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QPX, a Thraustochytrid Disease of Clams

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Category

Category 2 (in Canada and of regional concern)

Common, generally accepted names of the organism or disease agent

Quahog Parasite Unknown (QPX), Chytrid-like disease.

Scientific name or taxonomic affiliation

The organism associated with mass mortalities in the clam Mercenaria mercenaria since the 1960s and known as QPX (Quahog Parasite X) (Whyte et al. 1994) was recently named Mucochytrium quahogii (Geraci-Yee et al. 2021). Mucochytrium quahogii was identified as a new genus and species of an unusual thraustochytrid in the family Thraustochytriaceae, order Thraustochytriales, class Labyrinthulomycetes and division (or phylum) Stramenopiles (Geraci-Yee et al. 2021). This affiliation was confirmed by analysis of the gene sequence of the18S rDNA component of the small-subunit ribosomal DNA (Ragan et al. 2000, Stokes et al. 2002, Geraci-Yee et al. 2021). Like other species of Labyrinthulomycetes, M. quahogii produces biflagellated zoospores (Geraci-Yee et al. 2021). Because Whyte et al. (1994) depicted a sagenogenetosome-like structure and Kleinschuster et al. (1998) reported the development of an ectoplasmic net (EN) in cultured QPX that had been transferred to sterile seawater, the inclusion of QPX with the Labyrinthulomycetes was supported. However, Smolowitz (2018), Maas et al. (1999) and Geraci-Yee et al. (2021) indicated that a sagenogenetosome (bothrosomes) or production of EN have not been observed by others. Nevertheless, all 3 stages of the described QPX lifecycle produce copious mucus, also referred to as mucofilamentous-nets, which is a unique characteristic of QPX (Kleinschuster et al. 1998, Smolowitz 2018, Smolowitz et al. 1998, Geraci-Yee et al. 2021). Maas et al. (1999) suggested that QPX was a primitive member of the class because of the absence of typical sagenogenetosomes (sagenogens) and ectoplasmic nets in the clam host. In the following text, the common name of M. quahogii, QPX, will be used because prior to 2021 this was the identity of this thraustochytrid pathogen of M. mercenaria.

Geographic distribution

Initially reported from wild and hatchery stocks of Mercenaria mercenaria (commonly called quahog (quagaug) or hard clam) in the Gulf of St. Lawrence, Canada (Drinnan and Henderson 1962-63, Whyte et al. 1994). Currently, QPX is reported in New Brunswick, Nova Scotia and Prince Edward Island, Canada (MacCallum and McGladdery 2000), and in Massachusetts, Connecticut, Rhode Island, New Jersey, New York and Virginia, USA (Smolowitz 2018). In Virginia, QPX was not found in M. mercenaria from Chesapeake Bay but was present in cultured M. mercenaria from 3 coastal embayments (Ragone Calvo et al. 1998). In Connecticut, QPX was not considered to pose a threat to the hard clam (M. mercenaria) industry because of low prevalence (0.3% in 2358 clams from 77 different samples from along the shoreline monitored over a period of about 8 years) (Sunila 2006). QPX was identified once in 1 M. mercenaria from a culture site in Rhode Island (Lyons et al. 2007) but hard clams are no longer cultured there and no further monitoring has occurred in that area (Smolowitz 2018). Lyons et al. (2007) found no latitudinal gradient in QPX prevalence or frequency over its geographic distribution and suggested that local factors were important in determining its distribution. A morphologically similar parasite was reported from Ruditapes decussatus from Portugal (Azevedo and Corral 1997).

Host species

Known molluscan hosts are Mercenaria mercenaria and Mercenaria mercenaria variety notata. Results of investigations by Ford et al. (2002), Ragone Calvo and Burreson (2002), Ragone Calvo et al. (2007), Smolowitz et al. (2008), Perrigault and Allam (2009) and Wang et al. (2016a) indicate that different strains of M. mercenaria varied in their susceptibility to infection, disease and mortalities caused by QPX. Mercenaria mercenaria stocks/strains from southern parts of the USA Atlantic coast (e.g., Florida) were more susceptible than those from more northern areas (e.g., Massachusetts and New York).

Impact on the host

Quahog Parasite Unknown (QPX), referred to as a facultative pathogen by Smolowitz (2018) and Geraci-Yee et al. (2021), has been associated with mass mortalities of cultured and wild M. mercenaria in Maritime Canada (Whyte et al. 1994, Ragan et al. 2000) and along the northeastern coast of the United States (Ragone Calvo et al. 1998, Smolowitz et al. 1998, Ford et al. 2002, Dove et al. 2004, Perrigault and Allam 2009). In Canada, QPX was suggested to be the primary cause of significant wild quahog stock mortalities in New Brunswick between 1959 and 1962 but no mortalities attributed to QPX have occurred in wild stocks in Atlantic Canada since that time (Bacon et al. 1999, MacCallum and McGladdery 2000). However, QPX was again encountered in Canada during the early 1990s in moribund quahogs being conditioned for spawning in a hatchery. In that case, QPX was associated with 80-90% mortalities in juvenile M. mercenaria (up to 30 mm in shell length) in a nursery and up to 100% in hatchery broodstock on Prince Edward Island (Whyte et al. 1994, Bacon et al. 1999). In the United States, QPX appears to be most prevalent in cultured M. mercenaria being held in the hatchery, nursery or during grow-out or occasionally in densely set natural populations. Specifically, QPX has caused severe mortality (80 to 95% in some instances) in aquacultured M. mercenaria stocks in Massachusetts (Fraser 1996, Smolowitz and Leavitt 1997, Smolowitz et al. 1998, Walton et al. 2008b), New Jersey (Ford et al. 2002) and the eastern coast of Virginia (Ragone Calvo and Burreson 2002). In the summer of 2002, QPX emerged as a severe threat to the M. mercenaria fishery, causing significant quahog mortalities in New York waters. However, QPX has also been observed in apparently healthy wild adult populations from Atlantic Canada and at some locations in Virginia (McGladdery et al. 1993; Ragone Calvo et al. 1997, 1998).

QPX appears to be widely distributed in the marine environment on the east coast of North America. It has been detected in almost all different types of environmental samples (water, sediment, algae, invertebrates, detritus) and in marine aggregates (i.e., marine snow) especially from coastal areas experiencing repeated disease outbreaks (Lyons et al. 2005; Liu et al. 2008; Gast et al. 2008a, b; Geraci-Yee et al. (2021). Liu et al. (2008) suggested that sediments represent a natural reservoir for the parasite. Also, the occurrence of QPX-laden aggregates (i.e., marine snow) suggests a means for the spread and survival of pathogens between epizootics and provides a specific target for environmental monitoring of QPX (Lyons et al. 2005, Smolowitz 2018). Laboratory studies indicate that QPX has a direct life cycle and QPX was directly transmitted between quahogs within 3 months of exposure (Smolowitz et al. 2001). In the field, the mantle tissues were the first tissues infected and at some locations, the infections was found only in the mantle of many M. mercenaria (Smolowitz 2018). In some of these clams, the gills were also infected and Smolowitz (2018) surmised that QPX then gained access to the open vascular system and spread to other parts of the body. The most common sites of proliferation were in the vascular spaces surrounding the intestines and gonads but proliferation also occurred in the lumens of other areas of the body including the pericardial sac, foot, kidney and gonadal tubule (Smolowitz et al. 1998, Dove et al. 2004).

Smolowitz et al. (1998) reported that QPX-infected M. mercenaria grew more slowly and had a lower condition index than uninfected quahogs. QPX disease in M. mercenaria disrupts the connective tissue throughout the body and is associated with gross lesions (swellings and nodules) in the mantle of infected quahogs. Necrotic haemocytes indicate the possible production of a toxic substance with lytic activity. The in vitro cytotoxic effects of QPX on haemocytes from M. mercenaria matched the pathogenicity of QPX in quahogs (Perrigault and Allam 2008, 2009). Aggregations of QPX vegetative stages in vivo are usually surrounded by clear zones (mucoid substance). The mucoid material produced by QPX resists host antimicrobial activity that occurs in filter-sterilized M. mercenaria plasma (Perrigault et al. 2008a, b) and may prevent phagocytosis by quahog haemocytes. Thus, the mucoid secretions of QPX may represent an important virulence factor (Anderson et al. 2003).

While many aspects of the basic biology and epizootiology of QPX disease are still unknown, observations suggest that genetic variability in the QPX pathogen and/or in the host could be responsible for differences in susceptibility toward the infection and in the presentation of the disease (Ragone Calvo and Burreson 2002; Ragone Calvo et al. 2003a, b, 2007; Camara et al. 2004; Dahl et al. 2008; Burge et al. 2013). In vivo investigations have shown that different QPX isolates display varying levels of pathogenicity toward hard clams. For example, QPX isolated from infected New York clams appeared more virulent than the QPX isolated from infected Massachusetts clams (Dahl et al. 2008). QPX produces virulence factors that are cytotoxic to M. mercenaria haemocytes. This cytotoxicity appears to be induced by quahog factors, suggesting that it may play an important role in supporting QPX infection and proliferation within the host. Moreover, application of this information to different QPX isolates and quahog broodstocks indicates variations of QPX cytotoxicity in agreement with previous in vivo experiments, strengthening the existence of different QPX strains (Perrigault and Allam. 2009). Similarly, field investigations and laboratory transmission studies revealed some variations in the susceptibility of different quahog stocks to QPX infection. Specifically, host genetic makeup has been clearly shown to be associated with clam susceptibility, as both field (Ford et al. 2002, Ragone Calvo et al. 2007, Kraeuter et al. 2011) and laboratory (Dahl et al. 2008, Wang et al. 2016a) experiments have demonstrated higher susceptibility toward QPX of southern quahog strains (originating from Virginia, South Carolina and Florida) as compared to northern strains (Massachusetts, New York and New Jersey). Perrigault and Allam (2012) and Wang et al. (2016a) reported differences in the immune responses between northern (New York and Massachusetts) and southern (Florida) stocks of M. mercenaria and suggested that these differences may be linked to the resistance or susceptibility of different quahog stocks to infection by QPX.

Mortality caused by QPX seems to be most severe in the spring and summer months in M. mercenaria at least 1 year old in the eastern USA and mortality outbreaks often occur in the summer (Smolowitz et al. 1998, Dove et al. 2004). For example, Liu et al. (2008, 2017) reported that the prevalence of QPX disease in quahogs in Raritan Bay, New York, increased during the spring and summer, peaked in August and declined in the fall. However, in a more detailed report, Liu et al. (2017) indicated that 2 of 3 sites showed this seasonal pattern but the third site the highest prevalence and intensity of QPX occurred in the spring where the overall prevalence was generally low. Also, from a compilation of published reports, Lyons et al. (2007) found that QPX infections occurred throughout the year with no discernable seasonal trends in the prevalence or frequency of disease. Ragone Calvo et al. (2007) and Kraeuter et al. (2011) also detected no clear seasonal pattern in disease development in different quahog strains planted in experimental plots in Massachusetts, New Jersey and Virginia. In addition to possible seasonal affects, other environmental parameters, such as blooms of harmful alga (e.g., Prorocentrum minimum), effect the immune response of M. mercenaria infected by QPX (Hégaret et al. 2010). Kraeuter et al. (2011) indicated that although M. mercenaria mortality was correlated with QPX levels, mortality was considerably higher than infection prevalence would indicate, suggesting that strain interactions with stressful environmental conditions or unidentified factors may also be involved in mortality.

Perrigault et al. (2010) used in vitro isolates of QPX to determine that significant difference in temperature optima occurred for geographically distinct isolates confirming the existence of different strains or ecotypes and that in vitro QPX was able to survive extreme temperatures (-12 to 32 °C) suggesting that QPX could survive extreme conditions in the field. In vitro grown QPX were also used by Rubin et al. (2015, 2016) to characterise the extracellular proteins of QPX. They identified the overexpression of 6 of these proteins in infected M. mercenaria tissues suggesting that they were involved in the interaction with the quahog host (Rubin et al. 2015). The peptidases secreted by QPX were identified and characterised and 1 (a subtilisin-type serine peptidase) was able to digest quahog plasma proteins with possible involvement in the disease process (Rubin et al. 2016). The results of both studies revealed good candidates for further investigations as possible virulence factors of QPX (Rubin et al. 2015, 2016). Bassim and Allam (2018) used transcriptome-wide single-nucleotide polymorphism (SNP) analysis of 4 QPX isolates cultured from infected quahogs collected from disparate locations along the northeastern United States. They indicated that the genomic variants detected could explain differences in disease prevalence noted in the different regions and supported views that this opportunistic parasite might be able to adapt to varying environmental conditions (Bassim and Allam 2018).

The constitutive defenses of M. mercinaria and their response to QPX are impacted by temperature with lower temperatures (e.g., 13 ºC) favouring disease development and warmer temperatures (21 and 27 ºC for 2 to 4 months) associated with healing and better resistance to infection (Dahl et al. 2011, Perrigault et al. 2011). Consequently, QPX disease is considered a cold water disease and has never been documented south of Virginia (Burge et al. 2013, Rubin et al. 2014). Higher mortality rates observed in the summer could be attributed to the chronic nature of QPX diseases, and various environmental parameters, with summer mortalities being the end point of an infectious process that developed weeks or months prior to death (Perrigault et al. 2011). Transcriptome characterisation identified temperature-induced differential gene expression in QPX associated with several virulence-related factors that were up-regulated at low temperature demonstrating the ability of QPX to cope with environmental temperatures considered to be suboptimal for quahog immunity (low temperature) thereby providing a mechanistic scenario for high disease prevalence and intensity at low temperature (Rubin et al. 2014). Also, the immune response of M. mercenaria towards QPX were detected by gene expression studies. These investigations permitted the identification of candidate genes and pathways for further analyses of biological bases of clam resistance to QPX allowing for a better understanding of bivalve immunity in general (Perrigault et al. 2009b; Wang et al. 2016a, c).

Diagnostic techniques

Gross observations

Swellings and round yellow-tan nodules (1-5 mm in diameter) in the mantle, often at the mantle edge and close to or directly adjacent to the siphon or adductor muscle (Smolowitz 2018). The gills can also be infected. Other non-specific signs of infection include decrease in new shell growth, swollen, retracted, tan-coloured mantle edges, mucus and sand granules caught between the swollen mantle and shell edges and a high degree of chipping of the shell edge in quahogs from sandy locations (Smolowitz et al. 1998, Burge et al. 2013). No gross signs of QPX infection, including lack of nodules in the mantle, have been observed in infected M. mercenaria in Canada (MacCallum and McGladdery 2000).

Squash preparations

Vegetative cells within the nodules that may contain up to 40 daughter cells.

Histology

Abscesses or necrotic lesions containing various stages of vegetative and spore-like stages, commonly within halos of translucent (mucoid), non-staining, tissue usually observed in the mantle, gills and gonad (Smolowitz 2018). QPX has less frequently been detected in the connective tissue of the foot, labial palps, digestive gland, kidney, heart and adductor muscle. Dove et al. (2004) reported significantly larger numbers of parasites and higher biomass of QPX in visceral infections than in infections found only in the mantle. Three basic vegetative forms occur in the tissues: 1) thallus (trophozoite, single nucleated organism, 2-10 µm in diameter), 2) sporangium formed from a large thallus undergoing endosporulation - appears to lack a well-defined membrane bound nucleus (10-15 µm in diameter) and 3) mature sporangia (18 to 25 µm in diameter) containing 20 to 40 endospores (immature thalli, 1.5 to 2 µm in diameter) each with a basophilic cell wall (Smolowitz et al. 1998, Ragone Calvo et al. 1998, Dove et al. 2004, Burge et al. 2013). All stages have a basophilic cell wall that varies in thickness and staining intensity and are usually surrounded by a cell free zone up to 8 µm thick with mucoid staining properties. When numerous parasites are present in a focal lesion, large lucent (mucoid) areas free of host cells were formed (Ragone Calvo et al. 1998). In some cases, the cell free zones showed evidence of stellar, possibly cytoplasmic, extrusions (mucofilamentous net) from the vegetative stages. Phagocytic multinucleate giant inflammatory cells of various sizes and containing 3 to 25 nuclei within the cytoplasm and haemocyte encapsulation of QPX occur as part of the quahog response to infection (Smolowitz et al. 1998, Smolowitz 2018) The haemocytic response was often associated with moribund looking QPX (Ragone Calvo et al. 1998).

Figure 1. Abscess lesion (between arrows) caused by QPX between loops of the intestinal tract (i) within the gonad of Mercenaria mercenaria. Haematoxylin and eosin stain.

Figure 2. Accumulation of haemocytes (h) near the surface of mucoid-like material produced by thalli (trophozoites, t) and a sporangium (s) of QPX within the mantle of Mercenaria mercenaria. The thickness of the mucoid-like material around 1 thallus is indicated by a double headed arrow. Haematoxylin and eosin stain.

Electron microscopy

Thalli and immature sporangia contain electron-dense lipid bodies, mitochondria with tubular cristae, large vacuoles, perinuclear Golgi apparatus and additional membrane-bound inclusions containing dark lipid material. More mature sporangia contain multiple nuclei resulting from karyokinesis, which is followed by cytokinesis, resulting in endospore production in the sporangia (Maas et al. 1999). Maas et al. (1999) suggested that QPX is a more primitive member of the class Labyrinthulomycetes (referred to as phylum Labyrinthulomycota) because of the absence of typical sagenogenetosomes and ectoplasmic nets characteristic of most Labyrinthulomycetes. Sagenogenetosomes were not detected by Kleinchuster et al.(1998) nor Smolowitz et al. (1998). However, Whyte et al. (1994) illustrated a sagenogenetosome-like structure near the surface of a thallus. Smolowitz (2018) suggested that the QPX used for transmission electron microscopic examination by Whyte et al. (1994) may have been contaminated by a Labyrinthulomycota that did produce sagenogenetosomes. Nevertheless, scale-like laminated cell walls characteristic of the phylum were observed on some endospores and occasional thalli. Also, sporangia containing numerous nuclei, which occur as a result of mitosis and are difficult to see via light microscopy, were obvious in electron micrographs (Whyte et al. 1994).

Molecular Characteristics

Small subunit ribosomal DNA (SSU rDNA) sequences for several isolates of QPX have been deposited in GenBank (Ragone Calvo et al. 1998, Maas et al. 1999, Ragan et al. 2000, Stokes et al. 2002, Geraci-Yee et al. 2021). Polymerase chain reaction (PCR) primers specifically designed to amplify a 665 base pair segment of the SSU rDNA of QPX was able to detect QPX in infected quahog genomic DNA and did not amplify DNA of uninfected M. mercenaria nor DNA of other species of thraustochytrids that were tested (Stokes et al. 2001, 2002). This PCR assay was sufficiently sensitive to detect 20 fg QPX genomic DNA and 1 fg cloned QPX SSU rDNA. Field validation indicated that the PCR assay was equivalent to histological diagnosis if initially negative PCR products were reamplified (Stokes et al. 2002). The limited sensitivity of the PCR assay for this parasite may be attributed to the focal nature of infection (i.e., QPX is usually localised in the tissues of M. mercenaria and not dispersed throughout its host) thereby increasing the possibilities of sampling error. The PCR primers identified by Stokes et al. (2002) were used in a nested PCR protocol with products analysed by denaturing gradient gel electrophoresis (DGGE) (Lyons et al. 2005; Gast et al. 2006, 2008a). The PCR identification of QPX proved effective at detecting QPX and provided new and important information on potential exposure of quahogs to environmental sources of pathogenic organisms. However, this assay targeted the relatively conserved SSU rDNA region, limiting the differential specificity of the test because of the potential for cross-reaction with unidentified, related species. Subsequently, Lyons et al. (2006) and Liu et al. (2009) developed real-time quantitative polymerase chain reaction (qPCR) assays. Application of the assays demonstrated positive qPCR results from naturally contaminated environmental samples including marine aggregates (i.e., marine snow), quahog pseudofeces, sediment samples and haemocyte aggregation nodules from infected quahogs (Lyons et al. 2006; Liu et al. 2008, 2009; Fitzsimons-Diaz et al. 2008).

A cocktail of 2 DNA probes for QPX was used to detect the parasite by in situ hybridisation (ISH) and these probes did not hybridize with tissues of M. mercenaria nor with several other species of thraustochytrids that were tested (Stokes et al. 2002, Gast et al. 2008a). The ISH assay has been utilized to detect QPX in marine aggregates (i.e., marine snow), collected from coastal embayments in Cape Cod, Massachusetts, USA where QPX outbreaks have occurred (Lyons et al. 2005). Qian et al. (2007) were not able to detect significant molecular genetic variations between isolates of QPX from an outbreak in Raritan Bay, New York, from the original outbreak in Massachusetts and from another outbreaks in Massachusetts when they assessed regions of the ribosomal DNA (small subunit or 18S rDNA, ITS1, 5.8S rDNA and ITS2) and 4 regions of mitochondrial genes (fragments of coxI, cob, nad1 and nad7).

Garcia-Vadrenne et al. (2013) developed genomic and transcriptomic resources by characterising the partial genome of QPX and examined the influence of temperature on gene expression in order to provide a foundation for better understanding virulence, pathogenicity and life history of thraustochytrid pathogens.

Culture

QPX extracted from mantle tissue of infected M. mercenaria into sterile seawater containing antimicrobics were cultured in modified Eagle Minimum Essential Medium (MEM) supplemented with 10% heat-inactivated foetal bovine serum and antibiotics (Whyte et al. 1994, Kleinschuster et al. 1998, Geraci-Yee et al. 2021). All forms that were observed in infected M. mercenaria, developed in the cultures. As QPX proliferated in the culture media, it produced abundant mucoid material that bound the individuals together. Optimal culture conditions were a temperature of 22 °C, salinity of 28 ppt and pH 7 to 8 (Brothers et al. 2000). Upon transfer of the culture forms to sterile seawater, clusters of endospores adhered to the bottom of the culture flask and developed ectoplasmic nets (Kleinschuster et al. 1998). Whyte et al. (1994) and Kleinschuster et al. (1998) described the production of biflagellate zoospores developing in culture forms transferred to sterile seawater. Cultures of QPX examined by Brothers et al. (2000) did not produce zoospores on transfer to seawater. Smolowitz (2018) suggested that the zoospores may have resulted from contamination of the original isolates by another Labyrinthulomycota, which are known to be very common in the marine environment. However, Geraci-Yee et al. (2021) reaffirmed the previous descriptions of zoospore production by QPX in culture, in multiple strains from several geographic locations, and provided detail on how to maintain QPX cultures under conditions that promote the production of zoospores. In addition to zoospores, Geraci-Yee et al. (2021) described new aspects of the in vitro life cycle not previously observed.

Buggé and Allam (2005) developed a fluorometric microplate technique for the in vitro measurement of proliferation and viability of QPX. Ragan et al. (2000) indicated that MEM culture with subsequent confirmation by microscopy was more sensitive in detecting QPX than standard histological methods. However, MEM will support the growth of a range of morphologically similar marine thraustochytrids and thus, additional assays such as PCR (see above) must be applied to the cultured organisms to confirm identification.

In experimental trials, QPX from cultures and washed free of mucoid material were not infectious to quahogs by injection or bath exposure (Smolowitz et al. 2001) but infection could be achieved by using QPX cultured in sea water with macerated quahog tissue (Smolowitz et al. 2008). However, Dahl and Allam (2007) and Dahl et al. (2008) were able to infect M mercenaria in the laboratory by injecting QPX from laboratory maintained cultures into the pericardial cavity (83% infected 2 weeks post injection) and into the pallial cavity (18% infected 31 weeks post injection). Geraci-Yee et al. (2021) suggested the possibility that 1 of the new stages of M. quahogii that theydescribed may be responsible for infection and pathogenesis because many parasites commonly are known to have specific infective stages.

Cultures of QPX isolates have been used to investigate the interactions between M. mercenaria and this parasite. Perrigault et al. (2008a, b) used in vitro procedures to demonstrate that the plasma of QPX challenged M. mercenaria is able to alter the growth of QPX. The anti-QPX activities in plasma from M. mercenaria stocks that demonstrated higher inhibition of QPX in vivo also demonstrated more inhibition to growth in vitro (i.e., New York (resistant) quahogs) compared to plasma from more vulnerable stocks (i.e., Florida (susceptible) quahogs). Some M. mercenaria from resistant and susceptible stocks appeared to be deficient in inhibitory factors, suggesting that such animals may become more easily infected by the parasite (Perrigault et al. 2009a). Perrigault et al. (2009a) also determined that extracts from gills, mantle tissues and plasma of M. mercenaria inhibited in vitro QPX growth, whereas foot and adductor muscle extracts enhanced parasite growth. Alternately, QPX had variable in vitro cytotoxic effects on haemocytes from M. mercenaria, which matched well with their in vivo pathogenicity of the quahog stocks assayed (Perrigault and Allam 2008, 2009).

Methods of control

Avoid importing stocks carrying this organism into areas currently free of QPX. However, QPX appears to be a ubiquitous member of the normal marine and bivalve flora on the east coast of North America and M. mercenaria disadvantaged in some way (e.g., unfavourable genotype-environmental interactions or stocks imported from southern locations) may be more susceptible to infection. Thus, QPX may be an opportunistic facultative parasite not dependant on a parasitic way of life (Guo and Ford 2016). However, Perrigault et al.(2008d) reported that both salinity and temperature affect defense parameters and disease progression in M. mercenaria with higher QPX related mortalities occurring at higher salinities and lower temperatures. QPX may be limited to areas with salinities above 25 ppt (Ragone Calvo 1998). Perrigault et al. (2012) showed that salinity modulates quahog defense factors with higher QPX-associated mortality in infected quahogs maintained at high salinity. However, the impact of high salinity (30 practical salinity units (psu) nearly equivalent to parts per thousand (ppt)) appears secondary when compared to findings reported for temperature (Perrigault et al. 2012). Dahl et al. (2011) and Perrigault et al. (2011) demonstrated that lower temperatures (13 ºC as compared to 21 ºC or 27 ºC) corresponded to higher QPX disease prevalence and intensity, and higher mortality, in M. mercenaria. Wang et al. (2016b) determined that brief air exposures to moderately high temperatures (heat shock at 27–32 ºC for 2–4 h) promoted the greatest remission while imposing the mildest stress to quahogs there by enhancing resistance to the infection, promoting the healing process and minimizing the risk of loss due to disease outbreaks. Thus, temperature should be taken into account for the timing of activities involving the monitoring, movement (e.g., relays, transplants) or grow out (e.g., commercial culture, municipal enhancement) of quahogs in enzootic areas (Dahl et al. 2011). Dahl et al. (2010) provided evidence for the use of local wild broodstock to enhance the resistance of cultured strains of M. mercenaria to QPX. Overall, using locally produced quahogs may be advantageous because both host and QPX strain seem to play a role in the severity of infection and associated mortalities in areas where QPX infections are high (Burge et al. 2013).

Stress on cultured M. mercenaria associated with high planting densities and poor husbandry are believed to increase the risk of QPX disease problems (Ragone Calvo and Burreson 2002, Ford et al. 2002, Allam et al. 2005, Walton et al. 2008a). Lyons et al. (2007) reported a higher prevalence of QPX in M. mercenaria from cultured (farmed) beds than in wild populations with the highest prevalence in quahogs of intermediate size (20 to 55 mm in shell length). It may be possible to keep the incidence of disease under control through good plot husbandry and the removal of infected and dying quahogs (Gast et al. 2008a, b). In an extreme case with very high quahog mortalities associated with QPX, over 1 million quahogs were removed from culture beds in Wellfleet Harbour, Massachusetts during the winter which apparently prevented the spread of QPX disease (Walton et al. 2008b). Reduction of the stocking density was reported as effective in reducing mortalities to a negligible level. However, Kraeuter et al. (1998) reported no significant difference in the prevalence of QPX in juvenile M. mercenaria (<10 mm shell length) after 4 months at densities of up to 860 quahogs per square meter on intertidal and subtidal sites in New Jersey. Also, Ford et al. (2002) noted that although there was a significant trend towards higher QPX levels at higher planting densities, the considerable variability in the data made it difficult to determine the effect of density with a high degree of confidence. Smolowitz (2018) suggested that selection of increased pathogenicity, as identified in different clones of QPX, may occur within an aquaculture setting because naȉve animals are constantly being introduced into an infected area and may account, in part, for the severity of the disease in some areas. Possible disease management strategies include crop rotation between quahogs and oysters, rinse quahog seed in fresh water, which is lethal for QPX, and keep plots clear of seaweed (Powell 2005). The dynamics of infection and pathogenicity under different holding and handling conditions require more investigation to manage QPX proliferation in aquacultured M. mercenaria (MacCallum and McGladdery 2000).

Dalh and Allam (2016) determined that relocation of M. mercenaria was a potential strategy for QPX disease mitigation within an enzootic estuary. Their study consisted of relocating QPX infected M. mercenaria from enzootic areas to nearby sites with prevailing environmental conditions suggested to deter infection and favour remission and healing. Mercenaria mercenaria were collected from a location with consistent disease prevalence and brought to near shore habitats subject to lower salinities and higher summer temperatures. Other treatments included a reduced host density treatment and another of retaining clams above the sediment because sediments are suspected to represent a QPX reservoir. At the end of the 4-month study, all treatments displayed less QPX disease than the control group and the greatest contrast was provided by the disappearance of infections in a tidal creek (Dalh and Allam 2016). However, as indicated by Smolowitz (2018), there is danger in relocation if the new area does not have substantially higher temperatures and/or lower salinities than the original infected area because a potentially pathogenic isolate of QPX and QPX abundance in the environment may be increased in the new area with movement of infected clams.

Ford et al. (1997) concluded that hatchery produced seed are an unlikely source of QPX, based on results of extensive surveys of M. mercenaria from 13 different hatcheries in 6 states of the USA over a 3-year period. Because strains of M. mercenaria seem to vary in susceptibility to QPX disease, growers in enzootic areas should consider the geographic origin of quahog seed as an important component of their QPX disease avoidance/management strategies (Ford et al. 2002; Ragone Calvo and Burreson 2002; Ragone Calvo et al. 2003a, b, 2007; Dahl et al. 2008; Walton et al. 2008a). For example, QPX has been linked to quahog culture practices, including the use, in northern areas, of southern seed quahogs, which grow fast but are more susceptible to infection (Ragone Calvo et al. 2007, Guo and Ford 2016). Dahl et al. (2010) indicated that the higher susceptibility of southern strains of M. mercenaria to QPX could not be attributed to cooler (winter) water temperatures as an aggravating factor and that aquaculture practices such as the selection of fast-growing stocks may exacerbate QPX disease problems. However, the identification of genes and other molecular markers in M. mercenaria that are associated with resistance to QPX could be used as biomarkers for the selection of quahogs for the development of strains resistant to QPX (Perrigault et al. 2008a, c). Farhat et al. (2020) began the process of identifying genetic markers associated with M mercenaria resistance to QPX disease by identifying some molecular variants (single nucleotide polymorphism (SNP)) associated with clam survivorship thereby leading the way for the development of resistant clam stocks through marker-assisted selection.

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Citation information

Bower, S.M. (2021): Synopsis of Infectious Diseases and Parasites of Commercially Exploited Shellfish: QPX, a Thraustochytrid Disease of Clams.

Date last revised: March 2021

Comments to Susan Bower

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