Temporal structure and trends of parasites and pathologies in U.S. oysters and mussels: 16 years of mussel watch.
KEY WORDS: oyster, mussel, Status and Trends, Mussel Watch, interannual variability, parasitism, pathology, temporal trends, Mytilus, Crassostrea, Dreissena
A number of surveys of parasites and pathologies of substantial geographic extent have been carried out for selected bivalve species in selected regions (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), but few surveys have been both geographically extensive and of multiyear duration. The National Oceanic and Atmospheric Administration Status and Trends Mussel Watch Program conducted a yearly survey of the parasites and pathologies of oysters and mussels from 1995 to 2010 (Kim & Powell 2006, 2007, Kim et al. 2008). Bivalves were sampled from most major coastal water bodies 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 long-term temporal trends and interannual variability in the prevalence and infection intensity of parasites and pathologies (Powell & Kim 2015).
Temporal patterns in the prevalence and infection intensity of parasites, the incidence of pathologies, and a range of physiological indices in bivalves occur through a variety of means. Among those well described are climate cycles that introduce periodic variations in temperature and precipitation, hence salinity, and food supply (Hayes et al. 2001, Mouritsen & Poulin 2002). Within the geographic region of Mussel Watch, foremost of these are the El Nino-Southern Oscillation (ENSO) and the North Atlantic Oscillation (NAO) (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 (Powell et al. 1992a, Wilson et al. 1992, Soniat et al. 2006, 2009, Doi & Yurlova 2011, Bushek et al. 2012). The Mussel Watch time series is of sufficient length to span minimally two full cycles for the NAO and twice that for ENSO. Of longer term are the multidecadal cycles such as the Atlantic Multidecadal Oscillation and the Pacific Decadal Oscillation (Sutton & Hodson 2003, McCabe et al. 2004, Miller et al. 2004), and the directional influence of global warming (Scavia et al. 2002, Parmesan & Yohe 2003, Friedland & Hare 2007). These climate patterns are of longer time scale than the Mussel Watch dataset and might introduce long-term trends in parasites, pathologies, and physiological indices (Ford 1996, Cook et al. 1998, Harvell et al. 2002, Lafferty et al. 2004, Mouritsen et al. 2005, Levinton et al. 2011).
Mussel Watch sentinel bivalves are, for the most part, relatively long lived (Powell & Cummins 1985, Powell & Stanton 1985, Heller 1990). For oysters, the influence of disease over most of the range sampled by Mussel Watch, particularly Dermo (causative agent Perkinsus marinus) and, over a lesser component of the range. Multinucleated Sphere Unknown (causative agent Haplosporidium nelsoni), limits average life spans to 3-4 y in many locales (Kraeuter et al. 2007. Powell et al. 2012a) despite the inherently longer life span present over evolutionary time (Powell & Klinck 2007, Mann et al. 2009). Even for oysters, however, the ecological memory embedded in the population would suggest that interannual variability frequently should be positively autocorrelated; that is, shifts in population metrics should occur over multiyear time scales. Powell et al. (1996) and Soniat et al. (1998) examined some aspects of this population behavior for oysters. For parasites, life spans may be important; some taxa remain in the host for significant components of the host's life span (Curtis et al. 2000. Tetreault et al. 2000, Jaenike 2002, Kube et al. 2002, Curtis 2003); others wax and wane seasonally (Svardh 1999, Ngo et al. 2003, Ngo & Choi 2004, Lyons et al. 2007). Thus, interannual variability may be influenced by the dynamics of recruitment and growth of the host and transmission of the parasite and these processes may respond to short-term environmental change as well as longer term climate cycles and climatic shifts. The purpose of this analysis was to examine the significance of interannual variability in parasites, pathologies, and selected physiological indices in Mussel Watch sentinel bivalves to evaluate the importance of long-term trends over a 16-y time span from 1995 to 2010, and determine the degree to which interannual changes are autocorrelated, suggesting a temporal memory or a response to cyclic environmental change in the population dynamics of the bivalve and its parasite complement.
MATERIALS AND METHODS
Species Sampled and Sample Collection
The bivalve samples were collected annually from a network of sites along the United States 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 & Powell (2007) for details on the bays and their associated bay numbers], A "bay," as termed herein, represents all sites in a single estuary, an estuarine reach of a large estuary, or group of neighboring sites along a contiguous open coastline.
The introduced zebra mussel Dreissena polymorpha and quagga mussel Dreissena hugensis were sampled at sites in the Great Lakes (bays 1-10) and Hudson River (bay 11). Rosenberg and Ludyanskiy (1994) discussed the taxonomy. Mussel Watch sites include the U.S. waters of all Great Lakes except Lake Superior (Lauenstein et al. 1997).
Mytilid mussels 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 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. Among the 58 total West Coast sites, M. californianus was collected at 31 sites;. At the vast majority of the more northern stations from Oregon to Alaska, M. trossulus was collected. The mussel M. 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, Elliott et al. 2008). Thus, M. galloprovincialis was collected at some California sites and may have been present in some Puget Sound collections. Moreover, hybrids occur in some locations (Braby & Somero 2006, Elliott et al. 2008). Powell and Kim (2015) found few differences in parasite body burden between M. californianus and the other mytilids that could not be explained by the inherently larger size of M. californianus. Thus, the mytilid species were not distinguished in subsequent analyses of temporal trends.
Four oyster taxa were sampled, Crassostrea virginica, Crassostrea rhizophorae, Crassostrea gigas, and Dendostrea sandvichensis. Of these, C. 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 were excluded from this analysis because of their unique species complement and limited geographic area.
Except in the Great Lakes, the sampling sites were visited annually or biennially during winter with each site occupied within 30 days of an annual target date (O'Connor 1994). Sampling occurred in winter to minimize the influence of gametogenesis and spawning on contaminant body burden (Jovanovich & Marion 1987, Ellis et al. 1993, Buisson et al. 2008). Dreissenid mussels were collected in late August through September because the Great Lakes are frequently frozen over during the 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 (Wallet & Lambert 1986, Burreson & Ragone Calvo 1996, Ford et al. 1999). For much of the time series, a biennial sampling protocol resulted in the sampling of sections of coastline in alternate years. Thus, for example, most of Louisiana was sampled in even years; much of Texas in odd years. This biennial regime can be expected to introduce interannual variability in the time series if geographic regions that encompass a number of sampling groups are composited and analyzed. Subsequent statistical analyses included this sampling protocol as a caveat.
Sample preparation is described by Kim et al. (2006a). For oysters, Perkinsus marinus was assayed by the more precise thioglycollate method of 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 and pathologies, including prokaryotic inclusions (Rickettsia, Chlamydia, etc.), ciliates, gregarines, nematodes, cestodes, and metacercariae of trematodes, that could be tallied individually, following procedures described by Ellis et al. (1998a) 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 was counted, although the sinuosity of a single individual may allow a number of cross-section of the individual to be present in a single scanned slide. 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) and ceroid bodies (Mackin 1951, Stein & Mackin 1955; also termed brown cells, Zaroogian et al. 1993). Some parasites and physiological 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. 1998a, Ashton-Alcox et al. 2006, Kim et al. 2006b). Gonadal stage designations are defined in Ellis et al. (1998b) and Kim et al. (2006a).
Weighted prevalence was used to describe parasite/pathology occurrence in this study (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:
= [n.summation over (i=1)] number of occurrences of parasite or pathology / number of animals infected.
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. The latter two are not necessarily correlated, particularly for parasites that proliferate after transmission. For some of the observed parasites, prevalences were zero for many bays in some regions; thus, analyses of regional trends perforce would emphasize prevalence if a comprehensive analysis is wanted. This would dismiss any consideration of differences in infection intensity. For others of the observed parasites, prevalence was nearly 100% over extensive regions; thus, analyses of regional trends perforce would emphasize infection intensity. Thus, to achieve uniformity in regional comparisons across parasite categories, a mixed metric is necessary. Accordingly, the compromise of weighted prevalence is used as the metric for comparison.
Inasmuch as the sheer number of samples obtained yearly by the Mussel Watch program prevented detailed identification of most parasites, parasites were identified, tallied, and analyzed statistically by major taxon following the strategy adopted by Yevich and Barszcz (1983) as part of 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, 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 oyster taxa, 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 not only for 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).
Physiological indices included length, gonadal state, sex ratio, number of ceroid bodies, and digestive gland atrophy; the latter included in this category assuming that the trait is a nutritional condition, not a pathology. Physiological indices were either the average of measurements (length), the average of counts (ceroid bodies), ratios based on counts (gonadal state, sex ratio), or the average of semiquantitative scale values (digestive gland atrophy). Gonadal state was assessed as the fraction of animals in late development, fully developed, or spawning. Sex ratio was calculated as the ratio between males and females. Undifferentiated animals were not included in the sex ratio, but were included in the gonadal index.
Three statistical analyses were used. The degree of variation between years was assessed using analysis of variance with bay and year as main effects. Differences between bays were considered by Powell and Kim (2015) and are not investigated further here. A significant "year" main effect was interpreted to mean that variation between years was significant. Linear trends through the time series were identified using Spearman's rank correlations. The tendency for adjacent years to be autocorrelated was assessed using Durbin-Watson tests. The influence of sampling sets of bays in alternate years was minimized by including a 2-y lag in the autocorrelation analysis. A summary of statistical analyses is provided in Tables 1-3.
Regional analyses were based on the allocation of bays to provinces as described in Powell and Kim (2015). East Coast bays where oysters were collected were divided into three sections: bays 56-61 (St. Johns River to Florida Bay), bays 49-55 (south Pamlico Sound to Sapelo Sound), and bays 39-48 (Delaware Bay to north Pamlico Sound). These will be termed the Eastern Florida, Southeast, and Southern 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 63-66 (Tampa Bay to the Everglades), was distinguished from the Northern Gulf, bays 67-87 (Cedar Key to the Brazos River). East Coast bays where mytilids were collected were separated into three groups about Cape Cod and the Hudson Canyon; from south to north, bays 31-38 (Fire Island to Delaware Bay), 23-30 (Narragansett Bay to Moriches Bay), and 12-22 (Penobscot Bay to Buzzards Bay). These will be termed the Northern 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), 103-112 (San Luis Obispo Bay to Tillamook Bay), 113-122 (Columbia River to the Strait of Juan de Fuca including all of Puget Sound), and 123-125 (Nahku Bay to Cook Inlet). These regions were termed Southern California, Pacific Central, Pacific Northwest, and Alaska, respectively.
The divisions follow provincial boundaries. 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 (Powell & Kim 2015). Within the geographic range of Mussel Watch, Hall (1964) identified major provinces as 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).
Variation between years was significant for physiological indices in nearly every geographic region and most significant results were highly significant (Table 1). This was particularly true for length, digestive gland atrophy, and the number of ceroid bodies (Figs. 1-3). Sex ratio and gonadal state differed significantly for oysters in most geographic regions of the East and Gulf Coasts and also for West Coast mytilids in two of four regions (Figs. 4 and 5). Thus, variations between years in sex ratio and gonadal state occurred frequently for oysters and less frequently in West Coast mytilids. In contrast, no significant differences were found for dreissenids or Mytilus edulis on the East Coast.
Variation can come about in three ways: a long-term trend may be present, years may vary sporadically, or autocorrelation may exist in the dataset as would be the case if influenced by a climate cycle. For physiological indices, variation between years was at least in part produced by directional shifts across the time series in many cases. Length declined significantly across the time series in six regions, mytilids from the Gulf of Maine and Northern Mid-Atlantic regions, Southern Mid-Atlantic oysters, and oysters from the Eastern, Western, and Northern Gulf Coasts (Table 2, Fig. 1). Although varying significantly between years, West Coast mytilids did not demonstrate a trend across the times series (Fig. 1, Table 2), although detecting such might have been difficult given the large difference in size between Mytilus californianus and members of the Mytilus edulis complex. Autocorrelation was significant in two cases that did not demonstrate linear trends (Table 3): mytilids from Southern New England and the Pacific Northwest (Fig. 1). Both time series were characterized by distinct zenithal and nadiral segments.
In essentially every geographic region, regardless of sentinel taxon, digestive gland atrophy scores declined over the time series (Table 2, Fig. 2). Generally, these declines were highly significant. Autocorrelation was not present (Table 3). The number of ceroid bodies declined over the time series for dreissenids and mytilids on the East Coast and for oysters from the Southern Mid-Atlantic (Fig. 3). Significant autocorrelation occurred also for the dreissenids, established in the first half-decade when the number of ceroid bodies plummeted (Fig. 3). Although significant differences between years were present in most East Coast and Gulf Coast regions where oysters were collected and in most West Coast regions where mytilids were collected (Table 1), directional trends in the number of ceroid bodies were not apparent (Table 2, Fig. 3); nor was autocorrelation significant in any case (Table 3).
Gonadal state varied over the time series in three regions. Gonadal state rose in Southern Mid-Atlantic oysters, but declined in Southeast oysters and Pacific Central mytilids (Fig. 4). Gonadal state was significantly autocorrelated in Western Gulf oysters, with scores generally lower in the middle years of the time series (Fig. 4). Sex ratio changed significantly across the time series in three regions: Southern Mid-Atlantic, Eastern Gulf, and Northern Gulf oysters (Fig. 5, Table 2). Significant autocorrelation was not present (Table 3). The inverse trends between length and sex ratio in oysters (compare Figs. 1 and 5) are consistent with the protandric nature of the species (Coe 1932, Powell et al. 2011, Harding et al. 2013).
Collected Parasite Categories
Total parasite body burden rarely varied significantly between years (Table 1), with significant results limited to the dreissenids from the Great Lakes, Eastern Gulf oysters, and Pacific Central mytilids (Fig. 6). Excising Nematopsis from this metric removed the significant result for Eastern Gulf oysters, but not from Pacific Central mytilids (Fig. 6, Table 1). Nematopsis was not present in dreissenids or East Coast mytilids (Powell & Kim 2015). Rare parasites varied significantly between years in Great Lakes dreissenids, Southeast and Western Gulf oysters, and in Southern California and Pacific Central mytilids (Fig. 6, Table 1).
Unlike the physiological indices, few long-term trends were present (Table 2, Fig. 6). Total parasites, excluding Nematopsis, rose over the time series in Southeast oysters and Alaskan mytilids (Fig. 6). The Alaskan trend was present also if Nematopsis was included (Fig. 6). The opposite trend was weakly significant in Pacific Central mytilids. Year-to-year changes in parasite body burden, after excluding Nematopsis, were significantly autocorrelated in northern Gulf oysters where body burdens tended to be higher in the central years of the time series (Table 3, Fig. 6). Neither long-term trends nor autocorrelation was present in total counted rare parasites in any region (Fig. 6, Tables 2 and 3).
Nematopsis was not detected in Great Lakes dreissenids or Atlantic coast mytilids (Powell & Kim 2015). Variation in total Nematopsis (Tables 1-3) subsumed significant variations in parasite body burden among tissues. The body burden of Nematopsis in the mantle tissue varied significantly between years in Western Gulf and Southern Gulf oysters and in Southern California and Pacific Central mytilids (Table 1, Fig. 7). For two of these, body burden in the body tissue also varied significantly (Table 1, Fig. 7). The body burden of Nematopsis in the gill tissue followed a distinctive trend in oysters, but not in mussels: Nematopsis body burden varied significantly between years in Eastern Gulf oysters rather than Western Gulf or Southern Gulf oysters, and once again varied significantly in Pacific Central mytilids (Table 1, Fig. 7). The differential in the Gulf of Mexico is likely due to the presence of different species of Nematopsis in the gill and mantle/body tissues. Sprague (1949) and Sprague and Orr (1952. 1955) suggested that two different species (Nematopsis ostrearum and Nematopsis prytherchi) occur in Gulf oysters, and N. prytherchi tends to concentrate in the gills (see also Winstead et al. 2004). The number of Nematopsis in the gill tissue rose significantly over the time series in Eastern Gulf oysters (Table 2, Fig. 7). Nematopsis in the body and mantle tissues averaged higher in mytilids from Southern California in the latter half of the time series (Fig. 7), rising significantly over the time series in both tissues (Table 2). Nematopsis from the mantle tissue of mytilids from Southern California also demonstrated significant positive autocorrelation (Table 3): highest tissue counts were present near the beginning and end of the time series; counts were near zero from 1997 through 2003 (Fig. 7). The tendency for body burdens to be higher in years near the beginning and end of the time series was also present in Nematopsis in the body and mantle tissues in Southeast Coast oysters, but only reached a level of significance in the body tissue (Table 3, Fig. 7).
Other Protozoa and Prokaryotic Inclusions
The body burdens of ciliates observed in the gill and alimentary canal varied significantly in Pacific Central mytilids (Table 1, Fig. 8); gill ciliates also varied significantly in oysters from the Western and Northern Gulf of Mexico (Fig. 8). For gill ciliates in Eastern Gulf oysters, body burden rose over the course of the study. A significant increase over the time series also occurred in Southeast Coast oysters, Northern Gulf oysters, and in three of four regions for mytilids on the Pacific coast (Table 2, Fig. 8). Pacific Central mytilids saw a barely significant decline (Table 2). Ciliates in the alimentary tract varied little over the time series in comparison with those in the gills (Table 1). Nevertheless, the number of ciliates in the alimentary tract rose significantly in Southern Mid-Atlantic oysters over the time series (Fig. 8). Significant autocorrelation occurred commonly in gill ciliates (Table 3): namely, Southeast Coast oysters, Western Gulf oysters, and Southern California mytilids (Fig. 8). Each of these cases was characterized by a substantial increase in body burden late in the time series.
Although prokaryotic inclusions were found in mytilids and oysters and on all coasts, East, West, and Gulf, the body burdens were relatively stable over the time series except in four cases (Table 1), namely, Pacific Northwest mytilids and oysters from the Southern Mid-Atlantic, the Southeast, and the Western Gulf (Fig. 4). Each of the time series was characterized by occasional years with high body burdens, with the extremes being most apparent in Southeast Coast oysters.
Haplosporidians were routinely encountered in only two regions, the Southern Mid-Atlantic and Southeast regions where Haplosporidium nelsoni is the dominant pathogen (Powell & Kim 2015). Weighted prevalence was relatively stable over the time series in both regions (Table 1). Perkinsus marinus offered a dramatic contrast; P. marinus varied significantly over the time series in 4 of 7 regions where oysters were collected, all in the Gulf of Mexico (Table 1, Fig. 5). In each of the Gulf regions, weighted prevalence declined significantly both statistically and biologically over the time series (Table 2, Fig. 5). In two cases, the time series was also characterized by increased weighted prevalence during a portion of the time series; during the late 1990s for the Eastern Gulf and during the early 2000s for the Southern Mid-Atlantic (Table 3, Fig. 5).
Multicellular Eukaryotic Parasites
In contrast to the single-celled parasites, the multicellular parasites varied over the time series relatively infrequently. Trematode sporocysts showed no significant changes over the time series in any region (Table 1). Trematode metacercariae were common only in mytilids (Powell & Kim 2015). Body burdens rose significantly in the latter half of the time series in Southern California mytilids (Table 2, Fig. 9) and varied sporadically, but significantly, in mytilids from the Gulf of Maine and the Pacific Northwest (Table 1). Cestodes varied sporadically, but in oysters from both the Southern Mid-Atlantic and the Western Gulf, body burdens tended to be higher late in the time series (Fig. 9). Year-to-year variations in the Western Gulf were in part a function of the alternate-year sampling regimen that by chance sampled bays with high body burdens every other year. Much of the biennial oscillation was due to extraordinarily high body burdens in the Laguna Madre of Texas (Powell & Kim 2015). Nematodes also varied significantly among the years in oysters from the Southern Mid-Atlantic and the Western and Northern Gulf, but without trend (Fig. 9, Table 1).
Major pathologies varied significantly through the time series in one or more statistical tests for all regions where mytilids were collected on the East Coast and for two of the four West Coast regions (Tables 1 and 2, Fig. 10). Major pathologies were present only early in the time series in dreissenids from the Great Lakes (Fig. 10). A decline in the frequency of major pathologies late in the time series established a significant decline over the time series in mytilids from Southern New England; the opposite trend was present in the Gulf of Maine, although the frequency of major pathologies declined late in the time series from highs in the 2004 to 2006 period. The frequency of major pathologies also varied sporadically, but significantly, in Eastern Gulf and Northern Gulf oysters and in Southern California mytilids (Table 1, Fig. 10). Weighted prevalence declined significantly across the time series in Pacific Central mytilids (Table 2, Fig. 10).
Tissue pathologies, including focal and diffuse hemocytic infiltration, varied significantly in mytilids only on the West Coast (Table 1); significant variation occurred in three of four West Coast regions: Southern California, Pacific Central, and Pacific Northwest (Fig. 11). The time series from Southern California demonstrated a strong tendency to oscillate (negative autocorrelation) (Table 3). Tissue pathologies expressed positive autocorrelation on the Southeast Coast as the frequency of pathologies reached a zenith in the 2002 to 2004 period (Fig. 11). The frequency of tissue pathologies varied significantly across the time series in oysters from all Gulf regions (Table 1, Fig. 11). in three cases, autocorrelation was significant resulting in a zenith in frequency during the 2000 to 2005 period (Table 3, Fig. 11).
The National Status and Trends Mussel Watch Program sampled parasites and pathologies in sentinel bivalves from all major coastal water bodies on the East, West, and Gulf Coasts and the Great Lakes from 1995 to 2010. The sampling design was fashioned to create a contaminant time series emphasizing polycyclic aromatic hydrocarbon, pesticide, and heavy metal body burdens (Kimbrough et al. 2008). As a consequence, sampling focused on the largest animals in each population and typically occurred during the winter months of December to January, except for August collections of dreissenids from the Great Lakes. The sampling protocol often included sampling bays in alternate years, which in some cases introduced an oscillatory signal into the time series, as certain parasites were more common in some bays than in others. A particularly dramatic example is cestodes in oysters from the Western Gulf of Mexico (Fig. 9), where the Laguna Madre site that yielded oysters with particularly high cestode counts (Powell & Kim 2015) was sampled in alternate years. The sampling protocol also involved the addition and subtraction of some sites within bays on any given sampling year. Such variations in the number of sampled sites within a bay were not uncommon. Thus, the Galveston Bay Ship Channel site was sampled only in 1999, 2001, 2003, and 2007, whereas the Galveston Bay Hanna Reef site was sampled eight times between 1995 and 2009. Additionally, sampling in the winter likely biased results for parasites such as Haplosporidium nelsoni and Perkinsus marinus whose weighted prevalences are significantly influenced by time of year (winter temperature) (Ford et al. 1999, Powell et al. 1996). The time series is considerably longer than climate cycles known to influence these sentinel bivalves such as the ENSO and NAO and collections are geographically extensive, so that the influence of local forcing, as in the aforementioned case for cestodes, overall is limited in its impact.
Temporal trends were examined for regional combinations of bays that in the main were delineated by known provincial boundaries. Powell and Kim (2015) analyzed this dataset from this perspective and provide results supporting the delineated regions used herein. Earlier analyses of Mussel Watch data consistently showed that neighboring bays tended to vary concordantly both in parasite and pathology weighted prevalence and in the body burden of many contaminants (Kim & Powell 1998, Kim et al. 1999, Kim & Powell 2009) and the scale of this concordancy was often hundreds of kilometers, lending additional support for the analytical approach adopted herein which focused on yearly changes in metrics within regions.
The temporal dynamics of the parasites, pathologies, and physiological indices of these sentinel bivalves, dreissenids, mytilids, and oysters, fell into a few clear categories. Significant differences between years occurred commonly; the absence of significant change over time was more noteworthy. This was true for parasites, pathologies, and physiological indices. In a few cases, these differences included autocorrelated trends in which year-to-year variation was more likely to result in multiyear increases or decreases in value within the time series. Such behavior might be anticipated by the presence of a multiyear cycle and, in fact, such behavior was much more common along the Southern East Coast, the Gulf Coast, and Southern California, where the effects of a relatively short cycle, ENSO, are well documented (Schoener & Tufts 1987, Millan et al. 2002, Soniat et al. 2009). More interestingly, for a number of parasites, pathologies, and physiological indices, significant trends existed across the time series. These trends substantively exceed the span of the oft-mentioned climate cycles influencing these regions such as ENSO and NAO (Bojariu & Gimeno 2003, Soniat et al. 2006, Bushek et al. 2012, Powell et al. 2012b, Chaalali et al. 2013). A few of these longer term coherent trends were common across sentinel taxa and multiple coasts. Regional trends were apparent in an important second subset.
The Major Taxa and Continental Trends in Physiological Indices
Trends on a continental scale were well represented in the physiological indices. Bivalve size (length) declined in mussels in the Northeast and oysters in the Gulf of Mexico and the Southern Mid-Atlantic. The trend was comprehensive across most regions of the Gulf of Mexico and both oysters and mussels followed similar trends north of Cape Hatteras on the East Coast. The West Coast mussels did not participate in this trend. In no case did length increase over this time frame in any region, a noteworthy void.
Digestive gland atrophy declined throughout the coastal regions of the continental United States and in the Great Lakes. Very few regions were exempted from this trend and in no case did digestive gland atrophy rise. The trend was coincident across all sentinel bivalve taxa. The number of ceroid bodies declined in three taxa, all in the north and northeastern region of the United States, dreissenids in the Great Lakes, mytilids in all three regions where they were collected on the Northeast Coast, and oysters from the Southern Mid-Atlantic. In no case did the number of ceroid bodies increase over the 1995 to 2010 time series.
The male-to-female ratio rose in oysters of the Gulf Coast in most regions and also oysters from the Southern Mid-Atlantic. In sharp contrast to all other physiological indices, gonadal index changed directionally only in a few cases across the time series, although year-to-year variation was often significant.
Length is a product of food supply, filtration rate, and longevity in bivalves (Hofmann et al. 1994, van der Veer et al. 2006, Munroe et al. 2013). A decline in length is manifested by three possible conditions. First, food supply, either quantity or quality, may have declined; the former occurs because either upstream concentrations changed or increased crowding reduced food availability downstream (Frechette & Bourget 1985, Powell et al. 1995, Wall et al. 2011). Second, filtration rate is a function of temperature and for oysters salinity. Temperature may have declined or risen above optimal, or salinity may have declined to suboptimal levels, any of which would decrease filtration rate (Powell et al. 1992b, Ren & Ross 2005, Freitas et al. 2009). Third, the mortality rate may have risen, thereby truncating the size distribution (Rice 2000, Kraeuter et al. 2007, Narvaez et al. 2015). Trends in food supply for bivalves are very poorly understood. The commonly measured metric, chlorophyll, is an inadequate measure of food (Powell et al. 2012c). Presumably, temperature has not declined over the time series. Examples of higher temperatures decreasing filtration rate are well documented in bivalves with range shifts being an extreme outcome. Increasing temperature can change the balance between somatic and reproductive growth, thereby decreasing adult size (Buxton et al. 1981, Hofmann et al. 1994, Munroe et al. 2013). Oysters can manifest a latitudinal variation in size (Hofmann et al. 1994), as can other bivalves (Ansell 1968, Bauer 1992), so that higher temperatures cannot be excluded as a causative factor for a decline in length; however, length declined in oysters from the Southern Mid-Atlantic Bight and also the Gulf of Mexico, suggesting that temperature is not a primary contributor, and the presence of the selfsame trend in all three regions in the Northeast where mytilids were collected, rather than, for example, just the southern region (Northern Mid-Atlantic) further disputes the importance of temperature. Although one can only speculate, a change in longevity or food supply represents intriguing options.
What is noteworthy in this context is the ubiquity of the decline in digestive gland atrophy. This decline was noted in all sentinel taxa and in nearly all regions, and on all coasts. Digestive gland atrophy is a response to nutrition in oysters (Palmer 1979, Winstead 1995, Kim & Powell 2004, Kang et al. 2010) and other bivalves (Bielefeld, 1991); however, digestive gland atrophy also has been observed associated with contaminant-produced and other sublethal stresses (Widdows et al. 1982, Axiak et al. 1988, Gold-Bouchot et al. 1995, Weis et al. 1995, Elston et al. 2003, Buisson et al. 2008). One possible explanation for the varying results is that stress in whatever form is likely to compromise nutrition, so that an inference relating digestive gland atrophy to nutrition is likely to be substantially correct. Digestive gland atrophy declined in all taxa and on all coasts. The inference is that nutrition improved. Nutrition might improve for a host of reasons. Food supply, quantity or quality, may have improved. Milder winter temperatures might have permitted increased filtration rates over winter when food supplies are typically low (Soniat et al. 1998, Zarnoch & Schreibman 2008). Smaller animals have an increased scope for growth and thus may retain an improved nutritional state even under less optimal food supplies (Hawkins & Bayne 1992, Jensen 1997, Munroe et al. 2013). It is indeed interesting that a decline in length and digestive gland atrophy co-occur often in the Mussel Watch dataset, for both oysters and mytilids, and in no case is a decline in digestive gland atrophy associated with an increase in size, all of which represent happenstances suggestive that smaller animals are responsible for the improved nutritional state (or vice versa). Regardless, the two physiological indices demonstrate a continental scale trend in bivalve physiology that can only be driven ultimately by a very large-scale climatology (Parmesan & Yohe 2003, Baines & Folland 2007).
Two other regional associations are of interest. In the Northeast, the number of ceroid bodies or brown cells declined with declining length and digestive gland atrophy. Little is known about the function of ceroid bodies. Whyte et al. (1994), Lassudrie et al. (2014), and Sunila and LaBanca (2003), among others, associated them with processes related to disease and pathology. Others have observed a connection with contaminants (Zaroogian et al. 1993, Zaroogian & Jackim 2000). Either explanation for the decline would imply an improved physiological state and thus would be consistent with a decline in digestive gland atrophy interpreted as evidence of an enhanced nutritive state.
Sex ratio in mussels is a product of maternal genotype (Kenchington et al. 2002, Yusa et al. 2013). Conceivably, such a dynamic might be influenced by climate change, but no evidence of trends exists in the Mussel Watch dataset on either the East or West Coast. In fact, although in several cases significant year-to-year variations occurred in mussels on the West Coast (Southern California and Pacific Northwest), the male:female ratio varied around 1:1 over the time series. Oysters, on the other hand, are protandrous and the protandric shift is a function of the dynamics within the population (Asif 1979, Kennedy 1983, Harding et al. 2013, Powell et al. 2013), which certainly might be influenced by the environment (Egami 1953, Katkansky & Sparks 1966, Kennedy 1983) and hence climate change. One obvious option would be an increasing maleness in the population with declining adult length, if that decline was a function of declining longevity or reduced growth rate. Powell et al. (2013) noted that the sex change was a complicated function of both age and length, modulated by within-population processes. The association of increasing maleness with decreasing length is dramatically apparent in oysters from the Gulf of Mexico over the 1995 to 2010 time series and also is present in oysters taken from the Southern Mid-Atlantic. In each of these cases, the inverse trend in sex ratio and length is most readily explained by a declining average age for the largest members of the population.
Putative Cyclical Trends in Distribution
Certain parasites, pathologies, and physiological indices demonstrated periods of relatively high or low values within the time series. In many cases, the nadir or apogee occurred around the year 2000. Mytilids in the Pacific Northwest, for example, reached a nadir in length between 1999 and 2002. Tissue pathologies reached apogeal levels between 2002 and 2004 in oysters from the Southeast Coast and from 1999 to 2005 for oysters at all four Gulf of Mexico regions. Perkinsus marinus reached local highs in Southern Mid-Atlantic oysters in 2002 and 2004, but apogeal levels in the Gulf of Mexico occurred earlier, in the late 1990s. Nematopsis in oysters, depending on the tissue, tended to reach peak values in the 2002 to 2004 time period and late in the time series. The tendency toward apogeal or nadiral values in the 2002 to 2005 time frame is consistent with positive Nino 3.4 sea surface temperature anomalies during that time frame (Tolan 2007). The tendency for certain metrics to have high values near the beginning of the time series, in the late 1990s, and at the end of the time series, 2010, is also consistent with the very positive Nino 3.4 sea surface temperature anomalies at those times. Although the Mussel Watch time series was not designed to validate a relationship between the ENSO or other climate cycles and certain physiological and parasitological traits, the time series does corroborate other studies associating variation in certain of these conditions with climate cycles. Weighted prevalence of P. marinus in Gulf Coast oysters is a good example (Powell et al. 1992a, Kim & Powell 2009, Soniat et al. 2009)
Regional Trends in Parasites and Pathologies
Major pathologies declined in three of four cases where trends in the time series were significant (Table 2). The most dramatic of these was in Pacific Central mussels, where weighted prevalence dropped by about a factor of 2 over the time series. The decline in major pathologies in mussels from Southern New England was more modest due to a tendency for higher values to be present in the 2001 to 2006 time frame. Higher values in this time frame were also present in mytilids from the Gulf of Maine, a tendency strong enough in this latter case to support a significant increase over the time series, despite a decline in weighted prevalence in the last few years. It is interesting that no parasites generated significant trends in mytilids from the Northeast Coast, and rarely were any year-to-year changes in weighted prevalence significant. Powell and Kim (2015) noted that major pathologies were much more prevalent in East Coast mussels than in East Coast or Gulf Coast oysters or mytilids from the West Coast. Thus, time series trends in major pathologies were concentrated in the region where weighted prevalences were highest.
In contrast, the remaining time series trends in mytilids were all associated with the West Coast and in large measure with the Southern California region, and this differential is present despite the higher weighted prevalences for most parasite taxa in East Coast mussels relative to their West Coast counterparts (Powell & Kim 2015). Trematode metacercariae, gill ciliates, and Nematopsis in the mantle and body tissues all increased over the time series in Southern California mytilids. Gill ciliates rose in most West Coast regions. In all cases, the outcome was determined by relatively low weighted prevalences in the 1990s relative to the following years.
In comparison, with the exception of Perkinsus marinus, regional trends in oysters were rare. Yet, as in West Coast mytilids, those that occurred were normally positive; that is, weighted prevalences rose over the time series. Like the Southern California region on the West Coast, nearly all trends were in a few regions, the Southeast Coast and the Eastern and Northern Gulf in this case, where the few regional trends were positive. Considering all regional trends, all sentinel bivalve taxa, and all coasts, nearly half of the significant regional trends for parasites were due to gill ciliates and, with one exception, all of these were positive; that is, gill ciliates rose over the time series in selected regions for West Coast mytilids and East Coast and Gulf Coast oysters.
The dramatic decline in Perkinsus marinus weighted prevalence in oysters from the Gulf of Mexico regardless of the division of the Gulf along latitudinal or longitudinal lines is particularly noteworthy, as is the association with a substantial decline in length, and presumably age. If increased mortality is the proximate cause of the decline in length in Gulf oysters, the agent would not likely be a predator, as most predators target the smaller size classes (Powell et al. 1997, Linton et al. 2007, Johnson & Smee 2012). Fishing targets the larger size classes, as most states have a 7.6-cm size limit. Although some Mussel Watch sites are fished, and probably overharvested in many cases, which would truncate the size distribution, the majority of sites are not fished. This is particularly true for the Southern Gulf sites. Length declined over the time series in Southern Gulf oysters, but this was the only Gulf region for which the decline was nonsignificant (P = 0.096), suggesting that fishing may have contributed in some measure to the observed decline in length. On the other hand, P. marinus-induced mortality targets the larger animals, particularly in the Gulf where oyster growth rates are high (Powell et al. 1996). An increase in adult mortality during the summer might result in the biased survival of smaller animals into the winter when Mussel Watch samples were collected and also produce a lower weighted prevalence as the animals with higher infection intensities had already died.
Many parasites had highly variable weighted prevalences from 1 year to the next, without significant trends. Significant year-to-year variability without apparent temporal pattern was the most common outcome for multicellular eukaryotic parasites where significant year-to-year differences existed. Examples include trematode metacercariae in Gulf of Maine mytilids, cestodes in Western Gulf oysters, and nematodes in oysters from the Southern Mid-Atlantic, Western Gulf, and Northern Gulf. This tendency for year-to-year variations to exist without trend was also typical for the most common parasite, the gregarine Nematopsis: examples include Nematopsis in the gill tissue of Eastern Gulf oysters and Pacific Central mytilids, Nematopsis in the mantle tissue of Pacific Central and Southern California mussels and in Southern Gulf and Western Gulf oysters, and Nematopsis in the body tissue of Southeast Coast and Western Gulf oysters and Pacific Central mytilids. Prokaryotic inclusions likewise followed this pattern: examples include Northern Mid-Atlantic mytilids, the Southern Mid-Atlantic and Northern Gulf oysters and Pacific Northwest mytilids. This group of parasites can be contrasted to the major pathologies and most of the remaining common unicellular eukaryotic parasites, such as Perkinsus marinus, and the gill ciliates, which more often showed temporal trends when significant temporal variations were present.
Significant year-to-year variation is arguably to be expected. Interestingly, one relatively common parasite, particularly in oysters, showed no significant trends of any kind: these were the trematode sporocysts, such as Bucephalus in oysters. The haplosporidians shared this characteristic, but this parasite group was restricted regionally in comparison with the trematode sporocysts (Powell & Kim 2015). For the remaining, the nonproliferating parasites such as the multicellular parasites and Nematopsis tended to have significant variation without trend and the major pathologies and the proliferating parasites, or those that might be so characterized by their ability to reproduce within the host such as the gill ciliates (Karatayev et al. 2000), tended to have significant variation with trend, the exception in the latter case being the prokaryotic inclusions and the ciliates in the alimentary canal.
Summary of Trends
The Mussel Watch dataset exhibits a host of significant year-to-year variations over the 1995 to 2010 time frame with patterns that are of potential interest in determining how the sentinel bivalves and their parasites and pathologies respond to local yearly forcing, regional environmental trends, and continental-scale climatology. In general, regional or larger-scale continental trends were produced by single-celled proliferating parasites, the pathologies, and physiological indices. The physiological indices were the most noteworthy in scale and taxon extensiveness. In contrast, the multicellular eukaryotes and the gregarines often showed significant year-to-year changes, but trends of any kind were observed to be much rarer. In fact, strong year-to-year differences were observed only five times, trematode metacercariae in mytilids from the Gulf of Maine, cestodes in Southern Mid-Atlantic and Western Gulf oysters, and nematodes in the Western Gulf and Northern Gulf oysters. Looking at regional trends, parasites were prominently represented in oysters on the Atlantic and Gulf Coasts and mytilids on the West Coast. Pathologies by contrast had strong temporal signals in northeastern mytilids.
Physiological characteristics likely influenced by food supply and nutrition vary over spatial scales of continental to near-continental scope. Parasites and pathologies did not do so to so great an extent, at least in part due to the differential in composition of parasite taxa and differential degree of occurrence of pathology shown by mytilids and oysters which de facto limited the geographic scale to the regions from which each species was sampled in most cases. Regional trends were commonly observed, however, for pathologies and a selection of unicellular parasites capable of proliferation, whereas multicellular eukaryotes and unicellular eukaryotes that do not proliferate in the bivalve host were most often characterized by year-to-year variations without trend when significant variations existed. The latter typically have additional hosts in the life cycle capable of independently exerting year-to-year variations in weighted prevalence; thus, local forcing might be anticipated to overwhelm regional trends as other components of the life cycle likely respond differentially to regional shifts in climatology.
The continental scale variations observed in many of the physiological characteristics offer a number of concerns. First, many contaminants interact profoundly with physiological characteristics in the mode of accumulation and depuration and in the physiological impact exerted at high contaminant body burdens (Ellis et al. 1993, Moraga et al. 2005, Buisson et al. 2008. Barrera-Escorcia et al. 2010. Baussant et al. 2011). Accordingly, evaluating trends in contaminant body burden requires also evaluating trends in the physiological state of the bivalve. The scale at which physiological characteristics vary and the fact that some aspects of this variance show coherent trends across sentinel species would suggest that continental-scale climatology may exert a degree of uniformity in influence that would find final expression at the level of regional trends in contaminant body burdens, ultimately, the target of programs such as Mussel Watch. The original design of the Mussel Watch Program, which included these physiological characteristics, would seem prescient in this regard.
Second, many parasites showed significant year-to-year variation, at least in certain regions, and similar parasites are known to accumulate selected contaminants (Sures et al. 1999, Heinonen et al. 2001, Nhi et al. 2013). Some of these parasites, the trematode sporocysts being good examples (Powell et al. 1999, Hechinger et al. 2009), can be significant components of tissue mass. Thus, year-to-year changes in parasite infection intensity or sampling location, such as the biennial sampling protocol in Mussel Watch, may introduce coherent and, under certain circumstances, spurious temporal variations in selected tissue contaminants. Kim et al. (1998, 1999, 2001, 2008) observed significant spatial and temporal correlations between certain contaminants and the pathologies and parasites monitored in the Mussel Watch Program and oscillations in regional values imposed by biennial sampling have been identified in this analysis.
Analysis of the 1995 to 2010 Mussel Watch dataset demonstrates a need for continental-scale monitoring of key coastal indicators of environmental and population health. Sentinel bivalves have been chosen historically due to their response to contaminants as "sponges," their sessility, their relatively large geographic range, and, in some cases, their substantive environmental eurytopy (Green et al. 1983, Jackson et al. 1994, Vaisman et al. 2005). Bivalves also are often biomass dominants, have unusually high parasite body burdens in comparison with many marine species, and are known to succumb to a range of pathologies some of which would appear to be life threatening and others at least physiologically degrading; thereby exposing themselves to a range of mediators of population health, including food supply, conditions resulting in pathologies, and a range of local- and regional-scale transmission dynamics for a wide range of parasites. These mediators provide the mechanism to generate regional and larger scale responses to climate change, both cyclical and directional, which provide bellwethers of change in the dynamics of the coastal region. The termination of the Mussel Watch Program represents an unfortunate failure to maintain an important and cost-effective long-term time series capable of informing management of coastal ecosystems.
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 and the staff and students at Rutgers University Haskin Shellfish Research Laboratory that assisted with sample processing and 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) * YUNGKUL KIM (2) AND DAVID BUSHEK (3)
(1) Gulf Coast Research Laboratory, University of Southern Mississippi, 703 East Beach Drive, Ocean Springs, MS 39564; (2) Departments of Integrated Environmental Science and Natural Sciences, Bethune-Cookman University, 640 Dr. Mary McLeod Bethune Boulevard, Daytona Beach, FL 32114; (3) Haskin Shellfish Research Laboratory, Rutgers University, 6959 Miller Avenue, Port Norris, NJ 08349
* Corresponding author. E-mail: firstname.lastname@example.org
TABLE 1. Results of analysis of variance analyses. Great Lakes/ Gulf of Southern Hudson River Maine New England Total counted parasites 0.0018 -- -- Total counted parasites less 0.0018 -- -- Nematopsis Total counted rare parasites 0.0013 -- -- Prokaryotic inclusions NA -- -- Total Nematopsis NA NA NA Nematopsis, body tissue only NA NA NA Nematopsis, mantle tissue only NA NA NA Nematopsis, gill tissue only NA NA NA Ciliates, alimentary canal NA -- -- only Ciliates, gill tissue only NA -- -- Haplosporidians NA NA NA Perkinsus marinus NA NA NA Trematode sporocysts NA -- -- Nematodes -- NA NA Cestodes NA NA NA Trematode metacercariae -- 0.0073 -- Major pathologies 0.0027 -- -- Tissue pathologies -- -- -- Ceroid bodies <0.0001 <0.0001 <0.0001 Digestive gland atrophy 0.0018 0.0099 -- Sex ratio -- -- -- Gonadal state -- -- -- Length 0.021 0.0008 0.048 Northern Southern Mid- Mid- Atlantic Atlantic Bight Bight Southeast Total counted parasites -- -- -- Total counted parasites less -- -- -- Nematopsis Total counted rare parasites -- -- 0.019 Prokaryotic inclusions 0.032 0.045 -- Total Nematopsis NA -- -- Nematopsis, body tissue only NA -- -- Nematopsis, mantle tissue only NA -- -- Nematopsis, gill tissue only NA -- -- Ciliates, alimentary canal -- -- -- only Ciliates, gill tissue only -- -- -- Haplosporidians NA -- -- Perkinsus marinus NA -- -- Trematode sporocysts -- -- -- Nematodes NA -- -- Cestodes NA 0.033 -- Trematode metacercariae -- NA NA Major pathologies 0.0044 NA -- Tissue pathologies -- 0.0008 -- Ceroid bodies 0.0028 0.044 0.0098 Digestive gland atrophy 0.042 0.0007 0.0041 Sex ratio SB 0.019 -- Gonadal state -- -- <0.0001 Length 0.0059 <0.0001 0.0189 Eastern Eastern Western Florida Gulf Gulf Total counted parasites -- 0.0026 -- Total counted parasites less -- -- -- Nematopsis Total counted rare parasites -- -- 0.0065 Prokaryotic inclusions -- -- -- Total Nematopsis -- 0.0042 -- Nematopsis, body tissue only -- -- 0.0061 Nematopsis, mantle tissue only -- -- 0.025 Nematopsis, gill tissue only -- 0.0023 -- Ciliates, alimentary canal -- -- -- only Ciliates, gill tissue only -- -- 0.039 Haplosporidians NA NA NA Perkinsus marinus -- <0.0001 <0.0001 Trematode sporocysts -- -- -- Nematodes -- -- 0.0095 Cestodes -- -- 0.0018 Trematode metacercariae -- -- -- Major pathologies -- 0.0037 -- Tissue pathologies 0.0012 0.0003 0.002 Ceroid bodies -- 0.023 0.0016 Digestive gland atrophy -- 0.0002 0.0074 Sex ratio -- 0.021 0.015 Gonadal state 0.042 0.0008 0.0007 Length -- <0.0001 <0.0001 Northern Southern Southern Gulf Gulf California Total counted parasites -- -- -- Total counted parasites less -- -- -- Nematopsis Total counted rare parasites -- -- 0.0015 Prokaryotic inclusions 0.045 -- -- Total Nematopsis -- -- -- Nematopsis, body tissue only -- -- -- Nematopsis, mantle tissue only -- 0.0065 0.02 Nematopsis, gill tissue only -- -- -- Ciliates, alimentary canal -- -- NA only Ciliates, gill tissue only 0.043 -- -- Haplosporidians NA NA NA Perkinsus marinus <0.0001 0.0009 NA Trematode sporocysts -- -- NA Nematodes 0.0007 -- NA Cestodes -- -- NA Trematode metacercariae -- -- -- Major pathologies 0.042 -- <0.0001 Tissue pathologies 0.0003 0.05 <0.0001 Ceroid bodies 0.0015 -- 0.0006 Digestive gland atrophy <0.0001 <0.0001 <0.0001 Sex ratio 0.003 -- 0.0019 Gonadal state 0.035 0.0052 0.0002 Length <0.0001 0.0025 <0.0001 Pacific Pacific Central Northwest Alaska Total counted parasites <0.0001 -- -- Total counted parasites less 0.0002 -- -- Nematopsis Total counted rare parasites 0.0008 -- -- Prokaryotic inclusions -- 0.013 -- Total Nematopsis 0.0004 -- -- Nematopsis, body tissue only 0.001 -- -- Nematopsis, mantle tissue only 0.033 -- NA Nematopsis, gill tissue only 0.0003 -- -- Ciliates, alimentary canal 0.0083 -- -- only Ciliates, gill tissue only <0.0001 -- -- Haplosporidians NA NA NA Perkinsus marinus NA NA NA Trematode sporocysts -- -- -- Nematodes NA NA NA Cestodes NA NA NA Trematode metacercariae -- -- -- Major pathologies 0.021 -- -- Tissue pathologies 0.0005 0.0029 -- Ceroid bodies <0.0001 -- -- Digestive gland atrophy <0.0001 0.042 0.022 Sex ratio -- 0.03 -- Gonadal state -- 0.0017 -- Length <0.0001 0.046 -- Significant differences indicate situations where the year main effect was significant. -, Not significant at [alpha] = 0.05; NA, insufficient or absence (e.g., parasite not present) of data. Regions are defined in the Materials and Methods section. TABLE 2. Results of Spearman's rank correlations. Great Lakes/ Gulf Southern Hudson of New River Maine England Total counted parasites -- -- -- Total counted parasites -- -- -- less Nematopsis Total counted rare -- -- -- parasites Prokaryotic inclusions NA -- -- Total Nematopsis NA NA NA Nematopsis, body tissue NA NA NA only Nematopsis, mantle NA NA NA tissue only Nematopsis, gill tissue NA NA NA only Ciliates, alimentary NA -- -- canal only Ciliates, gill tissue only NA -- -- Haplosporidians NA NA NA Perkinsus marinus NA NA NA Trematode sporocysts NA -- -- Nematodes -- NA NA Cestodes NA NA NA Trematode metacercariae -- -- Major pathologies (0.0064) 0.008 (0.013) Tissue pathologies -- -- -- Ceroid bodies (0.0004) (0.0003) (<0.0001) Digestive gland atrophy (0.025) (0.0003) -- Sex ratio -- -- -- Gonadal state -- -- -- Length -- (0.0003) -- Northern Southern Mid-Atlantic Mid-Atlantic Bight Bight Southeast Total counted parasites -- -- -- Total counted parasites -- -- 0.01 less Nematopsis Total counted rare -- -- -- parasites Prokaryotic inclusions -- -- 0.0089 Total Nematopsis NA -- -- Nematopsis, body tissue NA -- -- only Nematopsis, mantle NA -- -- tissue only Nematopsis, gill tissue NA -- -- only Ciliates, alimentary -- 0.023 -- canal only Ciliates, gill tissue only -- -- 0.012 Haplosporidians NA -- -- Perkinsus marinus NA -- -- Trematode sporocysts - -- -- Nematodes NA -- -- Cestodes NA 0.05 -- Trematode metacercariae -- NA NA Major pathologies -- NA -- Tissue pathologies -- -- -- Ceroid bodies (0.022) (0.0057) -- Digestive gland atrophy (0.017) (0.018) (<0.0001) Sex ratio -- 0.044 -- Gonadal state -- 0.049 (0.0015) Length (0.0014) (0.0004) -- Eastern Eastern Western Florida Gulf Gulf Total counted parasites -- -- -- Total counted parasites -- -- -- less Nematopsis Total counted rare -- -- -- parasites Prokaryotic inclusions -- -- -- Total Nematopsis -- -- -- Nematopsis, body tissue -- -- -- only Nematopsis, mantle -- -- -- tissue only Nematopsis, gill tissue -- 0.017 -- only Ciliates, alimentary -- -- -- canal only Ciliates, gill tissue only -- 0.0008 -- Haplosporidians NA NA NA Perkinsus marinus -- (<0.0001) (<0.0001) Trematode sporocysts -- -- -- Nematodes -- -- -- Cestodes -- -- -- Trematode metacercariae -- -- -- Major pathologies -- -- -- Tissue pathologies -- -- -- Ceroid bodies -- -- -- Digestive gland atrophy (0.0008) (<0.0001) (0.0007) Sex ratio -- 0.0022 -- Gonadal state -- -- -- Length -- (0.0053) (0.0003) Northern Southern Southern Gulf Gulf California Total counted parasites -- -- -- Total counted parasites -- -- -- less Nematopsis Total counted rare -- -- -- parasites Prokaryotic inclusions -- -- -- Total Nematopsis -- -- -- Nematopsis, body tissue -- -- 0.022 only Nematopsis, mantle -- -- 0.019 tissue only Nematopsis, gill tissue -- -- -- only Ciliates, alimentary -- -- NA canal only Ciliates, gill tissue only 0.0009 -- 0.022 Haplosporidians NA NA NA Perkinsus marinus (<0.0001) (0.033) NA Trematode sporocysts -- -- NA Nematodes -- -- NA Cestodes -- -- NA Trematode metacercariae -- -- 0.0002 Major pathologies -- -- -- Tissue pathologies -- -- -- Ceroid bodies -- -- -- Digestive gland atrophy (<0.0001) (<0.0001) (0.0002) Sex ratio 0.0035 -- -- Gonadal state -- -- -- Length (<0.0001) -- -- Pacific Pacific Central Northwest Alaska Total counted parasites -- -- 0.0116 Total counted parasites (0.046) -- 0.037 less Nematopsis Total counted rare -- -- -- parasites Prokaryotic inclusions -- -- -- Total Nematopsis -- -- -- Nematopsis, body tissue -- -- -- only Nematopsis, mantle -- -- NA tissue only Nematopsis, gill tissue -- -- -- only Ciliates, alimentary (0.0056) -- -- canal only Ciliates, gill tissue only (0.042) 0.048 0.0064 Haplosporidians NA NA NA Perkinsus marinus NA NA NA Trematode sporocysts -- -- -- Nematodes NA NA NA Cestodes NA NA NA Trematode metacercariae -- 0.025 -- Major pathologies (0.043) -- -- Tissue pathologies -- -- -- Ceroid bodies -- -- -- Digestive gland atrophy (0.017) (0.0002) (0.041) Sex ratio -- -- -- Gonadal state (0.0079) -- -- Length -- -- -- Significant differences without parentheses indicate a rising score through the time series. Significant differences within parentheses indicate a declining score through the time series-, Not significant at [alpha] = 0.05; NA, insufficient or absence (e.g., parasite not present) of data. Regions are defined in the Materials and Methods section. TABLE 3. Results of Durbin-Watson tests for autocorrelation. Great Lakes/ Southern Hudson Gulf of New River Maine England Total counted parasites -- -- -- Total counted parasites -- -- -- less Nematopsis Total counted rare -- -- -- parasites Prokaryotic inclusions -- -- -- Total Nematopsis NA NA NA Nematopsis, body tissue NA NA NA only Nematopsis, mantle tissue NA NA NA only Nematopsis, gill tissue NA NA NA only Ciliates, alimentary canal -- -- -- only Ciliates, gill tissue only -- -- -- Haplosporidians NA NA NA Perkinsus marinus NA NA NA Trematode sporocysts NA (0.0092) -- Nematodes -- NA NA Cestodes NA NA NA Trematode metacercariae NA -- -- Major pathologies -- -- -- Tissue pathologies -- -- -- Ceroid bodies 0.014 -- -- Digestive gland atrophy -- -- -- Sex ratio -- -- -- Gonadal state -- -- -- Length -- -- 0.041 Northern Southern Mid-Atlantic Mid-Atlantic Bight Bight Southeast Total counted parasites -- -- 0.028 Total counted parasites -- -- -- less Nematopsis Total counted rare -- -- -- parasites Prokaryotic inclusions -- -- -- Total Nematopsis NA -- 0.036 Nematopsis, body tissue NA -- 0.034 only Nematopsis, mantle tissue NA -- -- only Nematopsis, gill tissue NA -- -- only Ciliates, alimentary canal 0.043 -- -- only Ciliates, gill tissue only -- -- 0.036 Haplosporidians NA -- -- Perkinsus marinus NA 0.043 -- Trematode sporocysts -- -- -- Nematodes NA (0.029) -- Cestodes NA -- -- Trematode metacercariae -- NA NA Major pathologies -- NA -- Tissue pathologies -- -- 0.0013 Ceroid bodies -- -- -- Digestive gland atrophy -- -- -- Sex ratio -- -- -- Gonadal state -- -- -- Length -- -- -- Eastern Eastern Western Florida Gulf Gulf Total counted parasites NA -- -- Total counted parasites NA -- -- less Nematopsis Total counted rare NA -- -- parasites Prokaryotic inclusions NA -- (0.053) Total Nematopsis NA -- -- Nematopsis, body tissue NA -- -- only Nematopsis, mantle tissue NA -- -- only Nematopsis, gill tissue NA -- -- only Ciliates, alimentary canal NA -- -- only Ciliates, gill tissue only NA -- 0.024 Haplosporidians NA NA NA Perkinsus marinus NA 0.049 -- Trematode sporocysts NA -- -- Nematodes NA -- -- Cestodes NA -- -- Trematode metacercariae NA -- -- Major pathologies NA -- -- Tissue pathologies NA 0.033 0.038 Ceroid bodies NA -- -- Digestive gland atrophy NA -- -- Sex ratio NA -- -- Gonadal state NA -- 0.031 Length NA -- -- Northern Southern Southern Gulf Gulf California Total counted parasites -- -- -- Total counted parasites 0.0077 -- -- less Nematopsis Total counted rare -- -- -- parasites Prokaryotic inclusions -- -- -- Total Nematopsis -- -- -- Nematopsis, body tissue -- -- -- only Nematopsis, mantle tissue -- -- 0.025 only Nematopsis, gill tissue -- -- -- only Ciliates, alimentary canal -- -- NA only Ciliates, gill tissue only -- -- 0.003 Haplosporidians NA NA NA Perkinsus marinus -- -- NA Trematode sporocysts -- -- NA Nematodes -- -- NA Cestodes -- -- NA Trematode metacercariae -- -- -- Major pathologies -- -- -- Tissue pathologies -- 0.035 (0.0035) Ceroid bodies -- -- -- Digestive gland atrophy -- -- -- Sex ratio -- -- -- Gonadal state -- -- -- Length -- -- -- Pacific Pacific Central Northwest Alaska Total counted parasites -- -- NA Total counted parasites -- -- NA less Nematopsis Total counted rare -- -- NA parasites Prokaryotic inclusions -- -- NA Total Nematopsis -- -- NA Nematopsis, body tissue -- -- NA only Nematopsis, mantle tissue -- -- NA only Nematopsis, gill tissue -- -- NA only Ciliates, alimentary canal 0.052 -- NA only Ciliates, gill tissue only -- -- NA Haplosporidians NA NA NA Perkinsus marinus NA NA NA Trematode sporocysts -- -- NA Nematodes NA NA NA Cestodes NA NA NA Trematode metacercariae -- -- NA Major pathologies -- -- NA Tissue pathologies -- -- NA Ceroid bodies -- -- NA Digestive gland atrophy -- -- NA Sex ratio -- -- NA Gonadal state -- -- NA Length -- 0.0005 NA Significant differences without parentheses indicate positive autocorrelation within the time series. Significant differences within parentheses indicate negative autocorrelation within the time series-, Not significant at [alpha] = 0.05; NA, insufficient or absence (e.g., parasite not present) of data. Regions are defined in the Materials and Methods section.
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|Author:||Powell, Eric N.; Kim, Yungkul; Bushek, David|
|Publication:||Journal of Shellfish Research|
|Date:||Dec 1, 2015|
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