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Advances in our understanding of the global diversity and distribution of Hematodinium spp. – Significant pathogens of commercially exploited crustaceans

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Abstract

Hematodinium species are parasitic dinoflagellates known to infect a growing number of marine crustacean genera from around the world, many of which support important commercial fisheries. Affected hosts undergo dramatic pathological alterations to their organs, tissues and hemolymph. There are no known control measures for this disease. Economically important wild fished hosts known to be susceptible to Hematodinium spp. include Tanner crabs Chionoecetes bairdi and snow crabs Chionoecetes opilio in the Northeast Pacific and Atlantic Oceans, blue crabs Callinectes sapidus from the Atlantic and Gulf coasts of the United States, and Norway lobsters Nephrops norvegicus and Edible crabs Cancer pagurus from European waters. In recent years, several farmed aquatic crustaceans in China have also been negatively impacted by Hematodinium-associated diseases, likely representing an emerging issue for that expanding industry. Molecular sequence data indicates that there are two species, Hematodinium perezi, and a second species, currently unnamed, infecting hosts from the Northern Hemisphere. Three subtly different H. perezi genotypes have been identified infecting hosts from different geographical locations: the English Channel, the eastern seaboard of the United States and Gulf of Mexico, and eastern China. Genotypic variability between isolates of the Hematodinium sp. infecting hosts from the North Atlantic and North Pacific has also been reported, though it is unclear whether there is any correlation with host or location. Identification of Hematodinium species (and genotypes of H. perezi) is largely dependent upon geographical location, rather than host species. However this is not exclusive, as both Hematodinium species can be found infecting multiple species from same location, as is the case in the English Channel.

Highlights

Hematodinium spp. are parasitic dinoflagellates that infect both wild and aquaculture crustaceans. ► Several hosts support important commercial fisheries. ► Two Hematodinium spp. infect hosts from the Northern Hemisphere. ► Three different Hematodinium perezi genotypes.

Introduction

Hematodinium species are parasitic dinoflagellates that are known to infect a growing number of marine crustacean genera, many of which are commercially exploited (recently reviewed by Stentiford and Shields, 2005). Infections are fatal and there are no proven treatment measures. Grossly infected hosts are often lethargic, and undergo a number of pathological alterations to their hemolymph, tissues, and organs. These alterations are often used as the basis of names for the disease, though these conditions are not always present in all host species, or in light infections. One of the most common features in grossly infected hosts is hyperpigmentation, or a “cooked” appearance of the host carapace and appendages (see Fig. 1) and is observed in Chionoecetes spp. (Meyers et al., 1987), Nephrops norvegicus (Field et al., 1992, Tärnlund, 2000), Cancer pagurs (Pink Crab Disease (PCD), Stentiford et al., 2002) and occasionally in Portunus trituberculatus (Xu et al., 2007a) and Scylla serrata (Li et al., 2008). Advanced infections are typically characterized by lethargic hosts presenting masses of parasitic stages in their hemolymph (Fig. 2) and tissues (Fig. 3), the former’s color often being altered (white/cream) due to the presence of high numbers of parasites (often in excess of 106 ml−1, see Fig. 2). In recent years, the observation of cream-colored hemolymph and body fluids from a number of cultured hosts from China has given rise to several local names for the condition, including “milky disease” (Li et al., 2008, Xu et al., 2007a), “yellow water disease” (Xu et al., 2007b), and “milky shrimp disease” (Xu et al., 2010). Another pathological outcome of infection, with commercially important consequence, is presented in severely parasitized Alaskan Tanner crabs Chionoecetes bairdi, and snow crabs Chionoecetes opilio, in which there is a biochemical alteration of the meat products, such that these are bitter tasting and unmarketable, resulting in the condition known as Bitter Crab Disease (BCD) or Bitter Crab Syndrome (BCS, Meyers, 1990, Meyers et al., 1987). Cooked meats from Hematodinium-infected velvet swimming crabs Necora puber, from French waters have also been reported as having a bitter taste (Wilhelm and Mialhe, 1996), as have Hematodinium-infected meats from red king crabs Paralithodes camtschaticus, and blue king crabs P. platypus, from Russian waters (Ryazanova, 2008).

Hematodinium infections have the potential to significantly impact wild host crustacean populations and associated fisheries in several different ways. Direct effects include a loss of fishable resource, and a reduction of recruitment into the fishery. Numerous studies have described major outbreaks of Hematodinium-associated diseases that have significantly impacted host populations, yet these are likely underestimates as parasite prevalence is typically highest in unfished juveniles, which are not often effectively sampled in fishery-dependent (and independent) surveys. Prevalences of 70–100% have been reported in juvenile blue crabs Callinectes sapidus, from the seaside bays of Maryland and Virginia, USA, in 1991 and 1992 (Messick, 1994). Reduced annual landings of crabs from the same locations in the same years suggests significant effects to the population and fishery (Messick and Shields, 2000). Likewise, drastic reductions (96%) in velvet swimming crab catches from the Mor-Braz area of southern Brittany, France, between 1984 and 1988 coincided with the discovery and documentation of Hematodinium prevalence’s reaching 80% (Wilhelm and Mialhe, 1996). Significant commercial losses can also occur post capture, such as with BCD/BCS, where the inclusion of a single infected individual can ruin the flavor of an entire batch of processed crabs (Meyers et al., 1987). Poor survival of Hematodinium-infected C. pagurus during holding and transportation to continental Europe have also been reported (Stentiford et al., 2002). Other indirect effects include potential castration (see Stentiford and Neil, 2011), and immunocompromisation leading to co-infections with other pathogens (Appleton, 1996, Stentiford et al., 2003).

The genus was originally established by Chatton and Poisson (1931) and the type species, Hematodinium perezi, described as a rare parasite of the shore crab Carcinus maenas, and harbor crab Liocarcinus depurator (formerly Portunus depurator), from the French coastline. Members of this genus were infrequently encountered in French hosts during the following decade (Gallien, 1938) and received little attention in subsequent years. It was not until the 1970s when a morphologically similar parasite was encountered infecting commercially important blue crabs C. sapidus, from North Carolina, Georgia, and Florida, in the United States (Newman and Johnson, 1975), and was followed by additional reports of its presence in several other hosts, including amphipods, from the eastern seaboard (Johnson, 1986, MacLean and Ruddell, 1978). Meyers et al. (1987) subsequently reported a Hematodinium sp. infecting commercially important Tanner crabs C. bairdi, from southeast Alaska, and then from snow crabs C. opilio (Meyers, 1990). Since its reporting from Alaska in 1987, the frequency and number of Hematodinium infections have greatly increased, and it is now present in many hosts from several continents (see Table 1), including Europe (Denmark, England, France, Ireland, Scotland, Sweden), North America (eastern seaboard of America and Canada, Gulf of Mexico, North Pacific, Bering Sea, Greenland), Australia (east and west coast), and recently in Asia (China and Russia). Although dates and descriptions of the discovery of Hematodinium spp. in the literature are not definitive proof of the parasite’s first presence in that host, there is general agreement that Hematodinium infections are increasing in frequency and are being encountered in new hosts and locations (Bower et al., 2003, Eigemann et al., 2010, Morado, 2011, Morado et al., 2010, Ryazanova, 2008, Xu et al., 2007a, Xu et al., 2007b, Xu et al., 2010).

Despite its significant threat to both wild and cultured marine crustaceans, the taxonomy of members of the genus has remained largely in disarray, with only two species formally described from 40+ hosts, primarily due to a lack of distinctive characters and absence of knowledge of the ultrastructure and genetic characteristics of the type species. However, in the last two decades, and in particular the last decade, several studies attempting to assess the genetic relationships between Hematodinium isolates have revealed informative taxonomic affiliations (Eigemann et al., 2010, Hamilton et al., 2007, Hamilton et al., 2009, Hamilton et al., 2010, Hudson and Adlard, 1996, Jensen et al., 2010, Pagenkopp Lohan, 2011, Small et al., 2006, Small et al., 2007a, Small et al., 2007b, Small et al., 2012). In this paper I will review studies that have generated DNA-based data in an effort to clarify the distribution and taxonomic diversity among members of the genus. Emphasis is also placed upon reviewing the recent emergence of Hematodinium-associated diseases in crustaceans from Asia.

Section snippets

Hosts and worldwide distribution

At the present time, 38 species of marine decapod crustaceans have been diagnosed with Hematodinium spp. infections (see Table 1). In addition, several species of amphipods have also been suggested as infected with Hematodinium spp. or Hematodinium-like parasites (Johnson, 1986, Messick and Shields, 2000, Pagenkopp Lohan et al., 2012, Small, 2004). This list is likely to expand as the parasite spreads via oceanic currents, host movements and range extensions, and human mediated transport

Taxonomic diversity

The genus Hematodinium was originally established by Chatton and Poisson (1931), and was represented by the type species H. perezi, which was formally described from two European portunid crab species, C. maenas and L. depurator, from four locations on the English Channel, Atlantic, and Mediterranean coast of France. Parasite stages observed by light microscopy included motile elongate multinucleate plasmodia, globular multinucleate plasmodia, and either non-motile vegetative trophonts or

China

Within the last decade Hematodinium-associated diseases have emerged in several commercially-important marine crustaceans from China. In 2004 significant mortalities of cultured swimming crabs, P. trituberculatus, from open culture ponds in the Zhoushan island area, Zhejiang Province, eastern China (see Fig. 8), were reported to local authorities. Affected crabs were reported from July to September and were described as lethargic, having white muscle tissues and milky hemolymph leading to the

Conclusions and future directions

Though studies have been fragmented, it is obvious that significant progress has been made in the last two decades towards understanding the diversity and distribution of Hematodinium throughout the world’s oceans (see Fig. 4 and Table 1). The combined use of morphological and molecular sequence data, particularly the latter, is likely to drive the further classification and re-classification of Hematodinium species and strains (genotypes/ribotypes) as new informative regions of the parasite’s

Acknowledgments

Financial support is acknowledged from the Organization for Economic Co-operation and Development (OECD) and the National Science Foundation (NSF-grant No. OCEBE-UF 0723662). I would like to thank Kelly Bateman for providing the TEM image of H. perezi (used in the graphical abstract) and Dr. Caiwen Li for translating Chinese research papers into English. This is VIMS contribution No. 3203.

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