elminius modestus, and Verruca stroemia (Richard, 1899; Heath, 1976). Studies of B. crenatus and E. modestus inhabiting the carapace of either C. maenas or C. pagurus have shown that barnacles principally inhabit grooves or depressions in the carapace and are less common on raised or smooth regions. The infestation rate of barnacles on C. pagurus (25%) is lower than on C. maenas (46%), possibly reflecting the smoother carapace of C. pagurus (Heath, 1976).
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Descriptions of molluscs on the carapace of C. pagurus include the saddle oyster Anomia sp. and the common whelk Buccinum undatum (Renouf, 1932, cited in Ingle, 1996). Bryozoan infestations are also common, particularly in larger crabs with a presumably longer intermoult duration. Species such as Scruparia chelata have been implicated (Renouf, 1932, in Ingle, 1996). As part of survey work carried out by the Cefas Weymouth laboratory, C. pagurus are occasionally captured showing pronounced fouling by spirorbid polychaetes, barnacles, and bryzoans, alongside advanced shell-disease lesions (Figure 6). Although not reported for C. pagurus, the presence of a terminal moult may explain the condition of these heavily encrusted individuals, particularly as similar epibiont encrustations, and even bacterial shell disease, are most prevalent in other crab species that undergo a terminal moult (Engel and Noga, 1989; Fernandez et al., 1998).
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Experimental infections and risk of movements |
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As noted earlier, C. pagurus is a component of an extremely lucrative European fishery for decapod crustaceans. A significant feature of this market involves the movement of live animals between European member states for resale at market sites distant from capture sites. The movement of live crustaceans in this way is relatively uncontrolled, with losses in transport remaining unrecorded, and morbid or dead animals potentially finding their way back to the aquatic environment at the distant site. Moreover, the water used for transporting animals may be released accidentally or purposely to local waterways or drains. Although this review highlights a relatively detailed understanding of disease in species such as C. pagurus, the high rate of discovery of important pathogens in recent years, even from rather limited surveys, suggests a significant dearth in knowledge of potential pathogens of this and other commercially exploited species. Furthermore, we have almost no understanding of how these pathogens are transmitted, or of their potential for transmission to other commercially exploited and reservoir species. In this respect, the relatively uncontrolled cross-border movement of decapods has to be identified as a high-risk practice.
Additional risks to the European fishery for C. pagurus and other decapods have been demonstrated by their susceptibility to experimental infections by exotic pathogens. Most notably, WSSV, responsible for global catastrophic losses in culture facilities for penaeid shrimps, has been successfully transmitted to C. pagurus and other non-commercial crab species from European waters (Corbel et al., 2001). The extensive literature concerning this virus demonstrates the unusually large, susceptible crustacean host range, and the relative ease with which it can be transmitted to naïve hosts through ingestion of infected material. The high potential for spread to hosts from European waters, particularly from imported frozen-shrimp products and, presumably, imported broodstock or larvae for new culture ventures in the region, has been recognized recently by its inclusion in the European Council Fish Health Directive (2006/88/EC), which is being applied from August 2008. Importation of such exotic diseases when coupled with free movements of live crustaceans between states identifies a potential risk to the European crustacean fishery.
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Effects of disease on crustacean populations |
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Despite the relatively paucity of studies of disease in hosts inhabiting open-water marine systems in recent years, several authors have attempted to define the unique epidemiological features of marine habitats and the basis by which marine epidemics can be investigated (McCallum et al., 2003, 2004). These studies build on the growing realization that pathogen epidemics play a significant role in the population ecology of marine ecosystems (Harvell et al., 1999) and, further, that epidemics may be becoming more frequent because of various climatic and anthropogenic factors being imposed on them (Sherman, 2000; Lafferty et al., 2004; Ward and Lafferty, 2004). However, these studies also identify a basic gap in our knowledge of the baseline level of the diseases within these systems.
Despite the accepted importance of disease as a mortality driver in the ocean and the apparent separation of fisheries science from studies on disease prevalence, a study by Kuris and Lafferty (1992) highlighted the role that infectious organisms may play in crustacean populations and their associated fisheries—the particular infectious agent playing an appropriate role based upon its prevalence, intensity, and target organ(s). They also identify how specific fishing practices (e.g. the preferential capture of specific sexes, specific sizes, or within specific seasons) can alter the impact of pathogens within a population, particularly if post-capture practices such as disassembly of the catch at sea, culling of infected animals, or de-clawing crabs (Patterson et al., 2007) are also employed. Although these relationships between host, parasite, the environment, and fishers are complex, often requiring specific biological knowledge of pathogen and host life cycles, Kuris and Lafferty (1992) clearly identified how disease agents should be considered carefully when imposing management strategies onto a particular fishery. At present, the C. pagurus fishery in European waters is managed via area-specific MLS and, in certain areas, restrictions on trap numbers. Because of the increasing relative emphasis on this, and other, decapod crustacean fisheries in light of finfish stock declines, I urge managers to utilize disease data where possible in managing specific stocks and, further, to incorporate health surveys into standardized exercises on crustacean stock assessment. In this way, baseline data on important pathogens may be obtained, and early warning signs of a change in stock structure, for instance as a consequence of fishing pressure, can be placed into the context of likely future disease epidemics, particularly those involving host-size dependent pathogens.
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Acknowledgements |
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I thank my colleagues in the Pathology and Epidemiology team at the Cefas Weymouth laboratory for technical assistance with processing samples for histology and electron microscopy. The work was supported by the UK’s Department for Environment, Food and Rural Affairs (Defra) contract F1168.
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References |
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-
Anderson J. On the anatomy of Sacculina with a description of the species. Annals and Magazine of Natural History (1862) 9:3.
Armstrong D. A., Buchanan D. C., Caldwell R. S. A mycosis caused by Lagenidium sp. in laboratory-reared larvae of the Dungeness crab, Cancer magister, and possible chemical treatments. Journal of Invertebrate Pathology (1976) 28:329–336.[CrossRef][Web of Science]
Armstrong D. A., Burreson E. M., Sparks A. K. A ciliate infection (Paranophrys sp.) in laboratory-held Dungeness crabs, Cancer magister. Journal of Invertebrate Pathology (1981) 37:201–209.[CrossRef][Web of Science]
Austin B., Alderman D. J. Bacterial shell disease of crustaceans. (1987) ICES Identification Leaflets for Diseases and Parasites of Fish and Shellfish, 31. 4.
Ayres P. A., Edwards E. Notes on the distribution of "black spot" shell disease in crustacean fisheries. Chemistry in Ecology (1982) 1:125–130.[CrossRef]
Bang F. B., Audouin J., Leglise M. Ciliate infection of the blood of the edible crab, Cancer pagurus, in holding tanks in Brittany, France. Journal of Invertebrate Pathology (1972) 20:226–227.[CrossRef][Web of Science]
Bateman K. S., Stentiford G. D. Cancer pagurus bacilliform virus (CpBV) infecting juvenile European edible crabs (Cancer pagurus) from UK waters. Diseases of Aquatic Organisms (2008) 79:147–151.[CrossRef][Web of Science][Medline]
Boschma H. On the identity of Sacculina triangularis and Sacculina inflata. Proceedings of the Royal Society of Edinburgh, 51 (1931) (Cited by Boschma, 1955).
Boschma H. The Rhizocephala in the collection of the British Museum. Journal of the Linnean Society, 38 (1933) (Cited by Boschma, 1955).
Boschma H. The described species of the family Sacculinidae. Zoologische Verhandelingen (1955) 27:1–76.[Medline]
Brattey J., Elner R. W., Uhazy L. S., Bagnall A. E. Metazoan parasites and commensals of five crab (Brachyura) species from eastern Canada. Canadian Journal of Zoology (1985) 63:2224–2229.
Brun F. Sur la presence de Turbellariés parasites du genre Fecampia en Méditerranée. Bulletin du Muséum d’Histoire Naturelle de Marseille (1967) 32:141–145.
Castberg T., Torgersen T., Aasen J., Aune T., Naustvoll J. Diarrhoetic shellfish poisoning toxins in Cancer pagurus Linnaeus, 1758 (Brachyura, Cancridae) in Norwegian waters. Sarsia (2004) 89:311–317.[CrossRef][Web of Science]
Cattaneo G. Su di un infusorio ciliato, parasito del sangue del Carcinus maenas. Zoologischer Anzeiger (1888) 11:456–459.
Childers R. K., Reno P. W., Olson R. E. Prevalence and geographic range of Nadelspora canceri (Microspora) in Dungeness crab Cancer magister. Diseases of Aquatic Organisms (1996) 24:135–142.[CrossRef][Web of Science]
Cipriani G. R., Wheeler R. S., Sizemore R. K. Characterization of brown spot disease of Gulf Coast shrimp. Journal of Invertebrate Pathology (1980) 36:255–263.[CrossRef][Web of Science]
Codreanu R., Codreanu-Balcescu D. On two Metschnikowia yeast species producing hemocoelic infections in Daphnia magna and Artemia salina (Crustacea, Phyllopoda) from Romania. Journal of Invertebrate Pathology (1981) 37:22–27.[CrossRef][Web of Science]
Comely C. A., Ansell A. D. The occurrence of black necrotic disease in crab species from the west coast of Scotland. Ophelia (1989) 30:95–112.[Web of Science]
Corbel V., Coste F., Bonami J. R. CPSBV, a systemic virus of the edible crab, Cancer pagurus (L.). Journal of Fish Diseases (2003) 26:121–126.[CrossRef][Web of Science][Medline]
Corbel V., Zuprizal S. Z., Huang C., Sumartono A. J-M., Bonami R. Experimental infection of European crustaceans with white spot syndrome virus (WSSV). Journal of Fish Diseases (2001) 24:377–382.[CrossRef][Web of Science]
Costa-Ramos C., Rowley A. F. Effect of extracellular products of Pseudoalteromonas atlantica on the edible crab Cancer pagurus. Applied and Environmental Microbiology (2004) 70:729–735.
Couch J. A. Diseases caused by protozoa. In: The Biology of Crustacea. 6. Pathobiology—Provenzano A. J., ed. (1983) New York: Academic Press. 94–98.
Crothers J. H. Dale Fort marine fauna. Field Studies (1966) 2:i–ixxiv+169 pp.
Desportes I., Le Charpentier I., Galian A., Bernard P., Cochand-Priollet B., Lavergne A., Ravisse P., et al. Occurrence of a new microsporidian: Enterocytozoon bieneusi n.g. n. sp. in the enterocytes of human patients with AIDS. Journal of Protozoology (1985) 32:250–254.[Web of Science][Medline]
Desportes I., Perkins F. O. Phylum Paramyxea. In: Handbook of Protoctista—Margulis L., Corliss J. O., Melkonian M., Chapman D. J., eds. (1989) Boston: Jones and Bartlett. 30–35.
Dyrynda E. A. Shell disease in the common shrimp Crangon crangon: variations within an enclosed estuarine system. Marine Biology (1998) 132:445–452.[CrossRef]
Engel D. W., Noga E. J. Shell disease among the blue crab population of Pamlico Sound, North Carolina. Journal of Shellfish Research (1989) 8:460–461.
Fernandez L., Parapar J., Gonzalez-Gurriaran E., Muino R. Epibiosis and ornamental cover patterns of the spider crab Maja squinado on the Galician coast, northwestern Spain: influence of behavioral and ecological characteristics of the host. Journal of Crustacean Biology (1998) 18:728–737.[CrossRef][Web of Science]
Fisher W. S., Wickham D. E. Egg mortalities in wild populations of the Dungeness crab in central and northern California. Fishery Bulletin US (1975) 75:235–237.
Freeman M. A., Bell A. S., Sommerville C. A hyperparasitic microsporidian infecting the salmon louse, Lepeoptheirus salmonis: an rDNA-based, molecular phylogenetic study. Journal of Fish Diseases (2003) 26:667–676.[CrossRef][Web of Science][Medline]
Getchell R. G. Bacterial shell disease in crustaceans: a review. Journal of Shellfish Research (1989) 8:1–6.
Ginsburger-Vogel T., Desportes I. Étude ultrastructurale de la sporulation de Paramarteilia orchestiae gen. n. sp. n. parasite de l’amphipode Orchestia gammarellus (Pallus). Journal of Protozoology (1979) 26:390–403.[Web of Science]
Gotto V. Commensal and parasitic copepods associated with marine invertebrates. In: Synopses of the British Fauna, 46, 2nd edn.—Crothers J. H., Hayward P. J., eds. (2004) UK: Field Studies Council. 352.
Hansson H. G. NEAT (North East Atlantic Taxa): South Scandinavian Marine Plathelminthes Check-List. Internet edn, August 1998. (1998).
Harvell C. D., Kim K., Burkholder J. M., Colwell R. R., Epstein P. R., Grimes D. J., Hofmann E. E., et al. Emerging marine diseases—climate links and anthropogenic factors. Science (1999) 285:1505–1509.
Heath D. J. The distribution and orientation of epizoic barnacles on crabs. Zoological Journal of the Linnean Society (1976) 59:59–67.[CrossRef][Web of Science]
Holt E. W. L. Foreign substances attached to crabs. Nature (1890) 41:463–464.
Hryniewiecka-Szyfter Z., Babula A. Ultrastructural study of pathological effects on the female reproductive system of Saduria entomon L. (Crustacea, Isopoda) from the Baltic infected with Cryptococcus laurentii (Kufferath) Skinner. Invertebrate Reproduction and Development (1996) 29:149–156.
Hryniewiecka-Szyfter Z., Babula A. Ultrastructural changes in the hepatopancreas cells of Saduria entomon (Linnaeus, 1758) (Isopoda, Valvifera) from the Baltic infected with Cryptococcus laurentii (Kufferath) Skinner. Crustaceana (1997) a 70:822–830.[CrossRef][Web of Science]
Hryniewiecka-Szyfter Z., Babula A. Ultrastructural changes in the hindgut cells of Saduria entomon (Linnaeus, 1758) (Isopoda, Valvifera) from the Baltic infected with Cryptococcus laurentii (Kufferath) Skinner. Crustaceana (1997) b 70:198–205.[CrossRef][Web of Science]
Hryniewiecka-Szyfter Z., Smith M. T., Kaznowski A. Infection of Baltic Saduria entomon (Linnaeus, 1758) (Isopoda, Valvifera) with the yeast Cryptococcus laurentii (Kufferath) Skinner. Crustaceana (1994) 66:205–211.[CrossRef][Web of Science]
Hsu J-P., Liu C. I. Studies on yeast infection in cultured, giant, freshwater prawn (Macrobrachium rosenbergii). COA Fisheries Series, Taipei (1994) 47:55–68.
Ingle R. W. Shallow water crabs. In: Synopses of the British Fauna, 25, 2nd edn—Barnes R. S. K., Crothers J. H., eds. (1996) UK: Field Studies Council. 243.
James B. L. The digenea of the intertidal prosobranch, Littorina saxatilis (Olivi). Zeitschrift für Zoologische Systematik und Evolutionforschung (1967) 7:273–316.
Johnson P. T. Paramoebiasis in the blue crab, Callinectes sapidus. Journal of Invertebrate Pathology (1977) 29:308–320.[CrossRef][Web of Science]
Johnson P. T. Viral diseases of marine invertebrates. Helgoländer Meeresuntersuchungen (1984) 37:65–98.[CrossRef][Web of Science]
Kamm M. W. Studies on gregarines. 2. Synopsis of the polycystid gregarines of the world, excluding those from the Myriopoda, Orthoptera and Coleoptera. (1922) Illustrated Biological Monographs, 7. 104.
Knight-Jones P., Knight-Jones E. W. Taxonomy and ecology of British Spirorbidae (Polychaeta). Journal of the Marine Biological Association of the UK (1977) 57:453–499.
Kobatake M., Van Rij N. J. W. K., Placido M. T. L. C., Van Uden N. V. Isolation of proteolytic psychotrophic yeasts from fresh raw seafoods. Letters in Applied Microbiology (1992) 14:37–42.[CrossRef][Web of Science]
Kuris A. M., Lafferty K. D. Modelling crustacean fisheries: effects of parasites on management strategies. Canadian Journal of Fisheries and Aquatic Sciences (1992) 49:327–336.
Kuris A. M., Lafferty K. D., Torchin M. E. Biological control of the European green crab, Carcinus maenas: natural enemy evaluation and analysis of host specificity. In: 2nd International Symposium on Biological Control of Arthropods. Switzerland, 2005 (2005) USDA Forest Service Publication FHTET-2005-08.
Kuris A. M., Torchin M. E., Lafferty K. D. Fecampia erythrocephala rediscovered: prevalence and distribution of a parasitoid of the European shore crab, Carcinus maenas. Journal of the Marine Biological Association of the UK (2002) 82:955–960.[CrossRef]
Lafferty K. D., Porter J. W., Ford S. E. Are diseases increasing in the ocean? Annual Reviews in Ecology and Evolutionary Systematics (2004) 35:31–54.[CrossRef]
Latrouite D., Morizur Y., Noël P., Chagot D., Wilhelm G. Mortalite du tourteau Cancer pagurus provoquee par le dinoflagelle parasite. Hematodinium sp. ICES Document CM 1988/K: 32 (1988).
Leibovitz L. Hematopoietic chlamydiosis of the rock crab (Cancer irroratus) and the Jonah crab (Cancer borealis). Biological Bulletin (1988) 175:306.
Lom J., Dyková I. Protozoan parasites of fishes. (1992) Developments in Aquaculture and Fisheries Science, 26. 315.
Lom J., Nilsen F. Fish microsporidia: fine structural diversity and phylogeny. International Journal of Parasitology (2003) 33:107–127.[CrossRef][Web of Science][Medline]
Lu C. C., Tang K. F. H., Chen S. N. Identification and genetic characterization of yeasts isolated from freshwater prawns, Macrobrachium rosenbergii de Man, in Taiwan. Journal of Fish Diseases (1998) 21:185–192.[CrossRef][Web of Science]
Malm A. W. Om Cirripeder funna vid Bohusläns Kust. Göteborgs Naturhistoriska Museum. Zoology (1881) 3:26–32.
McCallum H., Harvell D., Dobson A. Rates of spread of marine pathogens. Ecology Letters (2003) 6:1062–1067.[CrossRef][Web of Science]
McCallum H. I., Kuris A., Harvell C. D., Lafferty K. D., Smith G. W., Porter J. Does terrestrial epidemiology apply to marine systems? Trends in Ecology and Evolution (2004) 19:585–591.[CrossRef]
McIntosh N. A study of black necrosis on the edible crab Cancer pagurus. (1963) Torry Research Station, Aberdeen, unpublished report. 13.
Metschnikoff E. Ueber eine Sprosspilzkrank-heit der Daphnien. Beitrag zur Lehre über den Kampf der Phagocyten gegen Krankheitserreger. English translation. Archiv für Pathologische Anatomie und Physiologie und für Klinische Medizin (1884) 96:177–195.
Meyers T. R. Diseases caused by protistans and metazoans. In: Diseases of Marine Animals, 3—Kinne O., ed. (1990) Germany: Biologische Anstalt Helgoland. 350–423.
Morado J. F., Giesecke R. H., Syrjala S. E. Molt-related mortalities of the Dungeness crab Cancer magister caused by a marine facultative ciliate Mesanophrys pugettensis. Diseases of Aquatic Organisms (1999) 38:143–150.[CrossRef][Web of Science]
Morado J. F., Small E. B. Morphology and stomatogenesis of Mesanophrys pugettensis n. sp. (Scuticociliatida: Orchitophryidae), a facultative parasitic ciliate of the Dungeness crab, Cancer magister (Crustacea: Decapoda). Transactions of the American Microscopical Society (1994) 113:343–364.
Morado J. F., Small E. B. Ciliate parasites and related diseases of Crustacea: a review. Reviews in Fisheries Science (1995) 3:275–354.[CrossRef]
Newman M. O., Feng S. Y. Susceptibility and resistance of the rock crab Cancer irroratus Say to natural and experimental bacterial infections. (1981) Abstracts of the National Shellfish Association Annual Meeting, Williamsburg, VA, USA. 105.
Olson R. E., Tiekotter K. L., Reno P. W. Nadelspora canceri n.g. n. sp. an unusual microsporidian parasite of the Dungeness crab, Cancer magister. Journal of Eukaryotic Microbiology (1994) 41:349–359.[CrossRef][Web of Science]
Patterson L., Dick J. T. A., Elwood R. W. Physiological stress responses in the edible crab Cancer pagurus, to the fishery practice of de-clawing. Marine Biology (2007) 152:265–272.[CrossRef]
Pearson J. Cancer (1908) Memoirs of the Liverpool Marine Biology Committee, 16. 223.
Pixell-Goodrich H. Reactions of Gammarus to injury and disease, with notes on some microsporidial and fungoid diseases. Quarterly Journal of Microscopical Science (1928) 72:325–353.
Powell A., Rowley A. F. Unchanged prevalence of shell disease in the edible crab Cancer pagurus four years after decommissioning of a sewage outfall at Langland Bay, UK. Diseases of Aquatic Organisms (2005) 68:83–87.[CrossRef][Web of Science][Medline]
Refardt D., Canning E. U., Mathis A., Cheney S. A., Lafranchi-Tristem N. J., Ebert D. Small subunit ribosomal DNA phylogeny of microsporidia that infect Daphnia (Crustacea: Cladocera). Parasitology (2002) 124:381–389.[Web of Science][Medline]
Reno P. W., Childers R., Olson R. E. Prevalence, lethality, and transmission of Nadelspora canceri, a microsporidian parasite of Dungeness crabs. (1994) University of California, International Symposium on Aquatic Animal Health, 1994 (Abstracts). 111.
Renouf L. P. W. Xantho incisus Leach and Cancer pagurus L. infested with Sacculina carcini Thompson, on the south coast of Co. Cork. Annals and Magazine of Natural History (1932) 10:132–133.
Richard J. Essai sur les parasites et les commensaux des Crustacés. Archives de Parasitologie (1899) 2:548–595.
Sawyer T. K. Two new crustacean hosts for the parasitic amoeba, Paramoeba perniciosa. Transactions of the American Microscopical Society (1976) 95:271.
Schmidt G. D., MacLean S. A. Polymorphus (Profilicollis) major Lundström 1942 juveniles in rock crabs, Cancer irroratus, from Maine. Journal of Parasitology (1978) 64:953–954.[CrossRef]
Sherman B. H. Marine ecosystem health as an expression of morbidity, mortality and disease events. Marine Pollution Bulletin (2000) 41:232–254.[CrossRef][Web of Science]
Shields J. D. The infestation and dispersion patterns of Carcinonemertes spp. (Nemertea) on their crab hosts. Hydrobiologia (1990) 266:45–56.[CrossRef]
Shields J. D. Research priorities for diseases of the blue crab Callinectes sapidus. Bulletin of Marine Science (2003) 72:505–517.[Web of Science]
Shields J. D., Okazaki R. K., Kuris A. M. Brood mortality and egg predation by the Nemertean, Carcinonemertes epialti, on the yellow rock crab, Cancer anthonyi, in southern California. Canadian Journal of Fisheries and Aquatic Sciences (1993) 47:1275–1281.
Sindermann C. J. Principal Diseases of Marine Fish and Shellfish, 2, 2nd edn (1990) London: Academic Press. 247–302.
Small H. J., Shields J. D., Moss J. A., Reece K. S. Conservation in the first internal transcribed spacer region (ITS1) in Hematodinium species infecting crustacean hosts found in the UK and Newfoundland. Diseases of Aquatic Organisms (2007) 75:251–258.[CrossRef][Web of Science][Medline]
Small H. J., Neil D. M., Taylor A. C., Bateman K., Coombs G. H. A parasitic scuticociliate infection in the Norway lobster (Nephrops norvegicus). Journal of Invertebrate Pathology (2005) 90:108–117.[CrossRef][Web of Science][Medline]
Sparks A. K., Hibbits J. A trematode metacercaria encysted in the nerves of the Dungeness crab, Cancer magister. Journal of Invertebrate Pathology (1981) 38:88–93.[CrossRef][Web of Science]
Sparks A. K., Hibbits J., Fegley J. Observations on the histopathology of a systemic ciliate (Paranophrys sp.) disease in the Dungeness crab, Cancer magister. Journal of Invertebrate Pathology (1982) 39:219–228.[CrossRef][Web of Science]
Sparks A. K., Morado J. F., Hawkes J. W. A systemic microbial disease in the Dungeness crab, Cancer magister, caused by a Chlamydia-like organism. Journal of Invertebrate Pathology (1985) 45:204–217.[CrossRef][Web of Science]
Spencer J. F. T., Phaff H. J., Gardner N. R. Metschnikowia kamienskii sp. n. a yeast associated with brine shrimp. Journal of Bacteriology (1964) 88:758–762.
Sprague V. Classification and phylogeny of the Microsporidia. In: Comparative Pathobiology, Systematics of the Microsporidia, 2—Bulla L. A., Cheng T. C., eds. (1977) New York: Plenum Press. 1–510.
Sprague V., Couch J. An annotated list of protozoan parasites, hyperparasites, and commensals of decapod Crustacea. Journal of Protozoology (1971) 18:526–537.[Web of Science]
Stentiford G. D., Bateman K. S. Enterospora sp.—an intranuclear microsporidian infection of hermit crab (Eupagurus bernhardus). Diseases of Aquatic Organisms (2007) 75:73–78.[CrossRef][Web of Science][Medline]
Stentiford G. D., Bateman K. S., Longshaw M., Feist S. W. Enterospora canceri n. gen. n. sp. intranuclear within the hepatopancreatocytes of the European edible crab Cancer pagurus. Diseases of Aquatic Organisms (2007) 75:61–72.[CrossRef][Web of Science][Medline]
Stentiford G. D., Evans M. G., Bateman K., Feist S. W. Co-infection by a yeast-like organism in Hematodinium-infected European edible crabs Cancer pagurus and velvet swimming crabs Necora puber from the English Channel. Diseases of Aquatic Organisms (2003) 54:195–202.[CrossRef][Web of Science][Medline]
Stentiford G. D., Green M., Bateman K., Small H. J., Neil D. M., Feist S. W. Infection by a Hematodinium-like parasitic dinoflagellate causes pink crab disease (PCD) in the edible crab Cancer pagurus. Journal of Invertebrate Pathology (2002) 79:179–191.[CrossRef][Web of Science][Medline]
Stentiford G. D., Shields J. D. A review of the parasitic dinoflagellates Hematodinium species and Hematodinium-like infections in marine crustaceans. Diseases of Aquatic Organisms (2005) 66:47–70.[CrossRef][Web of Science][Medline]
Stephenson K. Havedderkopper (Pycnogonida) og Rankefødder (Cirripedia). Danmarks Fauna (1933) 38. (Cited by Boschma, 1955).
Stunkard H. W. The morphology and life-history of the digenetic trematode, Microphallus similis (Jagerskiold, 1900) Baer, 1943. Biological Bulletin (1957) 112:254–266.
Thiel M., Kruse I. Status of the Nemertea as predators in marine ecosystems. Hydrobiologia (2004) 456:21–32.[CrossRef]
Torgersen T., Aasen J., Aune T. Diarrhetic shellfish poisoning by okadeic acid esters from brown crabs (Cancer pagurus) in Norway. Toxicon (2005) 46:572–578.[Medline]
Unestam T. Fungal diseases of Crustacea. Reviews in Medical and Veterinary Mycology (1973) 8:1–20.
Vivarès C. P., Azevedo C. Ultrastructural observations of the life cycle stages of Ameson atlanticum sp. nov. a microsporidian parasitizing Cancer pagurus L. Journal of Fish Diseases (1988) 11:379–387.[CrossRef][Web of Science]
Vogan C. L., Costa-Ramos C., Rowley A. F. A histological study of shell disease syndrome in the edible crab Cancer pagurus. Diseases of Aquatic Organisms (2001) 47:209–217.[Web of Science][Medline]
Vogan C. L., Costa-Ramos C., Rowley A. F. Shell disease syndrome in the edible crab, Cancer pagurus—isolation, characterization and pathogenicity of chitinolytic bacteria. Microbiology (2002) 148:743–754.
Vogan C. L., Llewellyn P. J., Rowley A. F. Epidemiology and dynamics of shell disease in the edible crab Cancer pagurus: a preliminary study of Langland Bay, Swansea, UK. Diseases of Aquatic Organisms (1999) 35:81–87.[CrossRef][Web of Science]
Vogan C. L., Rowley A. F. Dynamics of shell disease in the edible crab Cancer pagurus: a comparative study between two sites on the Gower Peninsula, South Wales, UK. Diseases of Aquatic Organisms (2002) a 52:151–157.[CrossRef][Web of Science][Medline]
Vogan C. L., Rowley A. F. Effects of shell disease syndrome on the haemocytes and humoral defences of the edible crab, Cancer pagurus. Aquaculture (2002) b 205:237–252.[CrossRef][Web of Science]
Ward J. R., Lafferty K. D. The elusive baseline of marine disease: are diseases in ocean ecosystems increasing? Public Library of Science (PloS), Biology (2004) 2:542–547.
Wickham D. E. Predation by the nemertean Carcinonemertes errans on the eggs of the Dungeness crab Cancer magister. Marine Biology (1979) 55:45–53.[Medline]
Wickham D. E. Aspects of the life history of Carcinonemertes errans (Nemertea: Carcinonemertidae), an egg predator of the crab Cancer magister. Biological Bulletin (1980) 159:247–257.
Wickham D. E. Epizootic infestations by nemertean brood parasites on commercially important crustaceans. Canadian Journal of Fisheries and Aquatic Sciences (1986) 43:2295–2302.
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