Protistan diseases of commercially important crabs: A review

Abstract

Protists are a diverse group of eukaryotes that possess a unicellular level of organization. As unicellular organisms, the differentiation of cells into tissues does not occur, although when cell differentiation does occur, it is limited to sexual reproduction, alternate vegetative morphologies or quiescent life history stages. Protistan parasites may possess simple or complex life histories that are important factors to consider when investigating protistan diseases of decapods. Unfortunately, the life histories of many protistan parasites of decapods are insufficiently described, resulting in the fact that modes of infection and transmission are often unidentified. This is surprising considering the economic importance of many marine decapods and the ability of protistan parasites to produce significant, but generally transient and area limited mortalities. However, the marine disease landscape is changing and will continue to change as climate change and ocean acidification will play important roles in disease occurrence and distribution. As a result, the following discussion attempts to summarize current knowledge on several crab diseases, their protistan etiological agents, the impact of disease on economically important crab populations and draw attention to areas of needed research. The discussion is not complete as only selected diseases are addressed, or perfect as the Microsporidia are included in the discussion (a traditional error continued in this summary) despite the recent, but controversial placement of the taxon with the fungi.

Introduction

Protistan parasites are extremely diverse pathogens that generally produce remarkable epizootics in wild crustacean and crab populations. Mortalities are the most striking feature of an epizootic, but other disease effects such as reduced growth and fecundity, and loss of product quality can greatly impact exploitation of a resource. Mortalities may be acute or chronic in duration and depending upon the severity of produced mortalities, they may impact local or widely distributed crab populations. I say “may” because with few exceptions, the effects of disease and associated mortalities on local, let alone large crab populations, have not been well documented. The reasons for this are linked to three major factors, the short-term nature of disease monitoring programs limiting the gathering of empirical data on the impact of parasites on free-living host populations (Grenfell and Gulland, 1995), the lack of information or understanding of recruitment processes that affect marine invertebrate populations (Hunt and Scheibling, 1997, Stenseth et al., 2002) and uncertainty of the size of the affected populations (Walters and Pearse, 1996, Orensanz et al., 1998).

A review of the literature suggests that long-term disease monitoring programs are few in number. Most diseases are described because an acute and major mortality event draws the attention of the fishing industry or recreational fishers. Management may also expand its search for explanations of rapid declines in population abundance of a crustacean resource such as the eastern Bering Sea red king crab (Paralithodes camtschaticus) collapse of the early 1980s. Several factors affect population abundance and distribution patterns of marine species, including habitat degradation, species interactions (e.g., predation, competition), exploitation rates of adults, fecundity of adults, environmental factors affecting larval drift and survival, and disease. Without dwelling on the role of each factor, it is likely that all probably interact in some fashion to affect population size and distribution patterns (Hastings, 1996). Caddy and Gulland (1983) classified exploited fish populations as steady state, cyclical, irregular or spasmodic and listed examples for each category. However, even for steady state fish populations, fluctuations do occur. As a result, Hilborn and Walters (1992) indicated that constancy is an anomaly rather than a rule and that changes in abundance of exploited fish populations should be expected, with or without fishing. It is highly probable that crustacean populations behave similarly.

Fish population abundance estimates are reliant upon fishery dependent and independent methods such as traditional acoustic and recently developed ocean acoustic waveguide remote sensing (Makris et al., 2006) methods, especially for schooling pelagic species. However, with the possible exception of euphausiid or krill populations (Foote and Stanton, 2000) the above techniques are not useful for other crustacean species. As a result, estimates of crustacean abundance are made through fishery independent assessment surveys and fishery dependent monitoring of commercial landings. Problems of relying upon each method are presented elsewhere (Hilborn and Walters, 1992) and will not be discussed here. Never the less, they may serve as proxies for estimating the size of a target population that may not be otherwise possible, but which must be supplemented with sufficient knowledge on the biology of an exploited resource and an objective view of that resource (Orensanz et al., 1998, Dew and McConnaughey, 2005).

So what is the significance of diagnosing and monitoring protistan diseases of wild crabs and other crustaceans? FAO (FAO, 2009) reports that marine landings of global capture fisheries for 2006 was 92 million tonnes (t) with an estimated value of $91.2 billion US. No crustacean species is listed among the top 10 with respect to worldwide landings (Fig. 1). However, when a similar list is compiled by value (US$ mil), crustaceans are well represented (Table 1). In the United States, crab and shrimp are ranked 7th and 9th in pounds landed, but are 1st and 2nd, followed by lobsters at 5th, with respect to value (Table 2). Clearly, crustacean species are an important food source, but they are also major components of ecosystems and contribute significantly to domestic and international economies. As a result, factors that may negatively impact crustacean abundance and product quality attract attention and are generally investigated. In this regard, some protistan diseases of historical and current importance include paramoebiasis in the blue crab, ciliate disease in the captive American lobster industry, and Hematodinium-associated disease in several decapod species worldwide.

In recent years, several researchers have suggested a correlation between an increase in the frequency of disease and climate change (Harvell et al., 1999, Harvell et al., 2002, Harvell et al., 2004). Other researchers have countered that the data are not unequivocal (Lafferty et al., 2004, Ward and Lafferty, 2004). Regardless, the notion of a dynamic relationship between pathogen, environment and host to produce disease is not new as the relation was first investigated by Hippocrates (Martin and Martin-Granel, 2006). In recent times, the relationship between host, pathogen and environment was re-addressed by Cockburn (1963) and later expanded to the aquatic environment by Snieszko (1973). The relation takes on current added importance because the marine environment is clearly changing in various parts of the world (Anderson and Piatt, 1999, Grebmeier et al., 2006). Parasite or disease affects are not limited to mortalities as parasite infections, especially microparasite infections may also affect fecundity, size structure of a population or cause reduced marketability of a resource (Dobson and May, 1987, Dobson and Hudson, 1995). As a result, a systematic approach for investigating epizootics and their potential effects on affected populations needs to be adopted. For example, Hematodinium-associated diseases are currently investigated via different methods with varying detection sensitivities (i.e., gross recognition, macroscopic methods, examination of bloodsmears, conventional polymerase chain reaction (cPCR), quantitative PCR (qPCR)) and with little or no environmental data. It is also clear that significant effort must be directed at understanding the biology and ecology of pathogens, host susceptibility and how the environment may modulate the host/pathogen relation. In this regard, the comprehensive approach on chytrid and viral pathogens of amphibians should serve as a model (http://lifesciences.asu.edu/irceb/amphibians/).

Protistan systematics has changed considerably in recent years. A previous classification of the Protozoa (Levine et al., 1980) followed the traditional grouping of morphologically similar organisms as initially proposed by Bütschli (1880–1889). However, the recent classification (Adl et al., 2005) is a marked departure from previous classification schemes. It is greatly influenced by molecular phylogenetics and is based on nameless ranked systematics. Six clusters or super-groups of eukaryotes are currently recognized and the following discussion on protistan pathogens of commercially important crabs will follow the new convention. The following discussion will follow a standard format in the discussion of selected protistan diseases of crabs. The discussion will not be exhaustive as that is impossible within the limits of this review and there are a number of excellent reviews in the literature.