Description
Phylum- Haplosporidians are parasites of marine and freshwater invertebrates, characterized by uninucleate or multinucleate cells, and propagules consisting of uninucleate spores with ornamented walls (Perkins 1990). The Haplosporidia have been placed in the phylum Acetospora in the past, and treated as a class, together with another protistan group, the Paramyxea. Recent phylogenetic analysis (small subunit RNA and ultrastructure), supports the treatment of the phylum Haplosporidia as a monophyletic sister group of the clade Alveolata, containing Ciliophora (ciliates), Dinoflagellida, and Apicomplexa (ciliates) (Flores et al. 1996; Siddall et al. 1995).
Species Name, Genus, Synonymy- There are only two genera in the phylum Haplosporidia, and these are defined morphologically. Flores et al. (1996) found that Minchinia and Haplosporidium could not be distinguished using ribosomal RNA subunit sequences, so that the generic distinction was not supported. These two genera may be combined, or split further, in the future (Flores et al. 1996).
Potentially Misidentified Species - Haplosporidium costale (Seaside Disease, SSO) is also a disease of Crassostrea virginica (Eastern Oyster), which differs from H. nelsoni in spore morphology, sites of infection, and salinity tolerance (Andrews 1980; Andrews 1984; Ford and Tripp 1996). Minchinia teredinis is a parasite of the shipworms Teredo nelsoni, T. furcifera, and T. bartschi, and is immunologically and morphologically distinct from H. nelsoni (Hillman et al. 1990; McGovern and Burreson 1989; McGovern and Burreson 1990).
Taxonomy
| Kingdom | Phylum | Class | Order | Family | Genus |
|---|---|---|---|---|---|
| Protista | Haplosporidia | Haplosporea | Haplosporida | Haplosporidiidae | Haplosporidium |
Synonyms
Invasion History
Chesapeake Bay Status
| First Record | Population | Range | Introduction | Residency | Source Region | Native Region | Vectors |
|---|---|---|---|---|---|---|---|
| 1958 | Established | Expanding | Introduced | Regular Resident | Eastern Pacific | Western Pacific | Fisheries(Oysters-accidental); Ballast Water; Fouling Community |
History of Spread
Haplosporidium nelsoni (MSX, Delaware Bay Disease), a parasite of Crassostrea virginica (Eastern Oyster), first appeared in North America in 1957 on Egg Island Bar, on the NJ side of Delaware Bay. The disease was associated with massive die-offs of oysters, and prompted intensive research, but it was not until 1966 that the causative organism was sufficiently well characterized for a formal description. Before this, the organism was often referred to as 'MSX' (for 'multiple spheres of X' (Haskin et al. 1966). The origin of the disease has been a source of speculation.
Andrews and Wood (1967) once suggested that this disease could have arisen as a mutation of Haplosporidium costalis (Seaside Disease), a presumably native oyster parasite found in high salinity Atlantic coast Bays. Ford (1992) suggested that H. nelsoni was, like H. costalis, an endemic species of high salinity bays, but less well adapted to this environment than H. costalis. She suggested that H. nelsoni became epizootic after its transfer into Delaware and Chesapeake Bays.
However, the discovery of spores similar in size and shape to H. nelsoni in Crassostrea gigas (Pacific Oyster) from South Korea (Kern 1976b) and the Pacific coast of the United States (CA) (Katkansky and Warner 1970) suggests that C. gigas may have been the original host of H. nelsoni (Andrews 1980). Several unofficial plantings of C. gigas are known to have occurred in coastal waters of NJ, MD, and DE in the 1930's through the 1970's. None of these introductions resulted in known reproducing populations of C. gigas, and none coincide with the appearance of H. nelsoni, but they are suggestive of Pacific oyster introductions as a possible mechanism (Andrews 1980). Recent immunological and ultrastructural comparisons between the Haplosporidium sp. found in Korean C. gigas and H. nelsoni from Chesapeake Bay indicate that the two are nearly identical (Burreson et al. 2000; Kern 1998). While deliberate oyster plantings are a possible vector, oysters in ship fouling and spores in ballast water could also have transferred the parasite to the US East Coast (Burreson 2004).
In quarantined flumes with running York River water, Crassostrea gigas (Pacific Oyster) did not contain detectable levels of H. nelsoni (Barber 1996), indicating that this oyster, at least under the prevailing conditions, was highly resistant to the parasite. In Korea, Japan, and the Pacific Coast of North America, the incidence of H. nelsoni appears to be very low (0.3-7%) (Kern 1976b; Friedman 1996).
The first recorded cases of H. nelsoni infection occurred in Delaware Bay in 1957, in Chincoteague Bay in 1958, and Chesapeake Bay in 1959. From 1960 to 1980, the parasite spread, often in a highly localized fashion, but Chesapeake and Delaware Bays remained the major sites of epizootic occurrences and massive oyster mortality due to MSX. However, in the 1980's and 1990's, major epizootic outbreaks occurred in many other estuaries. While there is evidence for the development of increasing resistance to the parasite, it appears that 'disease pressure' has also increased (Haskin and Andrews 1988). The spread of H. nelsoni on the Atlantic coast of the United States is summarized below from south to north:
FL and southward - A few cases of H. nelsoni infection were seen in 1985 from Jacksonville FL, and in 1986 from Biscayne Bay FL (Haskin and Andrews 1988). In a survey using molecular methods, with samples taken in 1974, Ulrich et al. (2007) found H. nelsoni in Crassostrea gigas and C. rhizophorae on the Florida and Mexican Gulf Coast,and Venezuela.
GA - H. nelsoni was first recorded from GA in 1986, in creeks of Camden County, at the southern end of the GA coast. Prevalence was very low, 1-6%, and MSX was not an important cause of mortality at that time. (Lewis et al. 1992).
SC - Occasional cases of H. nelsoni have been known in SC as early as 1986. In 1992, sporulating cells were found in oysters from Charlestown Harbor (Dougherty et al. 1993).
NC - In 1989, H. nelsoni was observed at a number of locations in Pamlico Sound NC, at prevalences of 2-28%. No mortalities were noted. The parasite was absent from oysters in the New and Cape Fear River estuaries to the south (Morrison et al. 1992).
Chesapeake Bay - H. nelsoni first appeared in Mobjack Bay VA in 1959 (Andrews and Wood 1967). Its subsequent spread is summarized below.
Hog Island-Chincoteague Bays - H. nelsoni appeared in Chincoteague Bay in 1958, and other VA Seaside bays in 1959 (Andrews and Wood 1967; Couch et al. 1968). In 1963, high rates of prevalence and mortality were seen in newly planted seed oysters. However, rates of mortality were lower than those seen in Delaware Bay or areas of highest prevalence in Chesapeake Bay (Couch et al. 1968). In recent years, prevalence of H. nelsoni has greatly decreased in the Mockhorn Channel, Hog Island Bay, reaching a maximum of 12% in 2008, indicating the development of resistance to the parasite these oysters (Carnegie and Burreson 2011).
Delaware Bay - Extensive oyster deaths due to H. nelsoni first occurred on Egg Island Bar, on the NJ side of the lower Bay in 1957 and subsequently spread through the lower Bay in 1958-59. The prevalence of disease decreased up the Bay, reaching peaks of 75-90% infection in the lowermost beds (Ledge Line, Egg Island, mean salinities of 20-23 ppt) but 10-30% in the uppermost beds surveyed (Arnolds, Cohansey, mean salinities of 9-12 ppt). Frequency of H. nelsoni infection in the upper Bay beds is correlated with river flow, and is highest during droughts, but in the lower Bay, year to year fluctuations are independent of salinity. Infections in the lower Bay show a long-term cyclic pattern with peaks every 6-8 years. At the same time, resistance to the disease has gradually increased among oyster populations (Ford and Haskin 1982; Haskin and Ford 1982; Haskin and Andrews 1988). An epizootic of the disease in the 1980s removed non-resistant oysters from low-salinity upper regions of the Bay, and since then prevalence of the parasite has been close to zero (Carnegie and Burreson 2011).
Before the advent of MSX, average oyster production had been ~1 million bushels per year, in 1957-1970 it fell to 75,000 bushels per year, but recovery occurred in the 1970's, to ~370,000 bushels per year, probably due in part to development of resistance, as well as changes in planting practices. However, drastic mortalities due to Perkinsus marinus (Dermo) reduced harvests again in the 1980's (McKenzie 1996).
Great South Bay, Long Island - H. nelsoni infections were found with prevalences of 24-54% and ~15% mortality in 1965 (Haskin and Andrews 1988).
Long Island Sound - H. nelsoni infections were found in Milford Harbor CT, in 1960, and at other CT oyster-growing areas, through 1985, with prevalences of 12-40% (Haskin and Andrews 1988).
MA - H. nelsoni appeared in Wellfeet Harbor MA (Cape Cod Bay) at low levels of prevalence in 1969. In 1969 and 1970, it was absent from other Cape Cod oyster-growing areas, suggesting that it been recently introduced by transplants from an area where the disease was epizootic (Krantz et al. 1972). MSX was confined to Wellfleet Harbor, and caused little mortality until extensive oyster mortalities occurred in 1982-1987 in Wellfleet Harbor and in 1985 in Cotuit Bay MA (off Nantucket Sound) (Haskin and Andrews 1988; Matheissen et al. 1990). Cape Cod oyster growers have traditionally depended on Long Island Sound seed from CT (Haskin and Andrews 1988).
NH and ME - In the Piscataqua River on the NH-ME border, H. nelsoni infection was first seen in 1983, but high prevalence and extensive mortality did not occur until 1995, and was associated with unusually warm conditions and high salinity (Barber et al. 1997). MSX has also been reported from the Damariscotta River, ME (Ford and Tripp 1996).
Gulf of St. Lawrence- In 2002, H. nelsoni caused extensive oyster mortalities in Bras d'Or Lake, a large estuary on Cape Breton, Nova Scotia (Canadian Broadcasting Corporation 2002).
Chesapeake Bay region records are summarized in more detail below:
Hog Island - Chincoteague Bays - H. nelsoni appeared in Chincoteague Bay in 1958, and other VA 'Seaside' bays in 1959 (Andrews and Wood 1967; Couch and Rosenfeld 1968). In the VA 'Seaside' bays, in August-October 1959, 11% of oysters were infected. In 1967, Andrews and Wood considered MSX to be reduced in activity in Seaside bays, compared to fully epizootic areas in lower Chesapeake Bay (Andrews and Castagna 1978; Andrews and Wood 1967). However, mortalities among previously unexposed James River seed oysters placed in VA 'Seaside' Bays increased from ~3-35% in 1959-1974 to 30-65% in 1976-1982 (Haskin and Andrews 1988). In the 1990s, Chincoteague Bay produced few oysters because of extensive diebacks due to MSX (McKenzie 1996). In recent years, prevalence of H. nelsoni has greatly decreased in the Mockhorn Channel, Hog Island Bay, reaching a maximum of 12% in 2008, indicating the development of resistance to the parasite these oysters (Carnegie and Burreson 2011).
Lower Chesapeake Bay - The arrival of H. nelsoni in Chesapeake Bay was expected after the 1957 outbreak in Delaware Bay and the 1958 occurrence in Chincoteague Bay, because there had been heavy traffic in shell and seed among the various bays. A monitoring program using trays of oysters was already in place because of high mortality due to Perkinsus marinus ('Dermo'). In August 1959, the first cases of H. nelsoni were observed in Horn Harbor, Egg Island and New Point Comfort (all in VA waters near Mobjack Bay). By December 1959, it had been found in the lower James, York, and Rappahannock Rivers, producing extensive mortalities, and mean prevalences of 13-31% (Andrews and Wood 1967). By 1967, H. nelsoni appeared to have 2 foci, Hampton Roads, and the lower York River where it was fully epizootic, producing high rates of mortality in every year, with reduced but variable activity in other saline areas, and greatly reduced rates of infection in low-salinity areas (Andrews and Wood 1967). Additional factors besides salinity seem to regulate the penetration of the disease into regions near H. nelsoni's upper limit of distribution (Andrews 1983). The prevalence and spatial extent of H. nelsoni stabilized during the wet years of the 1970's, but in 1980-81, and again in 1987-88, H. nelsoni, together with P. marinus expanded greatly, causing devastating losses in both MD and VA waters (Burreson and Ragone Calvo 1996; Haskin and Andrews 1988). In recent years, prevalence of H. nelsoni has greatly decreased in the Lynnhaven River, Norfolk, reaching a maximum of 12% in 2008, indicating the development of resistance to the parasite in lower Bay oysters (Carnegie and Burreson 2011).
James River - In August 1959, at Ocean View, at the river mouth oysters were in poor condition, with 3 of 17 (17%) infected. No infections were found in the upper James River beds (Brown Shoal Horsehead Bar) used for seed production (Andrews and Wood 1967). In 1967, Andrews and Wood considered H. nelsoni to be still fully epizootic in the lower river (Hampton Bar) and decreasing in prevalence and mortality upstream, and absent at Horsehead Rock (Andrews and Wood 1967). On Wreck Shoal, midway between Hampton Bar and Horsehead Bar, infection rates were highest (10-28%) in the early years of the disease (1960-1964), and then fell to near zero, rising again (8-12%) in 1980-81. Mortalities in this seed area occurred only in 1964 and 1980, but did not occur in other drought years (Andrews 1983). As H. nelsoni wiped out formerly productive beds in Hampton Roads and the lower river, areas formerly treated as seed areas became increasingly important for production (McKenzie 1996). In recent years, trends have reversed, with a high prevalence of disease (80-90%) and mortality among newly imported,'naive' young oysters at Wreck Shoa, but lower prevalence (20-40%) among established oysters, indicating the development of resistance (Carnegie and Burreson 2011).
York River - In September 1959, the first cases of H. nelsoni were observed at the Amoco pier at the river mouth, Gloucester Point, and Tillages Bar. The mean infection rate for 1959-60 was 17% (Andrews and Wood 1967). Andrews and Wood considered H. nelsoni to be still fully epizootic in all the oyster beds they sampled (Andrews and Wood 1967). Mortalities of previously unexposed seed oysters in trays at the Virginia Institute of Marine Sciences Pier usually ranged from 40-70% from 1959 to 1984 but fell to 10-15% in 1972 and 1984, and exceeded 70% in 1986-1987 (Haskin and Andrews 1988). After a peak of about 38% prevalence in 1998, prevalence of H. nelson declined to about 5-15%, indicating the development of resistance in wild populations (Carnegie and Burreson 2011).
Rappahannock River - A few cases of H. nelsoni were seen in October 1959-February 1960, particularly in the lower portions of the estuary (Broad Creek-Smoky Point). The mean infection rate for 1959-60 was 13%. In 1967, Andrews and Wood considered H. nelsoni to be reduced in activity at Hoghouse Rock in the lower river, and rare further upriver, except in dry years compared to fully epizootic areas. In 1964-1965, a drought pushed the upriver limit of H. nelsoni infections to Morrattico Bar (Andrews and Wood 1967). Oysters from the upper Rappahannock remain highly susceptible to the disease, and have high rates or prevalence and mortality, when transplanted to more saline waters of the lower Bay. However, prevalence of the diseases in the lower Rapphannock has dropped to 0-15% since 1998, and 0-5% since 2003, indicating the development of resistance to the disease (Carnegie and Burreson 2011).
Potomac River - A few cases of H. nelsoni infection were found near the mouth of the Potomac, but the disease was rare or absent in the estuary proper in the 1960's (Andrews and Wood 1967). In 1982, an intense spatfall occurred in Great Wicomico River, which became infected with H. nelsoni and died out in May-June 1983.
Eastern Shore - A few cases of H. nelsoni were seen in August 1959-October 1959-March 1960 from Cherrystone Creek VA near the Bay mouth to Pocomoke Sound (MD-VA). The mean infection rate for the fall 1959-spring 1960 was 13% (Andrews and Wood 1967), but in the fall of 1960 it was 26-55% (Farley 1975). By 1967, H. nelsoni was reduced in prevalence (~10% mean), compared to fully epizootic areas (Andrews and Wood 1967; Farley 1975). However, the spatial extent of infections increased dramatically on the Eastern Shore, reaching Kent Island MD by 1967 (Farley 1975), in 1981, and again in 1987-88. In 1985-1987, infections reached the Choptank and Chester Rivers H. nelsoni's prevalence and spatial extent increased greatly (Haskin and Andrews 1988; Burreson and Ragone Calvo 1996).
Oyster landings in MD waters had been about 2-2.7 million bushels per year in the 1960's to 1981, but following the increased incidence of both H. nelsoni and Perkinsus marinus, they fell to 1 million bushels in 1983, and 400,000 bushels in 1987 (McKenzie 1996). Current oyster harvests have ranged between 200,000 and 400,00 bushels. Estimates of abundance of the oyster population indicate that present abundances were 98.3 to 99.9% lower than in the early 1800's, and 92& since 1980 (Wilberg et al. 2001).
History References - Andrews 1976; Andrews 1980; Andrews 1983; Andrews and Castagna 1978; Andrews and Wood 1967; Barber 1996; Barber et al. 1997; Burreson and Ragone Calvo 1996; Burreson et al. 2000; Couch and Rosenfeld 1968; Dougherty et al. 1993; Farley 1975; Ford and Haskin 1982; Ford and Tripp 1996; Haskin et al. 1966; Haskin and Ford 1982; Haskin and Andrews 1988; Katkansky and Warner 1970; Kern 1976b; Kern 1998; Krantz et al. 1972; Lewis et al. 1992; Mattheissen et al. 1990; MacKenzie 1996; Morrison et al. 1992
Invasion Comments
Native Region, Source Region - Crassostrea gigas (Pacific Oyster) from Japan, Korea, and introduced C. gigas from CA are known to harbor at least one species of Haplosporidium (Friedman 1996; Katkansky and Warner 1972; Kern 1976b). Korean Haplosporidium sp. appear to be genetically very similar to Atlantic H. nelsoni (Burreson et al. 2000; Kern 1998). However, the taxonomy and geographic range of range of haplosporidians in Pacific oyster populations appears to be still largely unknown.
Range Status - The range of H. nelsoni in Chesapeake Bay appears to expand and contract, influenced partly by salinity. We've chosen to describe it as stable, but it reached a greater penetration into the upper Bay in the late 1980's and early 90's than seen in the 1960's and 1970's (Farley 1975; Haskin and Andrews 1988; MacKenzie 1996).
Ecology
Environmental Tolerances
| For Survival | For Reproduction | |||
|---|---|---|---|---|
| Minimum | Maximum | Minimum | Maximum | |
| Temperature (ºC) | 5.0 | 22.0 | ||
| Salinity (‰) | 10.0 | 35.0 | 15.0 | 35.0 |
| Oxygen | ||||
| pH | ||||
| Salinity Range | meso-eu |
Age and Growth
| Male | Female | |
|---|---|---|
| Minimum Adult Size (mm) | 0.0 | 0.0 |
| Typical Adult Size (mm) | 0.0 | 0.0 |
| Maximum Adult Size (mm) | 0.0 | 0.0 |
| Maximum Longevity (yrs) | ||
| Typical Longevity (yrs |
Reproduction
| Start | Peak | End | |
|---|---|---|---|
| Reproductive Season | |||
| Typical Number of Young Per Reproductive Event |
|||
| Sexuality Mode(s) | |||
| Mode(s) of Asexual Reproduction |
|||
| Fertilization Type(s) | |||
| More than One Reproduction Event per Year |
|||
| Reproductive Startegy | |||
| Egg/Seed Form |
Impacts
Economic Impacts in Chesapeake Bay
Haplosporidium nelsoni (MSX) has had very severe economic effects on Chesapeake Bay and the surrounding region. While it is difficult to separate out effects of Perkinsus marinus ('Dermo') and overharvesting, 'the trend in oyster harvests during the period (after 1980) parallels the course of MSX infection' (Lipton et al. 1992).This parasite has a direct effect on fisheries by drastic reducing oyster biomass and harvests, through elimination of oysterbeds as habitats, and possibly also through altering Bay foodwebs, through elimination of a major filter-feeder (Kennedy 1996).
Fisheries- H. nelsoni killed 90-95% of oysters in high salinity waters of Chesapeake Bay in the first few years of its invasion (1959-1962), but had little effect on seedbed areas in the James River or on beds in MD waters at this time (Haskin and Andrews 1988). Periods of low salinity in the 1980's and 1990's allowed MSX to penetrate far into the upper Bay, causing a drastic decline in MD harvests, together with epizootics of Perkinsus marinus ('Dermo'), and the effects of the oyster fishery itself (Lipton et al. 1992; McKenzie 1996).
Currently, fewer than 5% VA's traditional public oyster grounds are productive (Burreson and Calvo 1996). The state's total market oyster harvest, centered on the James River, but also including many other estuaries, dropped from ~4 million bushels/year in 1958 to 0.4-.6 million bushels/year in 1984-86 (Lipton et al. 1992).
In the lower Bay, the upper James River estuary, was the major source of seed oysters, while Hampton Roads was an important region for growth of market oysters. In 1959-1962, H. nelsoni wiped out formerly productive beds in Hampton Roads and the lower river, and parts of the estuary formerly treated as seed areas became increasingly important for production. However oyster sets on the seedbeds declined also, probably because adult oysters at Hampton Roads had been the primary source of larvae settling in the upper estuary (McKenzie 1996). The James River regularly produced ~2 million barrels of seed oysters per year from the 1850s to the 1950's. In 1986-1987, the harvest was 238,000 bushels of market oysters per year, and in 1995, a 'small quantity' of market oysters and ~20,000 bushels of seed oysters (McKenzie 1996). 'As a consequence of the small oyster stocks in Virginia, few tongers and planters remain active. The planters spread only test quatities of seed to determine whether they will live. Most oyster boats have decayed, lie in disuse around the Virginia oystering ports, or are used in other ventures' (McKenzie 1996).
The economic impact of H. nelsoni was delayed in MD waters by the parasite's intolerance of low salinities. In the mid-1960's it affected Pocomoke and Tangier sounds, but left most of the MD portion of the Bay (Farley 1975). However, in 1985-1987, MSX infections reached the Choptank and Chester Rivers. Haplosporidium nelsoni's prevalence and spatial extent increased greatly (Haskin and Andrews 1988; Burreson and Calvo 1996). Oyster landings in MD waters had been about 2-2.7 million bushels per year in the 1960's to 1981, but following the increased incidence of both H. nelsoni and P. marinus, they fell to 400,000 bushels in 1987, and 125,000 bushels in 1992-93. The oystering fleet fell from 1,200 hand-tonging boats, 700 patent-tonging boats, and 45 skipjacks, in the 1960's to 400 hand-tonging boats, 30 suba divers, and 7 skipjacks in 1992-93. A slight recovery occurred with lower salinities in 1992-94 (McKenzie 1996). H. nelsoni and P. marinus have also shifted the geography of oyster production up the bay. In 1973-74, 2.1% of the oyster harvest came from the Chester River, in 1993-94, 66% was from the Chester River (Burreson and Calvo 1996). A slight recovery in the harvest occurred in 1993-94 due to lower salinities (Burreson and Calvo 1996), but this has not altered the overall picture. The last oyster/shucking houses along the Bay have closed, so that the oysters which are harvested must be sent to southern states for packing (Kern 1998). 'Some Maryland ports still have oyster boats in them, but most are in disuse and various states of decay' (McKenzie 1996).
Habitat Change - Reduction in the area of oysterbeds has the potential to affect feeding and cover for some commercial fish species, including juvenile Morone saxatilis (Striped Bass) (Kennedy 1996).
Aesthetics - It has been suggested that the decrease in the filtering biomass of oysters is linked to an increase in phytoplankton concentrations, which has resulted in decreased visibility. A possible (but poorly documented) consequence of the intensification of the planktonic foodweb is an increased abundance of Chrysaora quinquecirrha (Sea Nettle) (Kennedy 1996).
References - Burreson and Calvo 1996; Farley 1975; Haskin and Andrews 1988; Kennedy 1996; Kern 1998; Lipton et al. 1992; MacKenzie 1996
Economic Impacts Outside of Chesapeake Bay
From the onset of Haplosporidium nelsoni (MSX) disease in 1957, through the 1970's, the disease has been regarded as epizootic only in Delaware and Chesapeake Bays, but in the 1980's, serious mortalities occurred in eastern Long Island Sound and in Cape Cod waters (Haskin and Andrews 1988).
In Delaware Bay, before the advent of H. nelsoni, average oyster production had been ~1 million bushels per year; in 1957-1970 it fell to 75,000 bushels per year, but recovery occurred in the 1970's, to ~ 370,000 bushels per year, probably due in part to development of resistance, as well as changes in planting practices. After H. nelsoni became established, oystermen planted seed oysters large enough to be harvested after only one growing season. Between 1973 and 1985, the volume of oysters harvested was roughly equal to the volume of seed planted. However, increased mortalities due to H. nelsoni occurred after 1985, resulting in the closure of beds in NJ and DE waters from 1987 through 1989. In 1991, drastic mortalities due to Perkinsus marinus (Dermo) reduced harvests again in the 1990's (McKenzie 1996). The two oyster packing houses, and one shucking house left on the Bay process mainly out of state oysters, and seafood products other than oysters, and many of the remaining oystering boats are in poor condition (MacKenzie 1996).
References - Haskin and Andrews 1988; MacKenzie 1996
Ecological Impacts on Chesapeake Native Species
Haplosporidium nelsoni (MSX) has had profound effects on the native biota of Chesapeake Bay, by removing much of the living Crassostrea virginica (Eastern Oyster) population from more saline regions of the Bay. Combined with Perkinsus marinus (Dermo) and the effects of human harvesting, Haplosporidium nelsonihas altered the character of the Bay as a habitat (Kennedy 1996).
Parasitism - H. nelsoni first infects the epithelia of the gills and palps of the oyster, multiplying along the basal laminae, often causing extensive sloughing of parasite and host cells. In susceptible oysters, infection spreads rapidly through all tissues, causing mechanical disruption through proliferation of parasites, and lysis of cells. Symptoms in non-resistant oysters include recession of the mantle, emaciation, and 'pale digestive gland' . (Andrews 1976; Ford and Tripp 1996). Filtering rates drop sharply, probably due to gill damage, but metabolic rates under steady conditions are unchanged (Newell 1985). However, infected oysters rapidly increase respiration in response to temperature changes, compared to controls (Littlewood and Ford 1990). As a consequence of impaired energy balance, non-resistant infected oysters show a reduced condition index (an index of health, calculated as dry tissue weight/shell volume X 1000). Condition index on non-resistant infected oysters was 65% of that of uninfected controls, while fecundity was 19% of controls (Barber et al. 1988). The most vulnerable oysters begin to die within a month, and may be killed so rapidly that they do not show noticeable loss of condition (Andrews 1976; Ford and Tripp 1996). The combination of H. nelsoni with other symbionts, such as the shell-boring polychaete Polydora sp. may greatly increase mortality, presumably because the drain of energetic reserves makes Crassostrea virginica more vulnerable to other stressors (Wargo and Ford 1993).
Crassostrea virginica populations show varying degrees of resistance, depending on frequency and duration of previous exposure. The ability to contain H. nelsonii infection appears to be due mostly to resistance at the epithelial level, rather than detectable differences in hemocyte immune responses. Resistant oysters are still adversely affected by H. nelsoni parasitism, they suffer chronically rather than acutely, but a substantial percentage of them survive to market size. The condition index (see above paragraph) of infected, resistant oysters was higher than that of infected non-resistant animals. Resistant oysters only had epithelial infections. Their condition index was 87% of that of uninfected controls, while their fecundity was reduced to 65% (Barber et al. 1988). Chronically infected, resistant, Delaware Bay oysters in lower Delaware Bay, showed inhibition of gonad development in spring, but as temperatures increased, many had remissions and spawned. Thus, an effect of chronic H. nelsoni infection is the delay of gamogenesis. However, there was no correlation between year-to-year fluctuations in prevalence of the parasite and setting of oyster spat (Ford and Figueras 1988).
After a few years of the H. nelsoni epizootic which killed 90-95% of the native oysters, the descendants of the survivors of the initial epidemic had ~30% survival to marketable size, compared to 7% for introduced unexposed stocks (Ford and Tripp 1996). In Chesapeake Bay, where surviving broodstocks were mostly unexposed to the disease, resistant strains of oysters were produced by selective breeding and planted in lower Bay grounds (Andrews 1984). However, both resistant oyster populations also had high mortalities when exposed to the increased disease pressure which occurred in the 1980' s in Delaware and Chesapeake Bays (Ford and Tripp 1996). In Lynnhaven Bay, at the mouth of the Chesapeake, researchers found decreasing prevalence of H. nelsoni from 1997 to 2008, indicating increasing resistance to the parasite (Carnegie and Burreson 2011).
The effect of H. nelsoni epizootics, in combination with Perkinsus marinus (Dermo) and human harvesting is clearest in VA waters, where annual harvests dropped from ~4 million bushels/year in 1958 to 0.4-.6 million bushels/year in 1984-86. In MD waters, up to 1980, H. nelsoni was absent from most of the oyster grounds, and harvest was above 2 million bushels/year for most of the 1970's. From 1980 to 1988, the disease, together with 'Dermo', penetrated far up the bay, and harvests fell, reaching ~0.3 million bushels/year by 1988 (Lipton et al. 1992).
Competition - Another haplosporidian oyster parasite, H. costale (SSO; Seaside Disease), co-occurs with H. nelsoni in some creeks on the lowermost VA eastern shore of Chesapeake Bay, and in Atlantic coastal embayments of VA-MD north to NJ and possibly ME in high-salinity waters (above 25 ppt) (Andrews 1976; Ford and Tripp 1996; Wood and Andrews 1962). Haplosporidium costale appears to be less virulent than H. nelsoni, with a long incubation period, and a short (2 month, July-August) period of intense proliferation (Couch and Rosenfeld 1968). It is perhaps better adapted to C. virginica as a host, although it does regularly cause mortality in oysters (Andrews 1982). In Virginia Seaside bays, infections of H. costale appeared to have been partially suppressed by increased mortality due to H. nelsoni in the 1970's. H. nelsoni kills oysters more quickly than H. costale, removing potential hosts for the latter parasite (Andrews 1984).
Habitat Change - Crassostrea virginica (Eastern Oyster), as well as being historically abundant in numbers and biomass in Chesapeake Bay, is a major source of structure, a modifier of habitat, and plays a large role in both benthic and planktonic foodwebs. Oyster beds provide substrate and cover for a wide range of mobile and sessile fauna (Lippson and Lippson 1984; Kennedy 1996). Newell (1988) estimated that before 1870, the oyster population filtered the Bay water column in less than a week, while the current population would take 46 weeks to accomplish the same degree of filtration. This decrease in filtration could be partially responsible for the apparent increase in phytoplankton biomass in the Bay. H. nelsoni, as a major factor in the decline of oyster biomass, may have had far reaching effects on the trophic structure of the Bay. However, these speculations are based on a combination of modelling and rather sketchy historical data (Kennedy 1996).
References - Andrews 1976; Andrews 1982b; Andrews 1984; Barber et al. 1988; Couch and Rosenfeld 1968; Ford and Figueras 1988; Ford and Tripp 1996; Kennedy 1996; Lipton et al. 1992; Littlewood and Ford 1990; Newell 1985; Newell 1988; Wargo and Ford 1993
Ecological Impacts on Other Chesapeake Non-Native Species
Haplosporidium nelsoni (MSX) disease is a native parasite of the northwest Pacific oyster Crassostrea gigas (Pacfic Oyster), which it affects at low frequencies with few symptoms (Friedman 1996). The parasite also interacts with the cryptogenic oyster parasite Perkinsus marinus, competing for hosts, since mortality caused by one disease can limit the spread of the other (Andrews and Wood 1967).
Parasitism - In part as a result of the effects of the Haplosporidium nelsoni epizootic, the introduction of exotic oysters, first of Crassostrea gigas (Pacific Oyster), and later, C. ariakensis (Suminoe Oyster) has been extensively studied (Andrews 1980; Gottelieb and Schweighofer 1996). Pacific populations of C. gigas in several locations have been found to have haplosporidian parasites, though at very low frequencies (Friedman 1996; Katkansky and Warner 1972; Kern 1976b). Korean Haplosporidium sp. appear to be genetically very similar to Atlantic H. nelsoni (Burreson et al. 2000; Kern 1998). Crassostrea gigas, tested in York River water, in quarantined flumes, did not contain detectable levels of H. nelsoni, indicating a high degree of resistance to the parasite (Barber 1996). Some unofficial introductions of C. gigas are known to have occurred in the 1950's and 60's, but no reproduction is known to have occured, and no existing populations are known (Andrews 1980; Gottelieb and Schweighofer 1996). Official plantings of fertile C. gigas in Bay waters have not occurred and are the subject of intense debate (Gottelieb and Schweighofer 1996; Terlizzi 1996).
In trials in VA in 1998-1999, and in 2005-2006 C. ariakensis showed no detectable infection, or very rare infections with H. nelsoni (Calvo et al. 2001; Kingsley-Smith et al. 2009). The occurrence of H. nelsoni or other parasites in this oyster, in its native range, or elsewhere, appears to be unknown. As with C. gigas, proposed experimental plantings of C. ariakensis have generated intense disagreements (Hallerman et al. 2001). After a long process of research, trails with triploid oysters, and risk-assessment modelling, the Army Corps of Engineers, and the states of Maryland and Virginia, decided prohibit introduction of diploid C. ariakensis, end cultivation of triploids in open waters, and instead transfer resources to restoration of the native Eastern Oyster (Fahrenthold 2009; Wheeler 2009). (See the species account for Crassostrea ariakensis).
Competition - We consider Perkinsus marinus (Dermo) to be cryptogenic in Chesapeake Bay. This species can be considered a competitor with H. nelsoni, since both parasites can kill oysters, depriving the other of hosts. P. marinus is now found from the Gulf of Mexico north to Cape Cod MA (Ford 1996), and occurs at salinities above 10 ppt (Ford and Tripp 1996). During the onset of the H. nelsoni epizootic in the lower York River, 'Dermo' infections were rare because oyster populations had become too sparse to support the epidemic (Andrews and Wood 1967). P. marinus requires dense populations and high temperatures to produce epizootics (Andrews 1967). Intensifications of P. marinus infections in the 1980's and 1990's are likely to have affected the extent of mortality due to H. nelsoni (Haskin and Andrews 1988). Oysters have evolved some resistance to each parasite, but the existence of two major parasites (H. nelsoni; P. marinus) in Chesapeake Bay, and the probable evolution of the parasites themselves means that complex interactions are likely.
Habitat Change - Since reduction of oyster biomass is likely to have far-reaching effects on habitat and foodwebs (Kennedy 1996), introduced and cryptogenic species are likely to be affected as well. Infaunal filtering species such as Rangia cuneata could benefit by increased phytoplankton biomass, while fouling species, such as Garveia franciscana, Cordylophora caspia, Haliplanella lineata, and others, could suffer from the loss of hard substrate, even while benefitting from increased phyto- and zoo- plankton abundance. In the absence of long-term monitoring of these organisms, population effects on exotic biota, due to H. nelsoni or other oyster diseases remain speculative.
References - Andrews 1967; Andrews 1980; Andrews 1984; Andrews and Wood 1967; Barber 1996; Burreson et al. 2000; Calvo et al. 2001; Ford 1996; Ford and Tripp 1996; Friedman 1996; Gottelieb and Schweighofer 1996; Haskin and Andrews 1988; Katkansky and Warner 1972; Kennedy 1996; Kern 1976b; Kern 1998; Terlizzi 1996;
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