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The regional spatial structure of parasites and pathologies in oysters and mussels in the United States: 16 years of mussel watch.

ABSTRACT The Mussel Watch Program sampled bays on the East, Gulf, and West coasts of the United States over a period of 16 y. Analytical protocols included the recording of parasites and pathologies. Oysters (Crassostrea virginica) harbored significantly more parasitic taxa than mussels (Mytilidae). Cases where body burden was higher in mytilids were exclusively eukaryotic parasites, trematode metacercariae and trematode sporocysts. Oysters had higher body burdens of Nematopsis, alimentary tract ciliates, prokaryotic inclusions, and a number of unique taxa including haplosporidians, Perkinsus marinus, cestodes, and nematodes. Major pathologies were much more common in mytilids. For oysters, many parasitic taxa were more common in the Gulf of Mexico, including Nematopsis, P. marinus. trematode sporocysts, and nematodes. For mytilids, most parasites and pathologies were more common on the East Coast. Most parasite distributions were clinal on the East and West coasts, with clear relationships to well-known provincial boundaries. West Coast mytilids and East Coast oysters showed a similar trend toward increased parasite weighted prevalence in the south. The greater body burdens in Gulf Coast oysters might be a continuation of this trend. East Coast mytilids offer an opposing trend with higher body burdens in the Gulf of Maine. An increasing incidence of pathologies in mytilids at northern latitudes on both coasts runs contrary to the antithetical trends on the two coasts for parasite weighted prevalences. Within the parasite-rich Gulf of Mexico, oysters from the Texas coast were notable for their higher parasite body burdens. Some parasites and pathologies tended to have low variance-to-mean ratios and thus be identified as having even distributional patterns. Others showed a large range of weighted prevalences within a region and thus had contagious distributional patterns. With the exception of P. marinus, most of the contagious parasites were single celled. The multicellular taxa were more uniformly distributed: they tended to have much lower variance-to-mean ratios. Likely, the difference in spatial distribution between single-celled and multicellular taxa is due to the tendency for single- celled organisms to proliferate within the host or, being small, the ability to accumulate in larger numbers within the host.

KEY WORDS: oyster, mussel. Mussel Watch, geographic distribution, parasitism, pathology, latitudinal distribution, Mytilus, Crassostrea

INTRODUCTION

A number of surveys of parasites and pathologies of substantial geographic extent have been carried out for selected bivalve species in selected regions (e.g., Burton 1961, Otto et al. 1979. Karatayev et al. 2000, Svardh & Johannesson 2002, Vazquez et al. 2006, Darriba et al. 2010, Erazo-Pagador 2010, Meyer et al. 2010). The NOAA Status and Trends Mussel Watch Program carried out a yearly survey of the parasites and pathologies of oysters and mussels from 1995 to 2010. Bivalves were sampled from each major coastal body of water from the Gulf of Maine to Washington state with additional sites in Puerto Rico, Alaska, Hawaii, and the Great Lakes. Sentinel bivalves included four Mytilus mussel species, two Dreissena mussel species, and the oyster Crassostrea virginica. This is the most comprehensive dataset of its kind and provides a unique opportunity to examine large-scale spatial trends in the prevalence and infection intensity of parasites and pathologies. Analyses of the earlier portions of this dataset are reported by Kim and Powell (2006, 2007) and Kim et al. (2008).

Provincial boundaries, determined primarily by the latitudinal temperature gradient (Engle & Summers 1999, Llanso et al. 2002, Rohde 2002), exert a material influence on the distributional patterns of parasites, even when host ranges cross provincial boundaries, as do the ranges of the principal Mussel Watch sentinel bivalves, as parasite ranges often are restricted in comparison with the range of their host (George-Nascimento 2000, Kruess & Tscharntke 2000, Rohde 2002). Within the geographic purview of Mussel Watch, according to Hall (1964), generally accepted major provinces are: Atlantic coast--mild temperate [Virginian--northern boundary at 41[degrees] N--Cape Cod (Bay 21)], outer tropical [Carolinian--northern boundary at 35[degrees]N--Cape Hatteras (Bay 48),] and inner tropical [Caribbean--northern boundary at 30[degrees] N--north of Cape Canaveral (Bay 56)]; Pacific coast - mild temperate [Oregonian--northern boundary at 48[degrees] N--Cape Flattery (Bay 115)] and warm temperate [Californian--northern boundary at 34[degrees] N--Point Conception (Bay 102)]. Valentine (1966) provided more detailed provincial and subprovincial boundaries on the West Coast including Puget Sound (Bays 116-121), Cape Mendocino (Bays 107-108), Monterey Bay (Bay 104), and Point Conception (Bay 102). Wilson et al. (1992) noted geographic boundaries in the Gulf of Mexico at Tampa Bay, FL (Bay 66), in the vicinity of the Mississippi River (Bays 77-78), and between Matagorda Bay and Aransas Bay, TX (Bays 89-91) (bay numbers are defined by Kim & Powell 2007).

The range and prevalence of parasites of Crassostrea virginica are often a product of the temperature and salinity regime within a bay, and their geographic distributions are often associated with these provincial boundaries (Kim & Powell 2007). In large measure, such boundaries are defined by the clinal change in temperature on the East and West coasts of the United States, but longitudinal trends defined in part by trends in precipitation can also play a role, particularly in the Gulf of Mexico. The geographic regions demarcated by provincial boundaries are influenced by climatic cycles that introduce periodic variations in temperature and precipitation, hence salinity. Foremost of these are the El Nino-Southern Oscillation (ENSO) and the North Atlantic Oscillation (NAO) (e.g., Douglas & Englehart 1981, Hurrell & van Loon 1997, Schmidt & Luther 2002, Notaro et al. 2006). The influence of these cycles has been documented for some bivalve parasites (Soniat et al. 2006, 2009). The Mussel Watch time series is of sufficient length to cover minimally two full cycles for the NAO and twice that for ENSO. Thus, the average distribution of parasites as it varies regionally should reveal longer term determinants of parasite distribution. The purpose of this study is to examine the long-term mean in weighted prevalence to identify regional trends that may be indicative of provincial boundaries or subprovincial processes producing foci of infection.

METHODS

Species Sampled and Sample Collection

The bivalve samples were collected annually from a network of sites along the U.S. coastline. Sampling targeted the largest animals at each site. Each sampled site subsequently was assigned to one of 126 bays [see Table 1 in Kim and Powell (2007) for details on the bays and their associated bay numbers]. A "bay," as termed herein, represents all sites in a single estuary, estuarine reach of a large estuary, or group of neighboring sites on an open coastline.

The introduced zebra mussel, Dreissena polymorpha, and quagga mussel, Dreissena bugensis, were sampled at sites in the Great Lakes (Bays 1-10) and the Hudson River (Bay 11). Rosenberg and Ludyanskiy (1994) discussed the taxonomy. Mussel Watch sites include all Great Lakes except Lake Superior (Lauenstein et al. 1997).

Mytilid mussel taxa were collected from the Northeast (Bays 12-36) and West (Bays 94-125) coasts, including Alaska. According to Hilbish et al. (2000), mussels collected on the East Coast were Mytilus edulis sensu stricto, as M. edulis is the predominant species from central Maine south (Rawson et al. 2001) to Cape Hatteras (Wells & Gray 1960), although the presence of Mytilus trossulus in the most northern collections cannot be excluded. On the West Coast, three mussel taxa were collected, Mytilus californianus and two species referable to the M. edulis complex, Mytilus galloprovincialis and M. trossulus. The mussel Mytilus californianus was collected at 31 sites among the 58 total West-coast sites. The mussel Mytilus trossulus was collected at the vast majority of the more northern stations from Oregon to Alaska. The mussel Mytilus galloprovincialis was introduced into the eastern Pacific in the 1880s and now occurs from central California to Baja California with some populations probably farther north (McDonald & Koehn 1988, Koehn 1991, Seed 1992), including a population in Puget Sound established at least by 1988 (Wonham 2004). Thus, M. galloprovincialis was collected at some California sites and may have been present in some Puget Sound collections. The continued uncertainty in the taxonomy of the remaining mytilids and the insufficient number of sampled bays where only one species was collected prevented subdivision of the M. edulis complex in statistical analysis.

Four oyster taxa were sampled, Crassostrea virginica, Crassostrea rhizophorae, Crassostrea gigas, and Dendostrea sandvichensis. The oyster Crassostrea virginica was sampled from coastal and estuarine areas of the Mid-Atlantic and Southeast coasts (Bays 37-61) and the Gulf of Mexico (Bays 63-93); C. rhizophorae was collected in Puerto Rico (Bay 62), and C. gigas and D. sandvichensis were collected in Hawaii (Bay 126). In total, however, C. virginica was collected at 55 of 57 bays where oysters were collected. The remaining two bays are excluded from the present analysis.

To simplify discussion when referring to groups of these taxa, the following inclusive terms will be used: dreissenid in reference to the combination of Dreissena bugensis and Dreissena polymorphic, mytilid for Mytilus edulis and the combination of Mytilus californianus. Mytilus galloprovincialis, and Mytilus trossulus on the West Coast; and M. edulis complex for the mytilid subset of M. galloprovincialis and M. trossulus on the West Coast.

Except in the Great Lakes, sampling occurred annually during winter with each site occupied within 30 days of an annual target date (O'Connor 1994). Sampling was done in winter to minimize the influence of gametogenesis and spawning on contaminant body burden (Jovanovich & Marion 1987, Ellis et al. 1993). Dreissenid mussels were collected in late August through September because the Great Lakes frequently are frozen over during winter. As a consequence of sampling program design, subsequent analyses may be biased for those parasites that exhibit a strong seasonal cycle of infection intensity (e.g., Wallet & Lambert 1986, Burreson & Ragone Calvo 1996, Ford et al. 1999).

Sample Preparation

Sample preparation is described by Kim et al. (2006a). For oysters, Perkinsus marinus was assayed by the more precise thioglycollate method by Ray (1966) following Powell and Ellis (1998). All other parasites and pathologies were scored microscopically for intensity either quantitatively or on a semiquantitative scale. Quantitative scores were used for parasites, pathologies, and selected morphological conditions, including prokaryotic inclusions (rickettsia. Chlamydia, etc.), ciliates, gregarines, nematodes, cestodes, and metacercariae of trematodes: each of these could be tallied individually following procedures described by Ellis et al. (1998) and Kim et al. (2006b). Ciliates were quantified by tissue type (viz., gill and alimentary canal), as were the gregarines (viz., body, gill, and mantle). Each nematode cross-section observed was counted, although a single individual may account for a number of tissue cross-section. Certain tissue pathologies and tissue components were also quantified by direct counts, including cases of hemocytic infiltration that were scored separately as focal and diffuse (Kim & Powell 2004), granulocytomas (Lowe & Moore 1979), and ceroid bodies (Mackin 1951, Stein & Mackin 1955; also termed brown cells by Zaroogian et al. 1993). Some parasites and morphological conditions, such as ramifying trematode sporocysts, the disease-producing protozoans, P. marinus and Haplosporidium nelsoni, and digestive gland atrophy, a condition known to be caused by a variety of stressors most likely related to poor nutrition (Palmer 1979, Winstead 1995, Kim & Powell 2004), were assigned to semiquantitative scales depending on the intensity or extensiveness of the affected area (Ellis et al. 1998, Ashton-Alcox et al. 2006, Kim et al. 2006b).

Statistical Analysis

Weighted prevalence was used to describe parasite/pathology occurrence in this study (e.g., Ford 1988, Kim & Powell 2004). Weighted prevalence is defined as the multiple of prevalence and infection intensity: weighted prevalence = prevalence x infection intensity, where prevalence, the fraction of individuals with the parasite or pathology, was calculated as prevalence = number of animals affected / number of animals analyzed and infection intensity, the average number of occurrences of a parasite or pathology in the affected individuals only, was calculated as infection intensity [n.summation over (i=1)] number of occurrences of parasite or pathology / number of animals affected. For conditions rated using semiquantitative scales, the scale rating replaced the number of occurrences in this last calculation. Weighted prevalence confounds prevalence and infection intensity and the latter two are not necessarily correlated, particularly for parasites that proliferate after transmission. That said, for many of the parasites under consideration here, prevalences were zero for many bays in some regions; thus, analyses of regional trends would perforce emphasize prevalence if a comprehensive analysis is wanted and this would dismiss any consideration of differences in infection intensity. For some other parasites, prevalence was nearly 100% over extensive regions; thus, analyses of regional trends would perforce emphasize infection intensity and this would then require comparisons across parasite categories to be made using a mixture of metrics. Consequently, we use the compromise of weighted prevalence as the metric for comparison.

The shear number of samples obtained yearly by the Mussel Watch program prevented detailed identification of most parasites. As a consequence, parasites were identified, tallied, and analyzed statistically by major taxon following the strategy adopted by Yevich and Barszcz (1983) in the first Mussel Watch program (Farrington et al. 1983). In addition, total parasite body burden was calculated as the sum of all quantified parasites; that is, all parasites not evaluated using a semiquantitative scale. These included, for mytilid taxa, the gregarines, ciliates, prokaryotic inclusions, trematode metacercariae, coccidians, copepods, xenomas [cells distended with numerous gill ciliates as described in Otto et al. (1979)], pinnotherid crabs, and other unidentified organisms; for oyster taxa, the gregarines. all ciliates, cestodes, nematodes, prokaryotic inclusions, trematode metacercariae, copepods, xenomas, pinnotherid crabs, and other unidentified organisms; and for dreissenid taxa, nematodes, trematode metacercariae, and other unidentified organisms. Because of the numerical dominance of the gregarines in oysters, a modified total parasite body burden was also calculated as the sum of the quantitative counts of the remaining parasite groups. A group of consistently rare parasites was tallied together for the convenience of analysis, but also because the distribution of rare species is inherently interesting (Laird 1961. Rabinowitz et al. 1986, Haukisalmi et al. 1988). This sum excluded common taxa such as gregarines, ciliates, nematodes, cestodes, and prokaryotic inclusions. Pathologies were grouped into major pathologies, including neoplasms, unusual digestive tubules, and gonadal abnormalities, and tissue pathologies, including focal and diffuse hemocytic infiltration and granulocytomas as described in Villalba et al. (1997). Taxon richness was the sum of the total number of different types of parasites observed in each bay.

Relationships between bays were examined in four ways. Bays were clustered using an unweighted pair-group method with Euclidean distance as the similarity index (Boesch 1977). Data were standardized to parts per hundred within each parasite/pathology category prior to analysis. A principal components analysis (PCA) was carried out using weighted prevalence standardized to a mean of 0 and a standard deviation of 1. PCA factor scores were used to visualize regional trends in parasite distributional patterns. PCA factor loads were used to examine the degree of co-occurrence of parasites. The tendency for a series of neighboring bays to have parasite weighted prevalences above or below the regional median was evaluated using a Wald-Wolfowitz runs test (Conover 1980). The distribution of parasite weighted prevalences among samples was evaluated using a statistic based on the variance-to-mean ratio, Elliott's d (Elliott 1977). This statistic permitted identification of contagious and even distributional patterns within the data independent of geographic location of the samples.

Analysis of variance (ANOVA) and analysis of covariance (ANCOVA) were used to determine the significance of differences in regional distribution. For ANCOVA, length was used as the covariate. Particularly in cases of counted parasites, length is a surrogate for histological section size, as larger animals, having larger cross-sectional areas, might contain more observable parasites simply by the size of the histological tissue section searched. Tukey's Studentized Range Test was used a posteriori to identify sources of significance within the ANOVA/ANCOVA when main effects were significant. A summary of statistical analyses is provided in Table 1.

For regional analyses, we established the following bay groupings. East Coast oyster bays were divided into three sections: Bays 56-61 (St. Johns River to Florida Bay), Bays 49-55 (Pamlico Sound south to Sapelo Sound), and Bays 39-48 (Delaware Bay to Pamlico Sound, north). These will be termed the Floridian, Southeast, and Mid-Atlantic regions henceforth. Gulf of Mexico bays were divided in two ways. The Eastern Gulf, Bays 63-77 (Pass-a-Loutre to the Everglades), was divided from the Western Gulf, Bays 78-93 (Tiger Pass to the Laguna Madre), at the Mississippi River. The Southern Gulf, Bays 88-93 (East Matagorda Bay to the Laguna Madre) and Bays 63-66 (Tampa Bay to the Everglades), was distinguished from the Northern Gulf, Bays 67-87 (Cedar Key to the Brazos River). East Coast mussel bays were separated into three groups about Cape Cod and the Hudson Canyon; from south to north, Bays 31-38 (Fire Island to Delaware Bay), Bays 23-30 (Narragansett Bay to Moriches Bay), and Bays 12-22 (Penobscot Bay to Buzzards Bay). These will be termed the Mid-Atlantic, Southern New England, and Gulf of Maine regions henceforth. On the West Coast, four groupings were selected: Bays 94-102 (San Diego Bay to Point Conception), Bays 103-112 (San Luis Obispo Bay to Tillamook Bay), Bays 113-122 (Columbia River to the Strait of Juan de Fuca including all of Puget Sound), and Bays 123-125 (Nahku Bay to Cook Inlet). These regions will be termed Southern California, Pacific Central, Pacific Northwest, and Alaska henceforth.

RESULTS

Collected Parasite Categories

A series of parasites were tallied by individual occurrence. Oysters carried significantly more parasites by this measure than mytilids or dreissenids which did not differ significantly (Fig. 1, Table 1); respective weighted prevalences were 46.2, 4.4, and 0.1. Mytilids on the East and West Coast did not differ significantly; respective weighted prevalences were 4.9 and 3.5. Gulf Coast oysters were significantly more heavily parasitized than East Coast oysters (P < 0.0001): weighted prevalences were 64.4 and 22.0, respectively. When groups of bays were combined based on anticipated provincial boundaries, for the mytilids, parasite load did not vary significantly among the three East Coast regions (from south to north: 2.94, 1.76, 5.07) or among most of the four West Coast regions where the most southerly region differed from the two most northerly regions significantly (weighted prevalences from south to north: 8.44, 3.97, 2.86, 0.71). In contrast, for oysters, parasite load was significantly higher in the Western Gulf than in the Eastern Gulf (96.3, 30.0, respectively) and significantly higher in the Southern Gulf than in the Northern Gulf (94.0, 47.9, respectively), but did not differ significantly between the Floridian, Southeast, and Mid-Atlantic coasts (27.3, 25.6, 17.1, respectively). A Wald-Wolfowitz runs test was significant for Gulf of Mexico oysters (P = 0.01), but not for oysters from the East Coast or for mytilids from the East or West coast. Thus, adjacent bays tended to be similar in the Gulf of Mexico by this measure. High parasite load in the Western Gulf was primarily responsible for the significant runs test for Gulf Coast oysters. Elliott's d was significantly positive for both taxa on both coasts; thus the distribution of parasite body burden was significantly contagious at the bay scale. Weighted prevalences were higher for Mytilus californianus than for the Mytilus edulis complex on the West Coast (6.4, 3.5, respectively), but this was due to the larger size of M. californianus rather than an inherently higher body burden. Thus, high values for weighted prevalence in mytilids from bays 100, 102, and 103 (Fig. 1) are due primarily to M. californianus being the target species in those bays and the higher value is due primarily to the larger size of M. californianus and thus the larger histological section size analyzed.

Much of the differential between regions is generated by the overwhelming abundance of Nematopsis spp. in oysters. When this parasite group is removed, mytilids and oysters did not differ significantly in weighted prevalence (3.2, 2.3, respectively), but both remained significantly higher than the dreissenids (Table 1, Fig. 2). Nematopsis spp. were observed in oysters and in West Coast mytilids. Revisiting the comparison between coasts after removing Nematopsis spp. shows that East Coast mytilids were more heavily parasitized by the remaining parasite groups than West Coast mytilids (3.5 versus 1.2). Weighted prevalence in Mytilus edulis was significantly higher in the Gulf of Maine than in Southern New England or the Mid-Atlantic which did not differ significantly (from south to north: 2.9. 1.8, 5.1). West Coast regions did not differ significantly (south to north: 0.69, 2.23, 1.82, 0.66). In addition, the significant difference between the M. edulis complex and Mytilus californianus on the West Coast no longer existed (1.7, 1.4, respectively). Excluding Nematopsis spp. for oysters reveals that the significant difference observed between East Coast and Gulf Coast oysters was due primarily to Nematopsis spp.: weighted prevalences excluding Nematopsis spp. did not differ significantly (3.8, 2.8, respectively). The significant difference in weighted prevalence between the Southern and Northern Gulf likewise disappeared (3.2, 2.0, respectively), as did the difference between the Western Gulf and the Eastern Gulf (2.6, 2.7, respectively), whereas the three East Coast regions remained nonsignificantly different (from south to north: 1.71, 3.04, 5.25, respectively). Thus, Nematopsis spp. were a dominant determinant of differentials in total parasite body burden among species and locations. Not surprisingly, no Wald-Wolfowitz runs test was significant for any species or coast. The distribution of weighted prevalence among bays, excluding Nematopsis spp., was significantly contagious for mytilids on the East and West coasts and for oysters on the East Coast, but not on the Gulf coast (Table 1; Elliott's d).

Rare parasites were relatively more abundant in only a few cases, but these cases were substantive (Table 1, Fig. 3). Weighted prevalence exceeded one in eight bays: four for East Coast mytilids, eastern Long Island Sound, Fire Island, Absecon Inlet, and Delaware Bay; two for oysters, Pensacola Bay and Laguna Madre; and two Mytilus californianus sites on the West Coast, Mission Bay and southern Puget Sound. Partly as a consequence, rare parasites were found significantly more often in East Coast mytilids than West Coast mytilids (0.64 versus 0.30) and more often in Gulf Coast than in East Coast oysters (0.32 versus 0.09). The Northern and Southern Gulf did not differ significantly (0.28, 0.39, respectively), nor did the Eastern Gulf and Western Gulf (0.25, 0.33, respectively) or the three East Coast oyster regions (from south to north: 0.06, 0.10, 0.11). Mid-Atlantic mytilids had significantly more rare parasites than mytilids from the Gulf of Maine or Southern New England (1.89 versus 0.15, 0.29). West Coast mytilids did not differ between regions (south to north: 0.46. 0.15, 0.37, 0.16). On the West Coast, M. californianus did not differ significantly from the Mytilus edulis complex (0.24. 0.36, respectively). No Wald-Wolfowitz runs test was significant; however, rare parasites were contagiously distributed among bays for mytilids on the East Coast and uniformly distributed for oysters on both the East and Gulf coasts. The distribution was statistically random on the West Coast.

Nematopsis

Nematopsis is a common and widespread parasite of oysters (Landau & Galtsoff 1951, Feng 1958, Fisher et al. 1996, Winstead et al. 2004) and found more sporadically, though occasionally in high infection intensities, in mytilid mussels (Lima et al. 2001, Tuntiwaranuruk et al. 2008). In this study. Nematopsis was occasionally found in West Coast mussels, but was dominantly a parasite of oysters (Fig. 4). Weighted prevalence was significantly higher in oysters from the Gulf coast than in oysters from the East Coast (61.6 versus 18.2; Table 1). Weighted prevalence was significantly higher in Southern Gulf oysters than in oysters from the Northern Gulf (92.0, 44.6). Weighted prevalence was particularly high in oysters from the southwestern Gulf (Table 1, Fig. 4); hence the Western Gulf differed significantly from the Eastern Gulf (93.7 versus 27.6). The three East Coast oyster regions did not differ significantly (from south to north: 25.6, 22.5, 11.9). On the West Coast, Nematopsis was found in both Mytilus californianus and the Mytilus edulis complex, but was much more common in M. californianus (5.0. 1.8). This difference, however, was a product of the influence of histological section size rather than an inherently higher body burden. Nonetheless, discounting this size differential, weighted prevalences still were significantly higher in Southern California (from south to north: 7.8, 1.7, 1.0, 0.1). Wald-Wolfowitz runs tests were not significant in any case; however, the distribution of Nematopsis spp. in oysters was strongly contagious between bays on both the East and Gulf coasts, so the parasite was regionally patchily distributed, but without much local coherence between bays.

We examined the body burden of Nematopsis spp. in three separate tissues, body, mantle, and gill, because Sprague (1949) and Sprague and Orr (1952, 1955) suggested that two different species (Nematopsis ostrearum and Nematopsis prytherchi) occur in Gulf oysters, and that N. prytherchi tend to concentrate in the gills (see also Winstead et al. 2004). Feng (1958) found N. ostrearum primarily in mantle tissue of East Coast oysters.

The weighted prevalence of Nematopsis in oyster body tissue did not differ between East Coast and Gulf Coast oysters (8.6, 6.4), nor was Nematopsis present in significantly higher numbers in the Northern or Southern Gulf (5.6, 7.8), the Eastern or Western Gulf (7.3, 6.8), or the three East Coast oyster regions (from south to north: 11.2, 7.9, 7.7; Table 1, Fig. 5). Nematopsis was significantly higher in the body tissue of mytilids collected in Southern California than other West Coast regions (from south to north: 3.25, 0.56, 0.27, 0.01). Nematopsis parasite body burdens were much higher in Mytilus californianus (2.0, 0.6); however, once again, weighted prevalence was primarily a function of the larger histological section size for this species. A Wald-Wolfowitz runs test was significant for oysters on the East Coast (P = 0.0171) and mussels on the West Coast (P = 0.0292). Both suggest increasing numbers in more southerly climes, perhaps explaining the nonsignificant result for the Gulf of Mexico, all sites of which would qualify as southern in this sense. Weighted prevalence for Nematopsis was contagiously distributed among bays in all regions where the parasite was found in the body tissue of mytilids and oysters.

Nematopsis in the mantle tissue of oysters occurred at higher weighted prevalence in the Gulf than on the East Coast (3.7, 2.6; Table 1, Fig. 6). The parasite was not more common in the Northern or Southern Gulf (3.5, 3.9, respectively), but was much more abundant in the Western Gulf than in the Eastern Gulf (5.7 versus 2.1), and particularly in the southwestern Gulf from Matagorda Bay south. The three East Coast oyster regions did not differ significantly (from south to north: 3.54, 3.14, 1.75). Nematopsis was more common in the mantle tissue of Mytilus californianus than in the Mytilus edulis complex (1.2, 0.4), but this differential was a function of histological section size. Once again, the parasite was significantly more common in Southern California (from south to north: 2.18, 0.32, 0.02, 0.00). A Wald-Wolfowitz runs test was significant for Gulf Coast oysters (P = 0.0104), East Coast oysters (P = 0.0201), and West Coast mytilids (P = 0.0016). Weighted prevalence for Nematopsis was contagiously distributed among bays in all regions where the parasite was found (Table 1; Elliott's d).

Nematopsis was much more abundant in the gill tissue of oysters in the Gulf of Mexico than on the East Coast (51.5, 7.0; Table 1, Fig. 7). Southern Gulf oysters were more heavily infected than Northern Gulf oysters (80.2 versus 35.5). Western Gulf oysters had significantly more Nematopsis than oysters from the Eastern Gulf (81.2 versus 17.7). The three East Coast oyster regions did not differ significantly (from south to north: 1.7, 3.1, 5.3). On the West Coast, the most southerly region had a significantly higher weighted prevalence (from south to north: 2.31, 0.87, 0.75, 0.04). The differential was partly confounded by the relatively larger number of bays with Mytilus californianus as the target mussel in the southern portion of the West Coast. Once again, M. californianus was more heavily infected than the Mytilus edulis complex (1.7, 0.8), but as with the other Nematopsis categories, this was primarily a function of the larger histological section size for M. californianus. The differential between Southern California and the remaining regions remained once the section-size differential was taken into account, however. A Wald-Wolfowitz runs test was significant for Gulf Coast oysters (P = 0.0088); not surprising given the large bias in infection intensity toward bays south of Galveston Bay on the Texas coast. Nematopsis in the gill tissue was contagiously distributed among bays for both East Coast and Gulf Coast oysters, as found for the other tissue categories (Elliott's d > 1.96), but weighted prevalence for Nematopsis in the gill tissue was significantly uniform in its distribution on the West Coast, largely due to its rarity on that coast.

Protozoa and Prokaryotic Inclusions

Ciliates in the alimentary canal, including gut and digestive gland, were primarily a parasite of oysters (Table 1, Fig. 8). Weighted prevalences did not differ significantly between oysters collected on the Gulf and East coasts (0.87, 1.48, respectively), nor did the Northern and Southern Gulf (1.20 versus 0.28) or the Eastern and Western Gulf (0.59 versus 0.98) differ significantly. In contrast, the three East Coast oyster regions differed with the Mid-Atlantic significantly higher than the Floridian region. The Southeast region fell in between (from south to north: 2.49, 0.90, 0.12). A Wald-Wolfowitz runs test was not significant for either coast, but weighted prevalence for ciliates in the alimentary canal was contagiously distributed among bays on both coasts (Table 1; Elliott's d).

Ciliates of the gill tissue were much more widely spread (Table 1, Fig. 9). Oysters and mytilids did not differ significantly in weighted prevalence (0.88 versus 1.17). Weighted prevalence in mytilids did not differ significantly between the East and West coasts (1.26,1.12, respectively). Mytilids from the Gulf of Maine differed significantly from those collected in the Mid-Atlantic with the Southern New England collections falling in between (from south to north: 0.75, 0.59, 2.01). On the West Coast, mytilids from central California had weighted prevalences significantly higher than Southern California mussels (1.90, 0.13, respectively), with the Pacific Northwest and Alaska (1.37, 0.47, respectively) falling in between; however, Mytilus californianus did not differ significantly from the Mytilus edulis complex (0.97 versus 1.26). Weighted prevalences in oysters did not differ significantly between the East and Gulf coasts (1.30 versus 0.56); however, Northern Gulf oysters harbored significantly higher numbers of gill ciliates than did those in the Southern Gulf (0.77, 0.18, respectively). Once again, weighted prevalences in oysters were highest in the Mid-Atlantic portion of the East Coast, but not significantly so relative to the southern regions (from south to north: 0.24, 0.65, 2.23). Oysters from the Eastern and Western Gulf did not differ significantly (0.61 versus 0.39). A Wald-Wolfowitz runs test was significant for East Coast mussels (P = 0.019) and East Coast oysters (P = 0.0083), in both cases due to a tendency for highest weighted prevalences to be found in the more northerly sites. Gill ciliates were present in higher numbers at most mussel sites north of Buzzards Bay and had increased weighted prevalence in oysters from the Chesapeake Bay. Weighted prevalence of gill ciliates was contagiously distributed among bays for East Coast oysters and West Coast mussels, but bay values were randomly distributed elsewhere.

Prokaryotic inclusions (Harshbarger et al. 1977, Elston 1986, Norton et al. 1993, Sun & Wu 2004) were observed nearly exclusively in oysters (Table 1, Fig. 10). Weighted prevalence did not differ significantly between oysters collected on the East and Gulf coasts (0.50 versus 0.44). The Northern and Southern Gulf did not differ significantly, although the mean values diverged considerably (0.54, 0.26, respectively). Prokaryotic inclusions were most common in oysters on the Southeast Coast, but this region did not differ significantly from the Mid-Atlantic and Floridian regions (from south to north: 0.51, 0.75, 0.36), nor did oysters differ significantly between the Western and Eastern Gulf in this respect (0.26 versus 0.59). Though rare in mytilids from all regions, Mytilus californianus had significantly higher counts of prokaryotic inclusions than members of the Mytilus edulis complex after taking into account the larger size of the former taxon. A Wald-Wolfowitz runs test was nonsignificant in the Gulf, but significant on the East Coast (P = 0.0201). Elliott's d was significantly negative on the Gulf coast, but not on the East Coast, indicating an even distribution of weighted prevalence values among bays on the Gulf coast.

Haplosporidians were found exclusively in oysters and nearly exclusively on the East Coast (0.11 versus 0.00 in the Gulf) with a strong bias north of Florida and significantly higher weighted prevalences in the southeast region relative to the Mid-Atlantic (from south to north: 0.00, 0.23,0.10; Table 1, Fig. 11). A Wald-Wolfowitz runs test was nonsignificant, but Elliott's d identified a significantly contagious distribution of weighted prevalence values among bays on the East Coast. The effective absence of haplosporidians in the Gulf of Mexico agrees with Ford et al. (2011). The higher weighted prevalence in the Southeast relative to the Mid-Atlantic is partly due to the low weighted prevalences at the Delaware Bay sites; oysters in Delaware Bay have developed significant immunity to Haplosporidium nelsoni, the most common haplosporidian (Munroe et al., 2015).

The parasite Perkinsus marinus was found exclusively in oysters and at nearly every site in the Gulf of Mexico and on the East Coast (Table 1, Fig. 12). Weighted prevalence was higher in the Gulf than on the East Coast (0.95 versus 0.58). The Northern and Southern Gulf did not differ significantly (0.91. 1.01, respectively), nor did the Eastern and Western Gulf (0.92, 0.99, respectively). The Mid-Atlantic and Southeast Coast differed significantly from the Florida region, however (from south to north: 0.98, 0.43, 0.49): this trend likely originates from the strong latitudinal temperature gradient coupled with the wintertime collecting schedule for Mussel Watch. No Wald-Wolfowitz runs test was significant. Elliott's d was significant for both the East and Gulf coasts and indicated a uniform distribution of weighted prevalence values among bays in both cases (Table 1).

Multicellular Eukaryotic Parasites

Trematode sporocysts of the genus Bucephalus and related genera are commonly observed in oysters (Tennent 1906, Menzel & Hopkins 1955, Hopkins 1957), but more rarely reported in mytilids (Calvo-Ugarteburu & McQuaid 1998a, 1998b). Bucephalus-like sporocysts were observed in mytilids and oysters in this study; weighted prevalence was significantly higher in mytilids (0.080 versus 0.019; Table 1, Fig. 13). East Coast mytilids were significantly more infected than West Coast mytilids (0.214 versus 0.005). Gulf Coast oysters were significantly more infected than East Coast oysters (0.026 versus 0.009). No East Coast region was unusually heavily infected for oysters (from south to north: 0.019, 0.009, 0.003). The Northern and Southern Gulf did not differ significantly (0.021, 0.034, respectively), nor did the Eastern and Western Gulf (0.021 versus 0.030). Weighted prevalence was higher in mytilids from Southern New England and the Mid-Atlantic than from the Gulf of Maine. Each region differed significantly from the others (from south to north: 0.475, 0.218, 0.058). West Coast regions did not differ significantly (from south to north: 0.000, 0.007, 0.003, 0.017). The Mytilus edulis complex and Mytilus californianus did not differ significantly on the West Coast (0.006 versus 0.004). A Wald-Wolfowitz runs test was nonsignificant for East- and Gulf Coast oysters and West Coast mytilids, but was significant for East Coast mytilids (P = 0.0004). Elliott's d was significant in every case, each indicating an even distribution of weighted prevalence values among bays.

Trematode metacercariae are frequent parasites of mytilids (Calvo-Ugarteburu & McQuaid 1998a, 1998b. Sunila et al. 2004, Aarab et al. 2011) and occasionally reported from oysters (Winstead & Couch 1981). In this study, trematode metacercariae were observed primarily in mytilids and rarely in oysters (0.606, 0.006, respectively; Table 1, Fig. 14). For oysters, trematode metacercariae were observed exclusively in bays of the Gulf of Mexico and the Floridian region of the East Coast. For mytilids, weighted prevalence was much higher on the East Coast (1.497 versus 0.045 on the West Coast). Weighted prevalence was significantly higher in the Gulf of Maine than elsewhere on the East Coast (2.898 versus from south to north: 0.189, 0.872). West Coast regions did not differ (from south to north: 0.003,0.032, 0.019, 0.012). No Wald-Wolfowitz runs test was significant. The distribution of trematode metacercariae was significantly contagious for East Coast mytilids, but weighted prevalences were randomly distributed on the West Coast (Table 1; Elliott's d).

Nematodes were observed in oysters and rarely in dreissenid mussels (Table 1, Fig. 15). Weighted prevalence was significantly higher in Gulf of Mexico oysters than for oysters collected on the East Coast (0.287 versus 0.056). Oysters from the Northern and Southern Gulf did not differ significantly (0.301, 0.260, respectively). Weighted prevalence was much higher in the Western Gulf than eastward (0.404 versus 0.153). The East Coast regions did not differ significantly (from south to north; 0.126, 0.002, 0.058). No Wald-Wolfowitz runs test was significant. Both the East Coast and Gulf Coast distributional patterns of weighted prevalence among bays were significantly uniform.

Cestodes are commonly reported in oysters (Little et al. 1969, Cake 1978, Winstead et al. 2004). In this study, cestodes were found only in oysters (Table 1. Fig. 16). The East and Gulf coasts did not differ significantly (0.356, 0.325, respectively). Most Gulf cestodes were observed in oysters from the Southern Gulf (0.666 versus 0.135 in the Northern Gulf), whereas the Eastern and Western Gulf did not differ (0.478, 0.235, respectively). On the East Coast, oysters from the Floridian and Southeastern bays harbored significantly more cestodes than oysters from the Mid-Atlantic (from south to north: 0.643, 0.642, 0.038). A Wald-Wolfowitz runs test was significant for both Gulf Coast and East Coast oysters (P = 0.0007, 0.0201, respectively). Elliott's d was not significant in either case.

Pathologies and Tissue Characteristics

Major pathologies recognized in the Mussel Watch program are described by Kim et al. (2006b) and Kim and Powell (2007). Major pathologies occurred much more often in mytilids than in oysters (0.478 versus 0.017). Though much lower overall than in mytilids, Gulf Coast oysters significantly exceeded East Coast oysters in the frequency of major pathologies (0.026. 0.004, respectively; Table 1, Fig. 17). Oysters from the Northern and Southern Gulf did not differ significantly (0.033, 0.015, respectively), nor did oysters from the Eastern and Western Gulf (0.025 versus 0.023). The three East Coast regions likewise did not differ significantly (from south to north: 0.012, 0.004, 0.000). East Coast mytilids did not differ significantly between regions (from south to north: 0.722, 0.894, 0.882). The most northerly region (Alaska) differed significantly from the most southerly region (Southern California) on the West Coast (0.619, 0.095, respectively) with the two central regions establishing a clinal trend from south to north (0.248, 0.429, respectively). Part of this trend was due to the significantly higher weighted prevalence in the Mytilus edulis complex relative to Mytilus californianus (0.415 versus 0.116). A Wald-Wolfowitz runs test was significant only for West Coast mytilids (P = 0.0031). Elliott's d indicated a significantly uniform distribution of weighted prevalence values among bays in all cases.

When tissue pathologies, mostly cases of hemocytic infiltration, are considered, mytilids and oysters did not differ significantly (0.440 versus 0.332; Table 1, Fig. 18). Occurrence rate was higher in East Coast mytilids than West Coast mytilids (0.890 versus 0.185). East Coast and Gulf Coast oysters did not differ (0.367, 0.306, respectively). The Northern and Southern Gulf did not differ (0.278 versus 0.355), nor did the Eastern and Western Gulf (0.283, 0.313, respectively). No regional differences were significant for oysters on the East Coast (from south to north: 0.240, 0.411, 0.400). Farther north, mytilids from the three East Coast regions did not differ significantly, although each region had weighted prevalences above those seen for oysters on either the East or Gulf coast (from south to north: 0.762, 0.800, 1.027). West Coast regions did not differ significantly (south to north: 0.284, 0.126, 0.157, 0.149). The Mytilus edulis complex and Mytilus califomianus did not differ significantly on the West Coast (0.194, 0.174, respectively). A Wald-Wolfowitz runs test was significant for East Coast oysters (P = 0.0171). Elliott's d indicated a significant uniform distribution of weighted prevalence values among bays for both species and all coasts.

Mackin (1951) noted that ceroid bodies increased in number with increasing infection intensity of Perkinsus marinus. Stein and Mackin (1955) also reported significantly more ceroid bodies in oysters heavily infected by P. marinus, as did Kim and Powell (2006). Kim and Powell (2006) also noted an association between Nematopsis and ceroid bodies in West Coast mytilids. Ceroid bodies were present in oysters and in all mytilid taxa sampled in this study and on all coasts, but weighted prevalence was much higher in oysters than in mytilids (87.4 versus 6.1; Table 1, Fig. 19). Gulf Coast oysters significantly exceeded East Coast oysters in weighted prevalence (96.0, 75.8, respectively). The Northern and Southern Gulf did not differ (92.1, 103.2, respectively), nor did the Eastern and Western Gulf (97.2, 103.5, respectively); however, the Floridian bays on the East Coast significantly exceeded the two northern regions in weighted prevalence (from south to north: 123.3, 45.5, 72.8). Though lower in weighted prevalence than oysters, ceroid bodies in East Coast mytilids numbered significantly higher than in West Coast mytilids (9.4 versus 4.2). Occurrence rate was higher among mytilids from the Gulf of Maine than for the remaining East Coast regions (from south to north: 2.5, 8.8, 13.8). West Coast regions did not differ significantly (south to north: 5.7, 3.9, 3.0, 4.1). The larger Mytilus califomianus significantly exceeded the Mytilus edulis complex on the West Coast (6.0 versus 2.6); this was partly but not completely due to the larger size of M. califomianus (ANOVA: species P = 0.0163; length P < 0.0001). A Wald-Wolfowitz runs test was significant for East Coast mussels (P = 0.046). Elliott's d showed a significantly contagious distribution for each species on each coast.

Digestive gland atrophy is a condition that may be a true pathology or that may simply indicate nutritional state (Palmer 1979, Widdows et al. 1982, Winstead 1995, Weis et al. 1995, Gold-Bouchot et al. 1995, Watermann et al. 2008). Digestive gland atrophy scores were similar for mytilids and oysters (2.49 versus 2.08) and for East Coast and West Coast mytilids (2.50 versus 2.48), but not for East Coast and Gulf Coast oysters that significantly differed (2.30, 1.93, respectively; Table 1, Fig. 20). Oysters from the Northern and Southern Gulf did not differ (1.88, 2.01, respectively), nor did oysters from the Eastern and Western Gulf (1.87, 2.03, respectively), but oysters from the Mid-Atlantic significantly exceeded their Southeast Coast and Floridian brethren in weighted prevalence (from south to north: 2.02, 2.04, 2.60). For mytilids, no West Coast region differed significantly (from south to north: 2.46, 2.48, 2.52, 2.39), but the Southern New England region differed significantly from the Gulf of Maine (from south to north: 2.59, 2.60, 2.38) on the East Coast. Though similar in score value, the Mytilus edulis complex significantly exceeded Mytilus californianus on the West Coast (2.55 versus 2.40). A Wald-Wolfowitz runs test was significant for East Coast oysters (P = 0.0011). Elliott's d indicated a significantly uniform distribution for the intensity of digestive gland atrophy among bays for both species and both coasts.

Oysters had many more different kinds of parasites than mytilids (7.1 versus 3.2; Table 1, Fig. 21). Mytilids did not differ in taxon richness between the East and West coasts (3.1, 3.3, respectively). Oysters did differ in parasite richness between the East and Gulf coasts (7.8, 6.2, respectively). Oysters did not differ between the Northern and Southern Gulf (7.6 versus 8.0) nor did they defer between the Eastern and Western Gulf (7.55 versus 7.54), but parasite richness varied significantly between the Mid-Atlantic, Southeast, and Floridian portions of the East Coast (from south to north: 6.2, 8.1, 5.0). Mussels in Southern California had a significantly more diverse fauna (4.5) than mussels farther north (remaining from south to north: 2.87, 2.60, 2.26). The East Coast regions where mytilids were collected did not differ significantly (north to south: 3.1, 2.4, 2.2). The Mytilus edulis complex and Mytilus californianus did not differ on the West Coast (3.2, 3.3, respectively). No Wald-Wolfowitz runs test was significant. Elliott's d indicated a significantly uniform distribution in species richness among bays for East Coast mussels and Gulf Coast oysters.

Cluster Analysis

Cluster analysis (Fig. 22) separated oysters from mussels with one exception. The Rappahannock River (Bay 44), an oyster site, clustered with a few mytilid sites primarily due to an impoverishment of cestodes, a scarcity of ciliates in the alimentary canal, a low infection intensity of Perkinsus marinus, and the near absence of Nematopsis at this site. Nenuttopsis was rare in mytilids and normally very abundant in oysters. Generally, obvious clusters of bays from which oysters were collected were differentiated at lower levels of similarity than obvious clusters of bays where mytilids were collected; that is, overall, mytilid bays were more similar more consistently than oyster bays.

Bays from which oysters were collected fell into three primary clusters. Most bays from the Cape Fear River (Bay 51) north excluding nearly all Chesapeake Bay sites fell into one cluster with the Cape Fear River to Chesapeake Bay mouth (Bay 46) locales being rather distinct from the remainder. Apalachee Bay (Bay 68) also fell into this group whereas Beaufort Inlet (Bay 50) did not. The cluster split into two subgroups, the lesser group representing the Cape Fear River, Pamlico Sound (Bays 48-49), and the Chesapeake Bay mouth tended to have fewer cestodes, fewer ciliates in the alimentary canal, high haplosporidian prevalence, and few Nematopsis relative to the sites in the larger subgroup (Delaware Bay to Savannah River in Fig. 22).

A second group of bays where oysters were collected included the Chesapeake Bay sites (Bays 41-43) and most sites from Breton Sound to Choctawhatchee Bay (Bays 71-76). These sites were characterized by few gill ciliates and limited numbers of Nematopsis. The Chesapeake Bay sites had fewer rare parasites and fewer prokaryotic inclusions; in addition haplosporidians were present.

The final oyster cluster encompassed most Gulf of Mexico bays plus Beaufort Inlet (Bay 50) and most of the Floridian bays on the East Coast. The Western Gulf was relatively distinct from the Eastern Gulf and the southern locales on the East Coast. Oysters from Western Gulf bays had increased body burdens of Nematopsis in the mantle tissue and particularly in the gill tissue, a lower body burden of ciliates in the gill, more nematodes, and fewer cestodes.

In most cases, bays from which oysters were collected fell into clusters oriented approximately north to south on the East Coast and east to west on the Gulf coast. Nevertheless, in two cases, a number of bays from disparate regions fell into the same cluster. Thus, most Chesapeake Bay sites fell into a cluster with bays in the northeastern Gulf and most of the remaining Gulf bays fell into a cluster with the southeastern Floridian bays. Nearly all bays west of the Mississippi River fell into one cluster with the exception of Laguna Madre (Bay 93) that clustered with the southern Floridian bays. The distinctive parasite fauna of oysters in these regions has not gone unremarked (Wilson et al. 1990, Kim & Powell 1998, 2006).

All locales where dreissenid mussels were collected clustered together, but the bays were relatively similar to a block of northwestern bays where mytilids were collected, including some Puget Sound sites and the Alaskan sites, primarily due to the rarity of parasites in dreissenids and the relative rarity of parasites in mytilid mussels from the Pacific Northwest and Alaska. West Coast sites fell into three primary groups, the aforementioned Puget Sound and Alaskan sites, the California sites, and the Oregon and Pacific coast of Washington sites. The latter two are differentiated by increased weighted prevalence of major pathologies in the north and increased weighted prevalence of Nematopsis in the south.

East Coast bays from which mytilids were collected fell principally into three groups. Most Long Island bays separated from the remainder due to high prevalences of trematode sporocysts, relatively low incidence of gill ciliates, a near absence of trematode metacercariae, and fewer ceroid bodies. Bays farther north fell into two groups, but unlike most other clusters, these were not defined well geographically. These bays separated based on the tendency for fewer trematode metacercariae to be associated with more gill ciliates and more trematode sporocysts.

DISCUSSION

Perspective

For this analysis, 16 y of data for sites sampled in a series of "bays" on the East, Gulf, and West coasts and the Great Lakes were averaged. For the most part, these "bays" were clearly demarcated estuaries or lagoons or subsections of large estuaries and lagoons. In a few cases, "bays" were stretches of open coastline. In most cases, a bay-average included not only a series of years, but multiple sites sampled within a bay. A few bays were characterized by only a single site. In many cases, bays were sampled every other year for part of the time series, so that the total number of years sampled numbered 8 or 9, rather than 16. Generally, neighboring bays were sampled in alternate years when alternate sampling was used. The fact that neighboring bays frequently clustered together indicates that this alternating sampling scheme did not materially influence the present analysis.

Regardless of these sampling idiosyncrasies, the dataset is temporally and regionally extensive. In this study, by summing over years and subsuming sites into "bays," we focus on major regional patterns. Of note is the fact that the time frame substantially exceeds most climatic cycles affecting the East, Gulf, and West coasts, particularly the NAO and ENSO, so that the patterns observed are those that remain strong despite substantial year-to-year variation imposed by climate change (e.g., Kim & Powell 1998, 2009).

The Major Taxa and Oceanic Trends

Zebra and quagga mussels had very few parasites, in keeping with their invasive origin (Conn et al. 1994, Kim & Powell 2007, see also Aguirre-Macedo & Kennedy 1999, Torchin et al. 2002, Marshall et al. 2003). As a consequence, these taxa were not included in statistical analyses. Oysters (Crassostrea virginica) harbored significantly more different kinds of parasitic taxa than mytilids. The few cases where the body burden of a parasitic taxon was higher in mytilids were exclusively eukaryotic parasites, the trematode metacercariae and trematode sporocysts. In comparison, oysters had overwhelmingly higher body burdens of Nematopsis, higher body burdens of ciliates in the alimentary tract, more prokaryotic inclusions, and a number of unique taxa or taxa exceedingly rare in mytilids including the haplosporidians, Perkinsus marinus, cestodes, and nematodes. In contrast, major pathologies were much more common in mytilids, whereas ceroid bodies were more common in oysters. The distinction between oysters and mytilids was sufficiently profound as to separate these taxa almost completely in cluster analysis. The infamy of diseases in oysters (Ford & Tripp 1996, Lafferty et al. 2015) compared with the limited accounts in mytilids and the opposite tendency related to pathologies such as neoplasms and gonadal abnormalities (e.g., Farley 1976, Elston et al. 1988, Kent et al. 1989, Figueras et al. 1991, Iglesias et al. 2012) is consistent with the significantly greater body burden, both in types of parasites and weighted prevalences, and the lesser incidence of major pathologies observed in oysters in this study.

Oysters were collected on the East Coast from Delaware Bay south and throughout the Gulf of Mexico. Many parasitic taxa were more common in the Gulf of Mexico. Few were more common on the East Coast. Only the haplosporidians were found on the East Coast more commonly and this is due to the nonnative Haplosporidium nelsoni that was introduced to the East Coast (Burreson et al. 2000, Burreson & Ford 2004). The distinction between these two regions included higher body burdens in the Gulf of Mexico for Nematopsis, Perkinsus marinus, trematode sporocysts, and nematodes. Rare parasites also occurred more commonly in Gulf Coast oysters. Major pathologies and ceroid bodies were also more common. For oysters, only digestive gland atrophy was more pronounced on the East Coast, likely due to the colder winters in the northern portion of the collection range where colder water inhibits feeding during the time of collection (Powell et al. 1997). For mytilids, with the exception of Nematopsis, parasitic taxa were more common on the East Coast. This trend was dominated by the trematodes, sporocysts and metacercariae. Pathologies were also more common on the East Coast, as were ceroid bodies.

Regional Trends in Distribution

To a large extent, the distribution of parasites was clinal on the East and West coasts, with clear relationships to well-known provincial boundaries. Thus, for East Coast mussels, for example, parasite body burdens were usually highest in the Gulf of Maine (e.g., gill ciliates, trematode metacercariae) or in the Mid-Atlantic (e.g., trematode sporocysts, rare parasites). In no case did the central region of southern New England stand out. The suggestion is that Southern New England is a mixing area between the Virginian and the Nova Scotian provinces and that this reduces parasite weighted prevalence in mytilids in this region. On the West Coast, a strong tendency existed for parasite body burdens to be higher in the south (e.g., Nematopsis, gill ciliates) and more taxa were found in the south; however, major pathologies were more common in the north. In no case was a parasite category more common in the north. The collection of multiple mytilid species potentially confounded this trend. In only one case, however, prokaryotic inclusions, did the two major taxa, Mytilus californianus and the Mytilus edulis complex, differ significantly enough to exceed the expectation of increased parasite counts imposed by the larger histological section size for M. californianus. Thus, the latitudinal gradient in body burden is not explained by the tendency for M. californianus to be more commonly collected in the south. On the other hand, major pathologies were more common in the M. edulis complex and this likely explains their greater frequency to the north.

For oysters, a few parasitic taxa occur in higher numbers in the south (e.g., cestodes, Perkinsus marinus), but only ciliates of the alimentary canal are more common to the north. Ceroid bodies are also more numerous to the south, whereas digestive gland atrophy is more pronounced in the north. This latter may be evidence of poorer nutrition during the colder winters in the Mid-Atlantic, a trend not unexpected by the midwinter time of sample collection. West Coast mytilids and East Coast oysters show a similar trend toward increased parasite weighted prevalence in the south and the greater body burdens in Gulf Coast oysters might be explained at least partially as a continuation of this trend.

East Coast mussels offer a very different picture. Mussel collections covered a wide latitudinal range on the West Coast and a much narrower range on the East Coast. Weighted prevalences of parasites tended to increase southward on the West Coast, a trend that would suggest lower weighted prevalences on the East Coast and particularly in the Gulf of Maine. In fact, frequently, the opposite trend was found. The most substantive comparison is the Pacific Northwest and Alaska with the Gulf of Maine, wherein the former two are characterized by relatively low body burdens and the latter by much higher ones. Interestingly, an increasing incidence of pathologies in the north runs parallel on both coasts, in contrast to the contrary trends on the two coasts for parasite weighted prevalences.

Cluster analysis agrees overall with the statistical evaluation. West Coast mytilids divided into three clusters. The southernmost cluster had its northern terminus in the Point Conception region, a known provincial boundary (Valentine 1966). The central cluster had its northern terminus in Washington state, another provincial boundary (Valentine 1966). On the East Coast, mytilid locations were also partitioned into three groups. The southernmost group had its northern terminus in the vicinity of Block Island. Cape Cod is a well-known provincial boundary (Gabriel 1992, Hutchins 1997, Engle & Summers 1999) that has degraded over recent decades with the warming of the Mid-Atlantic Bight (Ford 1996, Barber et al. 1997, Cook et al. 1998). Coincidentally, summer water temperatures change significantly in the vicinity of Cape Cod, but no such strong demarcation in temperature occurs during the winter (Hutchins 1997) when Mussel Watch sampling occurs, thereby possibly minimizing the importance of Cape Cod as a regional boundary during the winter. Nonetheless, the transitional nature of Southern New England remains clear in the tendency for weighted prevalences to be lower in this region than north and south.

East Coast oysters fell primarily into three groups. A southern group had its northern terminus in the vicinity of the St. John's River in Florida, near Cape Canaveral, a known provincial boundary (Engle & Summers 1999). The remaining two clusters accommodated most of the northern bays. A break at Cape Hatteras was not readily apparent. Whether this too is a sign of warming of the Mid-Atlantic Bight is an open question, although many Carolinian Province species are now found north of Cape Hatteras.

The Gulf of Mexico is interesting in that a division can be made between the Eastern and Western Gulf at the Mississippi River and the Northern and Southern Gulf at Tampa Bay and Aransas Bay (Wilson et al. 1990, 1992). Parasites were more common west and south; that is, the Texas coast was notable for its higher body burdens. The trend was dramatic for Nematopsis in the gill tissue and notable for Nematopsis in the mantle tissue. The more southerly trend for Nematopsis in the gill accrued from the notably high body burdens in the southwestern Gulf of Mexico. These two Nematopsis are very likely different species (Sprague & Orr 1952). Following the same trend were nematodes and cestodes. Cestodes were more common to the south in both the Eastern and Western Gulf, more prominently in the east. Nematodes were more common on the western side of the Gulf, both north and south. By contrast, only gill ciliates were more common in the north. The bias toward the south might be interpreted as the continuation of the clinal trend on both coasts toward increased body burdens at southern latitudes. But, the bias toward the Western Gulf is not so easily explained.

Cluster analysis provides some additional information for the Gulf of Mexico. The three clusters include a suite of bays in the Western Gulf, a set of bays in the Southeastern Gulf, and a set of bays in the Northeastern Gulf. The Laguna Madre falls within the Southeastern Gulf cluster, consistent with its southerly latitude. Both winter northers and the influence of ENSO on regional precipitation and salinity tend to generate southwest-northeast trends that place the Northeastern Gulf in a unique area climatologically. With the exception of gill ciliates, parasite body burdens tend to be lower here. The tendency then will be to generate significant differences between the Northern Gulf and Southern Gulf or between the Eastern and Western Gulf, depending on the body burden trends along the Eastern Gulf coast south of Cedar Key and on the western Gulf coast west of the Mississippi River.

Geographic Relationships

We applied a PCA analysis to further visualize these geographic patterns. The first 12 PCA factors explained 84% of the variation. With two exceptions, individual parasite categories loaded on separate PCA axes (Table 2). The exceptions were Nematopsis in the body and mantle tissue that loaded on Factor 1 and Nematopsis in the gill tissue and Perkinsus marinus that loaded on Factor 4. Sprague (1949) and Sprague and Orr (1952) suggested that the mantle and gill Nematopsis are separate species. Very likely the Nematopsis in the body tissue is the same species as found in the mantle, hence the observed joint occurrence of these two categories on Factor 1. Pathologies were associated with trematode sporocysts (Factor 3) and trematode metacercariae (Factor 5). In all other cases, individual categories stood alone on separate PCA axes.

We identified bays with factor scores exceeding 0.75 or falling below -0.75. The northern and southern stretches of the East Coast and the Eastern and Western Gulf coasts were characterized by collections of neighboring or regionally delimited bays supporting high factor scores for one or more factors. This was not true of the West Coast. Although cluster analysis showed coherent trends in similarity on the West Coast along latitudinal lines (Fig. 22), this degree of similarity was clearly of lesser strength than the strong East- and Gulf Coast signals in the Mussel Watch dataset. The mixing of different mytilid species may be partly responsible, but even contiguous locales such as the Puget Sound-Strait of Juan de Fuca region failed to show groupings with strong factor scoring. The differing species, mixture of open coastlines, presence of estuaries and fjords, and relatively sparse coverage given the latitudinal range all likely contribute to the insularity of parasite/pathology distributions on the West Coast.

Figures 23-25 show the distribution of bays with factor scores exceeding 0.75 or falling below -0.75 on the East and Gulf coasts. Bays scoring high on Factor 1, Nematopsis in the body and mantle tissue, cover much of the Gulf and Southeast coasts exclusive of southwestern Florida (Fig. 23). The distributional pattern is distinctive from that of Nematopsis in the gill tissue (Factor 4; Fig. 24). Only Gulf bays achieved high factor scores for the latter and all but two are west of the Mississippi River. The distribution of prokaryotic inclusions is similar to that of Nematopsis in the body and mantle tissue in that bays in the Northeastern Gulf and Southeast dominate the bays with high factor scores (Factor 7; Fig. 24). With a few exceptions, these bays are found between roughly 30[degrees]N and 32[degrees]N latitude on both coasts. Cestodes were observed over a broader latitudinal range on both the eastern and western coasts of Florida and northward on the East Coast to North Carolina (Factor 2; Fig. 23). Only the Laguna Madre among Western Gulf bays achieved a high Factor-2 score and this is consistent with this bay falling with the Floridian bays in cluster analysis. Thus, three groups of parasites were characterized by cross-Florida distributions with ranges extending northward on the East Coast and westward on the Gulf coast to some degree: prokaryotic inclusions, cestodes, and Nematopsis in the body and mantle tissue.

In contrast, bays with high Factor-6 scores (nematodes) were concentrated west of the Mississippi River in the Gulf of Mexico (Fig. 25), as were bays with high Factor-4 scores (Nematopsis in the gill tissue). The provincial boundary identified by the Mississippi River delta is obvious in the Gulf of Mexico, with a boundary in the Tampa Bay area being somewhat less well defined, although the distribution of Nematopsis in the mantle and body tissues is a good example of the Northern Gulf province north of Tampa Bay on the east and Corpus Christi Bay on the west. Thus the parasite-rich Gulf of Mexico contains taxa that fall into the Eastern/Western provincial categories and also the Northern/Southern provincial categories.

The Mid-Atlantic-Southeast distribution of the haplosporidians is well defined by Factor 9 (Fig. 24). In large measure, this is Haplosporidium nelsoni, although other species are likely represented (Stokes & Burreson 2001, Burreson & Ford 2004). This is the only parasite with this type of distribution; otherwise the provincial boundary at Cape Hatteras (Cerame-Vivas & Gray 1966, Briggs & Bowen 2012), though not well defined, is evidenced by a transition of important taxa from South Carolina to the Chesapeake Bay. Rare parasites are most common along the New Jersey coast (Factor 12; Fig. 25), with a few bays scattered near the range extremes along the Gulf and West coasts. All of the bays on the East and West coasts scoring high on Factor 12 are locations where mytilids were collected, so that mytilids dominate this factor type, but the two locales in the Gulf of Mexico belong to the oysters. Bays with high Factor-8 scores (ciliates in the alimentary canal) were interestingly confined to the two large Mid-Atlantic Bays, Delaware and Chesapeake (Fig. 24). In contrast to the latter, bays with high Factor-10 scores characterized by abundant ciliates in the gill tissue were scattered sporadically on the East and West coasts (Fig. 23), but all were in the northern portion of the latitudinal range. This distributional pattern was unusual in including oyster and mytilid sites and in having only a limited degree of regional coherency.

The remaining factor score-defined groups are centered in the northeast. Trematode sporocysts dominate the Mid-Atlantic and extend into the Gulf of Maine, characterizing a large fraction of mytilid sites south of New Hampshire (Factor 3; Fig. 23). Trematode metacercariae characterize the Gulf of Maine, with a southern extension approximated by the provincial boundary along the southern coast of Massachusetts (Factor 5; Fig. 24). The overlap of these two shows the rather fluid nature of the Cape Cod provincial boundary. Digestive gland atrophy was most consistently noted in the Mid-Atlantic region and, interestingly, included mytilid and oyster bays along this stretch of coast, making this condition relatively unique in that a regional consistency extended across a species collection boundary (Factor 11; Fig. 25). Note that a number of bays were characterized by extremely negative Factor 11 scores (Fig. 25). These were concentrated among the bays in the Gulf of Mexico and southeast coasts where oysters were collected and among the dreissenid sites. Warmer temperatures in the southern oyster bays at the time of collection likely resulted in improved nutrition and so lower digestive gland atrophy scores (Winstead 1995) and dreissenid mussels were collected during the late summer months when they are likely to be in better nutritional condition (Bielefeld 1991).

Thus, with few exceptions, bays fell into regional groupings based on their parasites. With few exceptions, these regional boundaries are known provincial boundaries. With few exceptions, the regional groups do not overlap or overlap only moderately, so that parasites are effectively independently distributed along the oyster's and mytilid's latitudinal/longitudinal ranges on the East and Gulf coasts. The distributional pattern on the West Coast is dramatically different, being characterized by sporadic hot spots of local size, rather than regional continuity. These groupings also drive the cluster analysis which, however, does identify weak clinal linkages on the West Coast not obvious in the PCA and these are supported statistically by ANCOVA.

With few exceptions, parasites characterized by significant Wald-Wolfowitz runs tests (Table 1) also showed coherent patterns in the PCA analyses (Figs. 23-25). Most of the exceptions were for West Coast mussels, where some runs tests were significant, indicating a degree of regional coherency and agreeing with the tendency for West Coast bays to cluster clinally, but which failed to generate a strong enough signal to be identified in PCA. Nonetheless, for many of the dominant parasite types, distributional patterns exhibited regional coherency in the tendency for neighboring bays to be more similar in weighted prevalence than expected by chance and this was manifested by significant runs tests and similarly high PCA factor scores.

Local Effects

Some bays showed unusually high levels of certain parasites, but were sited remotely from the majority of such bays, or fell into a group of bays not obviously the result of larger scale latitudinal or longitudinal (in the Gulf of Mexico case) trends. The Laguna Madre was the only bay in the western Gulf with high cestode numbers (Factor 2; Fig. 23), even though such bays spanned the latitudinal range in the eastern Gulf. One probable reason for this singularity is the extended stretch of south Texas coastline encompassing the region around Baffin Bay without Mussel Watch sites. This hypersaline bay (Morse et al. 1992) and the surrounding Laguna Madre (Hedgpeth 1947, Parker 1959) do not provide habitat for oysters. Thus, only a single site exists that is comparable to the southwestern Floridian sites south of Tampa Bay.

Gill ciliates were sporadically distributed, but occasional bays had high numbers (Factor 10; Fig. 23). These include Boston Harbor and the Choptank River area of Chesapeake Bay. Nematodes were unusually common in oysters from the Choptank River area of the Chesapeake Bay and from Florida Bay, while routinely present in higher weighted prevalences in oysters from the Western Gulf. Rare parasites occurred prominently in oysters from two disparate locations in the Gulf of Mexico, Pensacola Bay and the Laguna Madre. These occurrences are in stark contrast to the regional coherency that dominated distributional patterns on the East and Gulf coasts.

Cluster analysis also revealed some unusual groupings. Santa Catalina Island (Bay 97), Monterey Bay (Bay 104), and Point St. George (Bay 109) clustered with the dreissenid sites. Mytilids from these three bays had relatively low weighted prevalences and few parasitic taxa and, in these respects, were similar to that routinely encountered for the dreissenids. The Rappahannock River (Bay 44), a bay where oysters were collected, clustered with a group of West Coast bays where mytilids were collected. The Rappahannock River was unusual for an oyster site in having low-weighted prevalences for all parasite categories, including Perkinsus marinus. Florida Bay (Bay 61) was another oyster collection locale that fell within a large group of bays wherein mytilids were collected. Florida Bay had a high Factor-6 score (nematodes) and a high Factor-2 score (cestodes), but low-weighted prevalences of Nematopsis, the former two being oyster traits and the latter being a trait more common to mytilids. Accordingly, Florida Bay clustered poorly with other bays and did not fit well with any sentinel taxon group.

An alternative approach to evaluate distributional patterns is to examine the tendency for a set of samples to provide similar or dissimilar values, regardless of the location from whence they came. Typically, this is approached by evaluating the relationship of the mean of the samples to their variance, with dissimilarity increasing as the variance-to-mean ratio increases. Here, we implement an aspatial analysis of this type using Elliott's d as the statistic (Elliott 1977). The analysis reveals that the tendency for parasite and pathology weighted prevalences to be contagiously or evenly distributed among samples was relatively independent of the geographic relationships measured by ANCOVA comparisons, the runs tests, and the visualized relationships obtained from PCA and cluster analysis. Parasites had a greater tendency to be contagiously distributed among bays than evenly distributed. Nevertheless, prokaryotic inclusions, Perkinsus marinus, nematodes, and rare parasites were evenly distributed, when their distributional pattern was nonrandom. Most of these occurrences came from the Gulf of Mexico region and thus they occurred much more frequently in oysters than in mytilids. That is, parasites and pathologies tended to be contagiously distributed among bays more predictably in mytilids than in oysters. Some few of the even distributions might have been caused by regional rarity, such that many bays had zero or near-zero weighted prevalences; however, certain of these were also found for common parasites, such as P. marinus, in which case nearly all sites had high infection intensities and so bay-to-bay variation was constrained. The pathologies were evenly distributed, perhaps for the same reason. On the other hand, many parasites were significantly contagiously distributed and these also occurred commonly in oysters and often in West Coast mytilids, but rarely in the northeast bays where mytilids were collected. Although the reasons for these trends are not clear, it is noteworthy that oysters are prominent in both the even and contagious category, whereas East Coast mytilids are poorly represented except for the pathologies. Regardless, the aspatial trends are distinct in large measure from the geographic relationships observed via the runs tests and cluster/PCA analyses.

Thus, parasites and pathologies that were common across a region or rare across a region tended to have low variance-to-mean ratios and thus be identified as having even or uniform distributional patterns. Parasites that showed a large range of weighted prevalences within a region were thus identified as having contagious or patchy distributional patterns. These latter could also be common or rare, however. Nematopsis types, for example, were abundant in oysters from most collection locales, yet the values were contagious; that is, the range of values observed was high even though the mean weighted prevalences were high. The ciliate groups were present in much lower weighted prevalences, but equally classified as contagious. Interestingly, with the exception of Perkinsus marinus, most of the contagious parasites were single celled, such as Nematopsis, the ciliates, the haplosporidians, and the prokaryotic inclusions (Table 1). The multicellular taxa, with the exception of the trematode metacercariae in East Coast mytilids, were evenly distributed. That is, the weighted prevalences of multicellular taxa tended to have a much lower variance-to-mean ratio. Likely, this is due to the tendency for the single-celled organisms to proliferate within the host or, being small, to be able to be present in larger numbers within the host, or to transmit directly between sentinel bivalve hosts without intervening (definitive or additional intermediate) hosts.

Summary of Trends

The parasites observed include a number with renowned impacts on host population dynamics. These include the haplosporidians and Perkinsus marinus (Lafferty et al. 2015). Most, however, are present with weighted prevalences too low to be consequential at the population level, although potentially devastating at the individual level (e.g., the trematode sporocysts). The one noteworthy exception is Nematopsis which is widely dispersed in high numbers throughout most of the sampled range of the eastern oyster and was found commonly in West Coast mytilids. Despite very high infection intensities in oysters, no mortality or morbidity is reported from this parasite (but see Brandao et al. 2013). Despite significant year-to-year variability in weighted prevalence (e.g., Powell et al. 1992, Kim & Powell 1998, Kim & Powell 2009), large-scale regional trends remain. These, in large measure, follow known geographic provinces and manifest themselves in a clinal pattern or a regionally coherent pattern along a latitudinal gradient or, for a few in the Gulf of Mexico, as a regionally coherent pattern with longitude. Very few follow geographic trends of sufficient similarity, however, to load on the same axis in a PCA. Thus, the regional distributional patterns of these parasites and pathologies, though similar in some cases in broad aspect, retain substantial uniquenesses.

The distribution of parasites is noteworthy in the bias favoring high weighted prevalence and taxon richness in oysters and in the Gulf of Mexico and in the relatively greater insularity in mytilids on the West Coast. Why oysters suffer a greater depredation by parasites than mytilids is unknown. The bias toward the Gulf is very likely consistent with the tendency for parasitism to increase in warmer climes (Rohde 2002), although the particularly intense levels seen in the Western Gulf remain unexplained. Likewise unusual is the tendency on the Northeast Coast for parasite weighted prevalences in mytilids to be higher toward the north, whereas the distributional pattern on the West Coast follows the more typical bias towards higher values at lower latitudes.

The study covers an epoch of warming temperatures (Weinberg et al. 2002, Nixon et al. 2004, Oviatt 2004) wherein range shifts (e.g., Southward et al. 1995, Sagarin et al. 1999, Weinberg 2005) might degrade the expected signal of long-established provincial boundaries. Despite this expectation based on some well-established range extensions over the last score of years (e.g., Perkinsus marinus; Cook et al. 1998), the traditional provincial boundaries agreed reasonably well with the distributional patterns of the majority of the common parasites, both multicellular and unicellular. This was true for both oysters and mytilids and for all three coasts, East, Gulf, and West, and these signals remained clear over a period of time encompassing at least double the time frame of the most important regional climate cycles, ENSO and NAO. The Mussel Watch program has provided the most temporally extensive and geographically comprehensive evaluation of parasites and pathologies in the marine world and demonstrates the importance of the inclusion of these organisms in long-term monitoring of estuarine and coastal community dynamics as parasites are an important and persistent component of the diversity of marine ecosystems (Rohde 2002, Mouritsen & Poulin 2005).

ACKNOWLEDGMENTS

We thank the Status and Trends field and laboratory teams at Texas A&M University and TDI-Brooks International who collected the animals for histopathological analysis. The Status and Trends Mussel Watch Program was supported through contracts with the U.S. Department of Commerce, National Oceanic and Atmospheric Administration, National Ocean Service.

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ERIC N. POWELL (1) * AND YUNGKUL KIM (2)

(1) Gulf Coast Research Laboratory, University of Southern Mississippi, 703 East Beach Drive, Ocean Springs, MS 39564; (2) Department of Integrated Environmental Science & Department of Biology, Bethune-Cookman University, 640 Dr. Mary McLeod Bethune Boulevard, Daytona Beach, FL 32114

* Corresponding author. E-mail: eric.n.powell@usm.edu

DOI: 10.2983/035.034.0324

TABLE 1.
Results of statistical analyses using ANOVA/ANCOVA.

                                 Mytilids   Oysters    Gulf      Gulf
                                   East      Gulf     oysters   oysters
                      Oysters     versus    versus     West      North
                       versus      West      East     versus    versus
                      Mytilids    Coast      Coast     East      South

Total counted            O          --         G         W         S
  parasites
Total counted            --         E         --        --        --
  parasites less
  Nematopsis
Total counted            --         E          G        --        --
  rare parasites
Total Nematopsis         O          W          G         W         S
Nematopsis, body         O          W         --        --        --
  tissue only
Nematopsis, mantle       O          W          G         W        --
  tissue only
Nematopsis, gill         O          W          G         W         S
  tissue only
Ciliates,                O          NA        --        --        --
  alimentary
  canal only
Ciliates, gill           --         --        --        --         N
  tissue only
Prokaryotic              O          --        --        --        --
  inclusions
Haplosporidians          O          NA         E        NA        NA
Perkinsus marinus        O          NA         G        --        --
Nematodes                O          NA         G         W        --
Trematode                M          E          G        --        --
  sporocysts
Trematode                M          E         NA        NA        NA
  metacercariae
Cestodes                 O          NA        --        --         S
Major pathologies        M          E          G        --        --
Tissue pathologies       --         E         --        --        --
Ceroid bodies            O          E          G        --        --
Digestive gland                     --         E        --        --
  atrophy
Taxon richness           O          --        --        --        --

                           East Coast              East Coast
                             oysters                 mussels

Total counted                  --                      --
  parasites
Total counted                  --              GM [greater than or
  parasites less                                equal to] MA = SN
  Nematopsis
Total counted                  --                 MA > GM = SN
  rare parasites
Total Nematopsis               --                      NA
Nematopsis, body               --                      NA
  tissue only
Nematopsis, mantle             --                      NA
  tissue only
Nematopsis, gill               --                      NA
  tissue only
Ciliates,              MA [greater than or             NA
  alimentary          equal to] SE [greater
  canal only           than or equal to] F
Ciliates, gill                 --              GM [greater than or
  tissue only                                 equal to] MA [greater
                                              than or equal to] SN
Prokaryotic                    --                      NA
  inclusions
Haplosporidians            SE > MA > F                 NA
Perkinsus marinus          F > SE = MA                 NA
Nematodes                      --                      NA
Trematode                      --                 MA > SN > GM
  sporocysts
Trematode                      NA               GM [greater than
  metacercariae                               or equal to] SN = MA
Cestodes                   F = SE> MA                  NA
Major pathologies              --                      --
Tissue pathologies             --                      --
Ceroid bodies              F > SE = MA            GM > SN > MA
Digestive gland            MA > SE = F          SN [greater than
  atrophy                                        or equal to] MA
                                                  [greater than
                                                 or equal to] GM
Taxon richness             SE > F > MA                 --

                                             West Coast
                                              Mytilus
                             West          californianus
                            Coast          versus Mytilus
                           mussels         edulis complex

Total counted          SC [greater than        (cal)
  parasites              or equal to]
                         PC = PN = A
Total counted                 --                 --
  parasites less
  Nematopsis
Total counted                 --                 --
  rare parasites
Total Nematopsis          SC > PC =            (cal)
                            PN = A
Nematopsis, body          SC > PC =            (cal)
  tissue only               PN = A
Nematopsis, mantle        SC > PC =            (cal)
  tissue only               PN = A
Nematopsis, gill          SC > PC =            (cal)
  tissue only               PN = A
Ciliates,                     NA                 NA
  alimentary
  canal only
Ciliates, gill         PC [greater than          --
  tissue only         or equal to] PN =
                      A [greater than or
                         equal to] SC
Prokaryotic                   --                cal
  inclusions
Haplosporidians               NA                 NA
Perkinsus marinus             NA                 NA
Nematodes                     NA                 NA
Trematode                     --                 --
  sporocysts
Trematode                     --                 --
  metacercariae
Cestodes                      NA                 NA
Major pathologies      A [greater than          edu
                      or equal to] PN =
                       PC [greater than
                       or equal to] SC
Tissue pathologies            --                 --
Ceroid bodies                 --               (cal)
Digestive gland               --                 --
  atrophy
Taxon richness            SC > PC =              --
                            PN = A

                      Wald-Wolfowitz
                         runs test          Elliott's d

Total counted               GO          EM EO GO WM
  parasites
Total counted               --          EM EO WM
  parasites less
  Nematopsis
Total counted               --          EM (EO) (GO)
  rare parasites
Total Nematopsis            --          EO GO
Nematopsis, body           EO MW        EO GO WM
  tissue only
Nematopsis, mantle       GO EO WM       EO GO WM
  tissue only
Nematopsis, gill            GO          EO GO (WM)
  tissue only
Ciliates,                   --          EO GO
  alimentary
  canal only
Ciliates, gill             EM EO        EO WM
  tissue only
Prokaryotic                 EO          (GO)
  inclusions
Haplosporidians             --          EO
Perkinsus marinus           --          (EO) (GO)
Nematodes                   --          (EO) (GO)
Trematode                   EM          (EM) (EO) (GO) (WM)
  sporocysts
Trematode                   --          EM
  metacercariae
Cestodes                   EO GO                --
Major pathologies           WM          (EM) (EO) (GO) (WM)
Tissue pathologies          EO          (EM) (EO) (GO) (WM)
Ceroid bodies               EM          EM EO GO WM
Digestive gland             EO          (EM) (EO) (GO) (WM)
  atrophy
Taxon richness              --          (EM) (GO)

Nonsignificant tests are identified by a dash. Single
designations show the higher value where a significant
result occurred comparing two regions or taxa. Hence, "O"
under "Oysters vs. Mytilids" for Total Counted Parasites
indicates that oysters were significantly higher than
mytilids at [alpha] = 0.05. Multiple comparisons are
reported from Tukey's Studentized Range tests. In this case,
> indicates a significant difference at [alpha] = 0.05,
[greater than or equal to] indicates that the variable was
not significantly different from the next one in line, but
significantly different from the remainder, = no significant
difference. Thus GM a MA = SN indicates that GM was not
significantly different from MA, but significantly different
from SN, whereas MA and SN were not significantly different.
For pairwise comparisons: O, oyster; M, mytilid; G, Gulf of
Mexico; W, West Coast or Western Gulf; E, East Coast or
Eastern Gulf; S, Southern Gulf; N, Northern Gulf. For
Tukey's tests: GM, Gulf of Maine; MA, Mid-Atlantic; SN.
Southern New England; SC. Southern California: PC, Pacific
Central; PN, Pacific Northwest; A, Alaska; F, Florida; SE,
Southeast Coast. NA, not applicable (parasite not found or
levels too low to test). For comparisons between M.
californianus and the M. edulis complex: cal, M.
californianus significantly higher; edu, M. edidis complex
significantly higher; () length covariate significant and
explains between taxon differences. For Wald-Wolfowitz Runs
Test and Elliott's d, abbreviation shows significance at
[alpha] = 0.05: GO, Gulf oyster; EO, East Coast oyster; EM.
East Coast mytilid; WM. West Coast mytilid. For Elliott's d,
() indicates an even distribution; no () indicates a
contagious distribution.

TABLE 2.
PCA variables loading on the first 12 factors at a
factor load score greater than 0.5.

Factor 1     Nematopsis, body and mantle tissue only
Factor 2     Cestodes
Factor 3     Trematode sporocysts; major pathologies; tissue
               pathologies
Factor 4     Nematopsis, gill tissue only; Perkinsus marinus
Factor 5     Trematode metacercariae; major pathologies
Factor 6     Nematodes
Factor 7     Prokaryotic inclusions
Factor 8     Ciliates, alimentary canal only
Factor 9     Haplosporidians
Factor 10    Ciliates, gill tissue only
Factor 11    Digestive gland atrophy
Factor 12    Total counted rare parasites
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