The role of alternate hosts in the ecology and life history of Hematodinium sp., a parasitic dinoflagellate of the blue crab (Callinectes sapidus)

Hematodinium sp. infections are relatively common in some American blue crab (Callinectes sapidus) populations in estuaries of the western Atlantic Ocean. Outbreaks of disease caused by Hematodinium sp. can be extensive and can cause substantial mortalities in blue crab populations in high salinities. We examined several species of crustaceans to determine if the same species of Hematodinium that infects C. sapidus is found in other crustaceans from the same localities. Over a 2-yr period, 1,829 crustaceans were collected from the Delmarva Peninsula, Virginia, examined for the presence of infections. A portion of the first internal transcribed spacer (ITS1) region of the ribosomal RNA (rRNA) gene complex from Hematodinium sp. was amplified and sequences were compared among 35 individual crustaceans putatively infected with the parasite, as determined by microscopic examination, and 4 crustaceans putatively infected based only on PCR analysis. Of the 18 crustacean species examined, 5 were infected with Hematodinium sp. after microscopic examination and PCR analysis, including 3 new host records, and an additional species was positive only via PCR analysis. The ITS1 rRNA sequences of Hematodinium sp. from the infected crustaceans were highly similar to each other and to that reported from C. sapidus (>98%). The similarity among these ITS1 sequences and similarities in the histopathology of infected hosts is evidence that the same species of Hematodinium found in C. sapidus infects a broad range of crustaceans along the Delmarva Peninsula. Our data indicate that the species of Hematodinium found in blue crabs from estuaries along the east coast of North America is a host generalist, capable of infecting hosts in different families within the Order Decapoda. Additionally, evidence indicates that it may be capable of infecting crustaceans within the Order Amphipoda.     

Epizootiology of the parasitic dinoflagellate Hematodinium sp. in the American blue crab Callinectes sapidus

Hematodinium sp. is a parasitic dinoflagellate that infects and kills blue crabs Callinectes sapidus. Periodic outbreaks of dinoflagellate infections with subsequent high host mortalities prompted a study of the epizootiology and distribution of the crab pathogen. Hemolymph samples from over 13000 crabs were assessed for infections over 8 yr. Moderate to high prevalences were found at several locations along the Atlantic and Gulf coasts of the United States. In the coastal bays of Maryland and Virginia, prevalence followed a seasonal pattern, with a sharp peak in late autumn. Infections were significantly more prevalent in crabs measuring less than 30 mm carapace width; host sex did not influence prevalence. Prevalences were highest in crabs collected from salinities of 26 to 30%o; no infected crabs were found in salinities below 11%o. Intensity of infection did not vary among crab sizes, molt stages, or sexes. Naturally and experimentally infected crabs died over 35 and 55 d in captivity, with a mean time to death of approximately 13 and 42 d, respectively. Several other crustaceans, including gammaridean amphipods, xanthid (mud) crabs, and the green crab Carcinus maenus, were found with Hematodinium-like infections. Considering its widespread distribution and high pathogenicity, we suggest that Hematodinium sp. represents a significant threat to blue crab populations in high salinity estuaries along the Atlantic and Gulf coasts of the USA.     

The effect of salinity on experimental infections of a Hematodinium sp. in blue crabs, Callinectes sapidus

The parasitic dinoflagellate Hematodinium sp. parasitizes blue crabs along the Atlantic seaboard of the United States. Infections in blue crabs have only been reported from waters where salinity is >11 practical salinity units (psu). Blue crabs maintain a hyperosmotic internal concentration at low salinities (0-5 psu), roughly comparable to 24 psu, and should be capable of maintaining an infection in low-salinity waters even if Hematodinium spp. cells are intolerant of low salinities. We tested this notion by observing the effect of low salinity on the progression of disease in crabs experimentally infected with the parasite. Blue crabs were acclimated to 5 psu or 30 psu salinity treatments. They were inoculated with Hematodinium sp. and necropsied 3, 7, 10, and 15 days post-inoculation. The low-salinity treatment did not have an effect on the proliferation of Hematodinium sp. infections in blue crabs; moreover, a greater proportion of infections in crabs in the low-salinity treatment developed dinospore stages than did those in the high-salinity treatment, indicating that salinity may affect the development of the parasite. However, dinospores from in vitro cultures rapidly became inactive when held in salinities <15 psu. Our experiments indicate that Hematodinium spp. can develop in blue crabs at low salinities, but that the parasite is incapable of transmission in this environment, which explains the lack of natural infections in crabs at low salinities.     

Conservation in the first internal transcribed spacer region (ITS1) in Hematodinium species infecting crustacean hosts found in the UK and Newfoundland

Parasitic dinoflagellates in the genus Hematodinium infect a number of decapod crustaceans in waters off the UK, including the Norway lobster Nephrops norvegicus and the edible crab Cancer pagurus. This study investigated sequence variability in the first internal transcribed spacer (ITS1) region of the ribosomal RNA complex of Hematodinium spp. infecting N. norvegicus, C. pagurus, and Pagurus bernhardus from 4 locations in the UK and from the Hematodinium sp. infecting Chionoecetes opilio from the province of Newfoundland and Labrador, Canada. Phylogenetic analysis of the Hematodinium ITS1 sequences from N. norvegicus, C. pagurus, P. bernhardus and C. opilio suggest that these crustaceans are infected with the same species of Hematodinium. Length variability of the ITS1 region was observed (324 to 345 bp) and attributed to 4 variable microsatellite regions (CATG)n' (GCC)nTCCGC(TG)n' (TA)n' and (GAA)n(GGA)n within the sequenced ITS1 fragment. The observed variation may be due to co-infection of the host crustacean with several different strains of Hematodinium or differences among copies of ITS1 region within the genome of a single parasite cell. The Hematodinium ITS1 sequence from N. norvegicus, C. pagurus, P. bernhardus and C. opilio isolates was sufficiently conserved in primer binding regions targeted by previous molecular diagnostic assays; therefore, we suggest that this assay could be used to screen for Hematodinium infections in these crustacean hosts.     

A new species of halfbeak, Hyporhamphus naos (Beloniformes: Hemiramphidae), from the tropical eastern Pacific

The tropical eastern Pacific halfbeak previously considered conspecific with the western Atlantic Hyporhamphus unifasciatus (Ranzani 1842) is described as a new species, H. naos. It resembles H. meeki from the Atlantic and Gulf coasts of the United States in number of gill rakers on the first arch (usually 32-36, mean 33.6), more than in H. unifasciatus (usually 29-32, mean 30.6), but fewer than in other sympatric species of eastern Pacific Hyporhamphus. Results of a three-treatment ANCOVA (H. naos, H. meeki, and H. unifasciatus) show significant differences in slopes and means for all 14 morphometric characters examined, 9 of 14 characters comparing H. naos with H. unifasciatus, and 7 of 14 comparing H. naos with H. meeki. Protein electrophoretic patterns clearly distinguish all three species with a number of fixed allelic differences.     

Taxonomy and biogeography of the fiddler crabs (Ocypodidae: Genus Uca) of the Atlantic and Gulf coasts of eastern North America

Fifteen species of fiddler crabs are reported for eastern North America between Massachusetts and Quintana Roo, Mexico. Thirteen occur in the United States and 11 in Mexico, with eight in common to the two countries. Of 13 species in the Gulf of Mexico, five are endemic and a sixth is restricted largely to the peninsulas of Florida and Yucatan. The status of U. rapax in the northern Gulf remains to be resolved. Range limits of most species approximate one or the other of two sets of intersecting thermal and geological boundaries that subdivide the Gulf of Mexico along north-south and east-west axes. Species belonging to subgenus Minuca tend to replace one another at the thermally-controlled Carolinian-Caribbean marine biotic boundary across the Florida peninsula and northern Gulf. However, only U. minax of all the North American fiddler crabs exhibits the classical disjunct Carolinian distribution, and this appears basically to reflect the discontinuous distribution of temperate salt marshes that are the habitat of the species. Distributions of species belonging to subgenus Celuca adhere for the most part to the subdivision of the Gulf into western terrigenous and eastern carbonate sedimentary provinces. The northern transition occurs in the vicinity of Apalachee Bay and the southern at Laguna de Terminos. A third distributional pattern is shown by U. subcylindrica , a specialized endemic species of the hypersaline Laguna Madre system of the western Gulf. The level of endemism in the fiddler crabs is relatively high in comparison with that of other marine groups within the Gulf of Mexico. This may be a consequence of the adaptations of fiddler crabs as specialized deposit feeders to regional differences in climatic and edaphic characteristics of a marginally marine upper shore habitat. The distributional patterns of the endemics could prove useful in reconstructing palaeoecological events of evolutionary significance within the Gulf of Mexico.     

Epidemiology of bitter crab disease (Hematodinium sp.) in snow crabs Chionoecetes opilio from Newfoundland, Canada

The parasitic dinoflagellate Hematodinium sp. causes a condition known as bitter crab disease (BCD) in snow crabs Chionoecetes opilio and Tanner crabs C. bairdi. As the name of the condition implies, crabs infected with BCD are unmarketable due to their bitter flavor. We surveyed the distribution of BCD in 3 regions within the snow crab fishery of Newfoundland from 1997 to 2003. Over time, the disease has become firmly established in Conception and Bonavista Bays and persists at low levels on the Avalon fishing grounds. An epizootic occurred within Bonavista and Conception Bays in 1999 and persisted in Conception Bay in 2000, reaching prevalences of over 2% to 9% in trapped and trawled male crabs and from 19 to 26% in trawled and trapped female crabs, respectively. Infections were highest in females and small males, i.e. the unfished and pre-recruit portions of the fishery. In a mortality study, all of the naturally infected crabs died and 50% of the experimentally inoculated crabs died. Patterns in the molting cycle and prevalence of infection indicate that transmission occurs during the post-molt condition, and that overt infections probably develop 2 to 4 mo later with mortalities occurring at least 3 to 4 mo thereafter. The hydrography of this bay may have contributed to the epizootic as infections were centered within the deeper confines of the bay. Analysis of various abiotic factors uncovered a significant positive association between prevalence, depth and mud/sand substrates; the nature of this relationship was not apparent but may be related to diet or alternate hosts. Lastly, given the increase in BCD in snow crabs in Newfoundland, we recommend that fishery management programs for Chionoecetes fisheries employ non-selective gear to monitor for Hematodinium infections in female and juvenile crabs because these under-sampled members of the population may forewarn of impending recruitment declines that might otherwise remain unexplained.     

A review of the parasitic dinoflagellates Hematodinium species and Hematodinium-like infections in marine crustaceans

Parasitic dinoflagellates in the genus Hematodinium are important parasites of marine Crustacea. Outbreaks of these parasites have damaged commercial stocks of Norway lobster Nephrops norvegicus, snow crab Chionoecetes opilio, Tanner crab C. bairdi, American blue crab Callinectes sapidus, and velvet swimming crab Necora puber. Species of Hematodinium can reach high enough levels to regulate their host populations, but mortalities are also centred on the unfished juveniles and females, hosts not normally sampled by fisheries; hence impacts are often underreported. Seasonal prevalences of up to 85 % occur annually in many host populations; in effect, these parasites form cryptic blooms in the water column with crabs and other crustaceans at risk of disease. We review the biology and ecology of Hematodinium spp. infections in crustaceans. Included is a comparison of the different infections, a synthesis of what is known, and an attempt to highlight fruitful areas for continued research.     

Bioaccumulation of lithium by marine organisms in European, American, and Asian coastal zones: microanalytic study using secondary ion emission

37 species of aquatic mammals, fish, crustacea, annelids, molluscs belonging to cephalopods, gasteropods and lamellibranchs were collected from coastal waters of France: North Sea, English Channel, Atlantic Ocean, Mediterranean Sea, from Greece: Aegian Sea, from North America: Atlantic Ocean and from Japan: Pacific Ocean, Sea of Japan and East China Sea. Microanalyses which were performed on organs and tissues, using secondary ion mass spectrometry, revealed high concentrations of lithium, which is commonly used in human therapy, but is also toxic in low amounts. The retention of this metal by the marine organisms appears as a general phenomenon independent of their biotope and geographical origin; the highest lithium levels were detected in the fish muscles (= edible part).     

Trans‐Pacific and trans‐Arctic pathways of the intertidal macroalga Fucus distichus L. reveal multiple glacial refugia and colonizations from the North Pacific to the North Atlantic

Aim We examined the phylogeography of the cold‐temperate macroalgal species Fucus distichus L., a key foundation species in rocky intertidal shores and the only Fucus species to occur naturally in both the North Pacific and the North Atlantic. Location North Pacific and North Atlantic oceans (42° to 77° N). Methods We genotyped individuals from 23 populations for a mitochondrial DNA (mtDNA) intergenic spacer (IGS) (n = 608) and the cytochrome c oxidase subunit I (COI) region (n = 276), as well as for six nuclear microsatellite loci (n = 592). Phylogeographic structure and connectivity were assessed using population genetic and phylogenetic network analyses. Results IGS mtDNA haplotype diversity was highest in the North Pacific, and divergence between Pacific haplotypes was much older than that of the single cluster of Atlantic haplotypes. Two ancestral Pacific IGS/COI clusters led to a widespread Atlantic cluster. High mtDNA and microsatellite diversities were observed in Prince William Sound, Alaska, 11 years after severe disturbance by the 1989 Exxon Valdez oil spill. Main conclusions At least two colonizations occurred from the older North Pacific populations to the North Atlantic between the opening of the Bering Strait and the onset of the Last Glacial Maximum. One colonization event was from the Japanese Archipelago/eastern Aleutians, and a second was from the Alaskan mainland around the Gulf of Alaska. Japanese populations probably arose from a single recolonization event from the eastern Aleutian Islands before the North Pacific–North Atlantic colonization. In the North Atlantic, the Last Glacial Maximum forced the species into at least two known glacial refugia: the Nova Scotia/Newfoundland (Canada) region and Andøya (northern Norway). The presence of two private haplotypes in the central Atlantic suggests the possibility of colonization from other refugia that are now too warm to support F. distichus. With the continuing decline in Arctic ice cover as a result of global climate change, renewed contact between North Pacific and North Atlantic populations of Fucus species is expected.     

Revision of the monogenean subfamily Priceinae Chauhan, 1953 (Polyopisthocotylea: Thoracocotylidae)

Members of the subfamily Priceinae are gastrocotylinean monogeneans of the gills of scombrid fishes of the genus Scomberomorus (and perhaps the genera Acanthocybium, Rastrelliger and Katsuwonus) from warm to warm-temperate seas of the world. We revise the diagnosis of the subfamily and regard the Mexicotylinae Lebedev, 1984 as a synonym. Two monotypic genera are accepted as valid. Pricea multae Chauhan, 1945 is recorded from seven species of Scomberomorus from the Indo-west Pacific, from off eastern South Africa north to the Persian Gulf and as far east as Fiji. New synonyms we recognise include P. minimae Chauhan, 1945 (described from India, reportedly on Katsuwonus pelamis), P. solandri Gupta & Chanana, 1977 (a single specimen was described from India, reportedly on Acanthocybium solandri) and P. microcotylae Chauhan, 1945 (also described from India, reportedly on Rastrelliger kanagurta). Mexicotyle mexicana (Meserve, 1938) Lebedev, 1984 is recorded on four species of Scomberomorus from the western Atlantic Ocean (United States to Brazil), two in the eastern Pacific (California to Peru) and one from the eastern Atlantic (Ghana).     

Predicting the distribution and ecological niche of unexploited snow crab (Chionoecetes opilio) populations in Alaskan waters: a first open-access ensemble model

Populations of the snow crab (Chionoecetes opilio) are widely distributed on high-latitude continental shelves of the North Pacific and North Atlantic, and represent a valuable resource in both the United States and Canada. In US waters, snow crabs are found throughout the Arctic and sub-Arctic seas surrounding Alaska, north of the Aleutian Islands, yet commercial harvest currently focuses on the more southerly population in the Bering Sea. Population dynamics are well-monitored in exploited areas, but few data exist for populations further north where climate trends in the Arctic appear to be affecting species' distributions and community structure on multiple trophic levels. Moreover, increased shipping traffic, as well as fisheries and petroleum resource development, may add additional pressures in northern portions of the range as seasonal ice cover continues to decline. In the face of these pressures, we examined the ecological niche and population distribution of snow crabs in Alaskan waters using a GIS-based spatial modeling approach. We present the first quantitative open-access model predictions of snow-crab distribution, abundance, and biomass in the Chukchi and Beaufort Seas. Multi-variate analysis of environmental drivers of species' distribution and community structure commonly rely on multiple linear regression methods. The spatial modeling approach employed here improves upon linear regression methods in allowing for exploration of nonlinear relationships and interactions between variables. Three machine-learning algorithms were used to evaluate relationships between snow-crab distribution and environmental parameters, including TreeNet, Random Forests, and MARS. An ensemble model was then generated by combining output from these three models to generate consensus predictions for presence-absence, abundance, and biomass of snow crabs. Each algorithm identified a suite of variables most important in predicting snow-crab distribution, including nutrient and chlorophyll-a concentrations in overlying waters, temperature, salinity, and annual sea-ice cover; this information may be used to develop and test hypotheses regarding the ecology of this species. This is the first such quantitative model for snow crabs, and all GIS-data layers compiled for this project are freely available from the authors, upon request, for public use and improvement.     

Hematodinium sp. (Alveolata, Syndinea) detected in marine decapod crustaceans from waters of Denmark and Greenland

Five decapod crustacean species were examined for presence of the parasitic dinoflagellate Hematodinium spp. (Alveolata, Syndinea) by morphological methods (colour and pleopod methods) as well as by PCR and nested PCR with Hematodinium-specific primers. Nephrops norvegicus, Pagurus bernhardus and Liocarcinus depurator were sampled by trawling in Danish waters and Chionoecetes opilio and Hyas araneus were sampled by trapping off the west coast of Greenland. The existence of Hematodinium has not previoiusly been documented in Danish waters, but it was detected in all 3 decapod species examined in the present study. Hematodinium sp. was also detected for the first time in H. araneus and the existence of Hematodinium sp. in Greenlandic C. opilio was documented by PCR. Analyses of 26 Hematodinium sp. ITS1 sequences, including sequences from all 5 host species sampled, revealed more than 95% sequence similarity between 24 of the sequences. Two Hematodinium sp. ITS1 sequences from C. opilio were only 81% similar to the 24 other ITS1 sequences. The nested PCR approach resulted in the highest reported percentages of positive samples for Hematodinium sp.in the hosts investigated (between 45 and 87.5%). However, no decapods were found to be infected with Hematodinium sp. based on morphological methods. Consequently, Hematodinium sp. may be more common than previously believed, and, assuming that the DNA found originated from viable and infectious parasite cells, infections may not always be fatal. We suggest that the hosts investigated may have been subject to latent infections that could develop into a fatal disease only if the hosts were physiologically stressed due to other factors.     

Differences in enzyme activities between two species of Hematodinium, parasitic dinoflagellates of crustaceans

Parasitic dinoflagellates of the genus Hematodinium infect several commercially important decapod crustaceans. Different species of Hematodinium have different levels of virulence in their respective hosts. Enzyme activities were studied from two species of Hematodinium, one isolated from the Norway lobster (Nephrops norvegicus) and the other from the American blue crab (Callinectes sapidus). We report the identification of differences in secretion of acid phosphatase (AP) and leucine arylamidase from two parasite species. Leucine arylamidase was only contained and secreted by the species infecting the blue crab. Both parasite species contained AP, but only the species infecting the Norway lobster secreted this enzyme. In this species, AP activity was predominantly in the soluble fraction (69.5%). AP activity was localized to cytoplasmic granules and on the membranes surrounding the cell nucleus. In addition to providing information on the cellular metabolism of the parasite, the pattern of activities of these enzymes may also be useful in distinguishing among different species of Hematodinium.     

Pathology of Hematodinium infections in snow crabs (Chionoecetes opilio) from Newfoundland, Canada

Bitter crab disease (BCD) of snow crabs, Chionoecetes opilio, is caused by a parasitic dinoflagellate, Hematodinium sp. The disease has shown an alarming increase in prevalence in the commercial fishery in eastern and northeastern areas of Newfoundland and Labrador since it was first recorded there in the early 1990s. We documented histopathological alterations to the tissues in snow crabs with heavy infections of Hematodinium sp. and during sporulation of the parasite. Pressure necrosis was evident in the spongy connective tissues of the hepatopancreas and the blood vessels in most organs. In heavy infections, little remained of the spongy connective tissues around the hepatopancreas. Damage to the gills varied; in some cases it was severe, particularly during sporulation, involving apparent thinning of the cuticle, loss of epithelial cells, and fusion of the membranous layers of adjacent gill lamellae. Affected lamellae exhibited varying degrees of distention with a loss of trabecular cells, hemocyte infiltrations, and swelling or "clubbing" along the distal margins. Large numbers of zoospores were located along the distal margins of affected lamellae suggesting that sporulation may cause a lysis or bursting of the thin lamellar cuticle, releasing spores. Pressure necrosis, due to the build up of high densities of parasites, was the primary histopathological alteration in most tissues. Hematodinium infections in the snow crab are chronic, long-term infections that end in host death, during sporulation of the parasite.     

Evidence for a permanent establishment of the snow crab (Chionoecetes opilio) in the Barents Sea

In the Atlantic the snow crab (Chionoecetes opilio) is naturally distributed on the northwestern side, i.e. eastern Canada and west Greenland. Until recently, there have been no observations of snow crab in eastern Atlantic. However, in 1990s single and occasional reports were made of crabs captured in the eastern part of the Barents Sea, presumably introduced through ballast water. Special attention during the annual bottom-trawl surveys in the Barents Sea during February 2004–2006 were given to include recordings of snow crab to evaluate if the introduced species has succeeded to establish a self-sustaining population in this region. Recordings of snow crabs were systematically noted and biological measurements carried out. The results confirm previous Russian observations of snow crabs in the northern region of Gåsebanken. In addition, a significant number of crabs were also found in the central region of the Barents Sea, mainly in deeper waters from 180 to 350 m depth. The sizes ranged from 14 to 136 mm carapace width. All females above 70 mm were berried with fertilised eggs. A major fraction (31% in 2005; 76% in 2006) of the crabs consisted of juveniles below 50 mm CW, providing evidence for successful recruitment. The small-sized crabs were exclusively found in Gåsebanken, identifying the main recruiting area at present for snow crab in the Barents Sea. The results obtained show that the snow crab is now adapted to the northeast Atlantic.