Surfclam histopathology survey along the Delmarva mortality line.
KEY WORDS: surfclam, Spinsula, histopathology
Surf clams, Spisula solidissima, support one of the largest fisheries in the Mid-Atlantic Bight and represent a biomass dominant for much of the inner half of the continental shelf of that region (Merrill & Ropes 1969, Weinberg 1998, Weinberg 1999, NEFSC 2003), Prior to 1999, surf clams were abundant from northern Virginia to inshore Long Island, with discontinuous but significant abundances along the southern New England coast and onto Georges bank (Theroux & Wigley 1983, NEFSC 2003). In 1999, estimated stock biomass, just in the Exclusive Economic Zone (EEZ), exceeded 1 million MT (NEFSC 2003), a stock biomass estimated to be at or near carrying capacity throughout much of the surf clam's range. Surf clams are long-lived, exceeding 30 y in the oldest specimens (Weinberg 1999). Natural mortality rate is estimated to be 0.15 [y.sup.-1] and current fishing mortality rate is less than half this value (NEFSC 2003). Changes in adult abundance thus occur slowly as a consequence of normal population dynamics.
The 2002 National Marine Fisheries Service--Northeast Fisheries Science Center (NMFS-NEFSC) survey revealed a substantial reduction in surf clam abundance off the Delmarva Peninsula (NEFSC 2003). Weinberg (1998) had earlier documented that clams in this region were slower growing than clams from more northern climes. NEFSC (2003) documented that the increased mortality since 1999 was focused inshore of a southeast trending line extending from approximately the Delaware Bay mouth to the central continental shelf off the month of Chesapeake Bay. Figure 1 shows the NMFS-NEFSC catches of surf clams during the 2002 survey in this region. No living surf clams were caught inshore of this mortality line, in contrast to the pre-1999 period when surf clams were caught in abundance over much of this area. Since 1999, yearly mortality rate has been well above the stock-wide average of 0.15 [y.sup.-1] previously estimated for this region. The southeastern trend, which follows more or less the isothermic structure of the region, supports the assumption that an underlying causal influence is rising sea temperatures. Weinberg et al. (2002) suggested that increasing temperatures in the Mid-Atlantic Bight associated with global temperature rise might significantly influence surfclam growth and mortality.
[FIGURE 1 OMITTED]
A recent survey of inshore Maryland waters by Powell (2003) reoccupying stations originally sampled by Loesch and Ropes (1977) found few living surf clams inshore of the EEZ along the same stretch of coastline. Although the time when surf clams disappeared from this inshore region is not well-documented, the inshore survey expanded the zone south of Delaware Bay where surf clams, once abundant, are no longer significant contributers to community biomass. The 2003 inshore New Jersey survey carried out by the New Jersey Department of Environmental Protection documents a substantial decline in the abundance of surf clams inshore of the EEZ off New Jersey as well (NJDEP, personal communication), suggesting that a widespread range contraction along the southern and inshore range boundary of the surf clam may be underway. This boundary probably is determined by temperature, as surf clams do not survive well over the summer in more southern climes (Spruck et al. 1995, O'Beirn et al. 1997) and summer temperature determines faunal boundaries of many species within the Virginian biogeographic province (Cerame-Vivas & Gray 1966).
Surf clams enter high temperature stress when temperatures exceed 23[degrees]C or thereabouts (Loosanoff & Davis 1963, Cable & Landers 1974, Goldberg 1989, Clotteau & Dube 1993, Walker et al. 1997). Weinberg et al. (2002) observed that bottom water temperatures in the offshore Delmarva region were unlikely to exceed these levels. Thus, a direct effect of temperature as an agent of mortality seems unlikely. However, small increments in temperature above optimal can significantly impact scope for growth in bivalves, a phenomenon often made most manifest in the larger adult animals (Taylor 1960, Hofmann et al. 1994), and temperature-dependent diseases and pathologies are well-known (e.g., Miller & Lawrenz-Miller 1993, Powell et al. 1996, Cook et al. 1998). Either could mediate the influence of temperature as it ultimately modulates the rate of natural mortality. To investigate further the proximate causes of mortality, we carried out a histopathological survey of surf clams collected along the southeast trending "mortality" line.
Sample Collection and Preparation
Samples were collected by the F/V Betty C, homeport Ocean City, Maryland, on August 28, 2003. The cruise track ran the mortality line from offshore of the Maryland/Virginia border to about the latitude of the mouth of Chesapeake Bay (Fig. 1). A selection of seven of the inshore-most stations at which the 2002 NEFSC survey found living surf clams was resampled. An additional two stations (stations 2 and 3, Figure 1) were sampled based on captains' reports of "sickly-looking" surf clams in commercial catches.
Samples were taken by hydraulic dredge (Wallace & Hoff, in press). Between 10 and 15 animals, catch being sufficient, were selected from each dredge haul for histopathological analysis (Table 1). In all, 105 surf clams were analyzed. The maximum anterior-posterior shell length of each animal was measured. Measured animals were then opened immediately using a stainless steel knife by cutting the adductor muscles. The shucked clam meats were placed in a bucket of seawater, rinsed to remove sand and other hard particles forced into the mantle cavity during capture, drained, and weighed. Immediately after weighing, a 2-cm-thick dorsal-ventral cross-section of tissue including visceral mass, mantle, gill and foot, was removed from each clam using a scalpel. Each section was stored in a glass jar filled with Davidson's fixative for two days until replaced by 70% ethanol for storage (Ellis et al. 1998a).
Methods followed NOAA Status and Trends protocols (Ellis et al. 1998a, Ellis et al. 1998b) except that tissue subsections were excised prior to embedding due to the large size of the clam cross-sections, rather than embedding an entire cross-section. Target tissues included mantle, gill, kidney, gonad, digestive gland, and connective tissue. Tissue samples were embedded in paraffin after dehydration and clearing. The paraffin-embedded tissue blocks were first sliced at 20 [micro]m to expose an entire tissue section. The tissue-paraffin block was then placed in a freezer overnight before final sectioning at 5 [micro]m. Tissue sections were deparaffinized and hydrated using a xylene-ethanol series, stained in a pentachrome series, dehydrated in a series of acetic acid dips followed by acetone, cleared in xylene, and mounted in Permount (Ellis et al. 1998b).
Tissue sections were examined under the microscope using a 10x ocular and a 10x objective. When necessary, a 25x or 40x objective was used for closer examination. All parasites and pathologies were scored for intensity based on either a quantitative or semi-quantitative scale. Quantitative scores were used for parasites that could be tallied individually, including prokaryotic inclusion bodies, nematodes, and cestodes. Each nematode cross-section observed was counted, although a single individual may be responsible for a number of tissue cross-sections. Certain tissue pathologies were also quantified by direct counts, including intense localized (focal) or diffuse infiltration of hemocytes.
Some conditions were assigned to semiquantitative scales depending on the intensity or extensiveness of the affected area. These include so-called digestive gland atrophy, characterized by thinning of the digestive tubule epithelium, and abnormal gonadal development, characterized either by unusual development of gametes at the base of the follicles, by an elevated presence of foreign cells and cellular debris in the follicles, or by immature gametes floating free within the follicular lumen. The semiquantitative scales used are defined in Tables 2 and 3.
Discretely counted parasites and pathologies, such as focal and diffuse infiltration of hemocytes, nematodes, and cestodes, were described in terms of their prevalence and infection intensity. Prevalence, the fraction of individuals with the parasite or pathology, was calculated as:
Number clams affected/Number clams analyzed
Infection intensity, the average number of occurrences of a parasite or pathology in the infected individuals only, was calculated as:
[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII.]
Certain statistical procedures, such as principal components analysis (PCA), necessitated combining uninfected and infected individuals by giving the uninfected individuals an infection intensity of 0. The average value, termed weighted prevalence or mean abundance, was calculated as
Prevalence x infection intensity.
Tissue disorders measured using semiquantitative scales, such as digestive gland atrophy and abnormal gonadal development, were described in terms of the arithmetic mean of their semiquantitative-scale values.
Condition index was calculated as:
Wet meat weight (g)/length (mm).
Gametogenic stage was assigned based on the stages set forth for mussels by Ellis et al. (1998a) (Table 4). These stages can be condensed into the simpler groupings of Ropes (1968). For some statistical analyses, the gametogenic stages were compressed into three larger categories: developing gonad (all D stages, Table 4), fully developed or ripe gonad (stage 5, Table 4), and spawning and partially spent gonad Call S stages, Table 4).
Condition index was lowest at stations 2, 3, 8, and 9 (Table 1). Average condition index was at or below 0.60 g [mm.sup.-1] for three of these stations, about 34% lower than the station with the highest average, station 6. The most northern group of stations and the most southern station, station 1, had the highest condition indices, averaging above 0.80 g [mm.sup.-1].
Most surf clams at the northern stations were in a late stage of gonadal development or ready to spawn (Tables 1 and 5). Most surf clams at the southern stations had begun spawning, but few animals had completed spawning. Spent animals were rare (Table 5). These observations generally agree with Ropes (1968) (see also Jones 1981, Chintala & Grassle 1995).
Two parasites were common, nematodes and cestodes. Larval cestodes were found in nearly all tissues. Cestodes were reported in Spisula similis by Cake (1977), but appear to be undocumented previously in S. solidissima. Most cestodes were observed in either the digestive gland, particularly the connective tissue around the gut or attached to the gut epithelium (Plate 1), or in the gonads. A complete accounting of observations by tissue type is: digestive gland (201 observations), gonad (61 observations), mantle (15), kidney (10), blood vessels (10), foot (6), muscle tissue (4), and gill (1). The formation of a thick tissue capsule surrounding the cestode was a frequently observed host reaction. Encapsulated cestodes appeared to be disintegrating and in the process of resorption.
Cestode prevalence fell below 50% only at station 2. Surf clams infected by cestodes were most common at stations 1, 7, and 9, where prevalence reached or exceeded 85% (Table 6). These are among the most southern stations. Cestode infection intensity was highest at stations 6, 8, and 9. Infection intensity exceeded 6 observations per clam subsection in surf clams taken from these stations (Table 6).
Larval nematodes were observed in nearly all tissues of surf clams in this study: gonad (77 observations, Plate 2), digestive gland (23 observations), the visceral mass between the body wail and the underlying muscle layer (17), foot (8), muscle tissue (2), and gill (1). In some cases, no conspicuous host response was observed. Frequently, however, hemocyte infiltration was observed in association with the worm. Nematodes were found in surf clams collected from all stations (Table 6). Prevalence was highest, exceeding 50%, at stations 1, 7, and 8. Two of these stations are among the three stations in which cestode prevalence was highest. The high prevalence of nematodes in surf clams off the Delmarva Peninsula is anticipated from previous reports. Nematodes were observed to frequently parasitize surf clams by Lichtenfels et al. (1976, 1978) and Perkins et al. (1975). Nematode infection intensity was highest, reaching at least 3 observations per clam subsection, at stations 1, 4, and 5, but exceeded 2 observations per clam subsection at all stations (Table 6). The distribution of nematode infection intensity diverged markedly from that of cestode infection intensity.
A variety of other parasites were found sporadically, including prokaryotic inclusions, often termed rickettsial or chlamydial bodies (Ellis et al. 1998b), also reported to infect surf clams by Otto et al. (1979), an unidentified worm, and the haplosporidian hyperparasite of larval nematodes, previously reported by Lichtenfels et al. (1978), Payne et al. (1980), Perkins (1979), and Perkins et al. (1975). Prevalence of prokaryotic inclusions was 16%, nearly all cases being located in the digestive tract epithelium. Haplosporidians were observed rarely, hyperparasitizing nematodes in only 4% of the surf clams harboring nematode parasites. One surf clam was observed to have two unidentified worms, one in the mantle and the other in the foot, similar to the echinostomes observed in the gonoducts of Gulf of Mexico oysters by Ellis et al. (1998b) and later identified by Winstead et al. (1998).
Pathologies and Related Conditions
Despite the nomenclatural connotations, neither digestive gland atrophy nor the disorders referred to as abnormal gonadal development are necessarily pathologic. Digestive gland atrophy manifests itself as a thinning of the digestive tubule cells (Ellis et al. 1998b; Table 2). The condition appears to be representative of poor nutrition in some bivalves (e.g., Palmer 1979, Winstead 1995), but may result from a variety of environmental stressors (e.g., da Ros et al. 1998, Axiak et al. 1988, Marigomez et al. 1990, Gold-Bouchot et al. 1995), although many of these likely also affect nutrition. Winstead (1995), for example, found that poor nutrition was a key element in producing the condition in oysters and that the digestive gland recovered to its normal state relatively rapidly once food supply improved. Therefore, digestive gland atrophy is not necessarily a pathology.
The origin of digestive gland atrophy in surf clams is unknown. Digestive gland atrophy was highest at the more southerly stations (Table 6). Averages at stations 1-3 and 8-9 were above 2 on a 0-4-point scale (Plate 3).
Putative cases of abnormal gonadal development was observed in some surf clams. This set of disorders was characterized by one or more of three conditions. In some cases, gametes developed in an unusual way at the base of the follicles. Follicles sometimes were filled with degenerating gametes and cellular debris beyond the extent normally observed at the end of the spawning cycle (Plate 4, left; Plate 5). Occasionally, immature eggs were observed floating free in the lumen of the follicle (Plate 4, right). The approach used to score instances of abnormal gonadal development was to estimate the traction of follicles affected, not the degree of effect in each follicle (Table 3). Normally, the entire follicle was completely affected or unaffected. Putative gonadal abnormalities were observed at all stages of the gametogenic cycle (Table 5), so that the possibility that these disorders represent normal phases of gametogenic development seems low. Nevertheless, the origin of the gonadal abnormalities summarized in Table 6 is unknown, as are their statuses as normal or pathologic conditions. Cases of abnormal gonadal development were most common at stations 3, 7, and 8 (Table 6).
Cases of hemocytic infiltration may be focal (localized) (Plate 6) or diffuse (extensive). The type of affected tissue and type of irritation responsible influence the nature of the cellular response (Ford & Tripp 1996). Diffuse infiltration of hemocytes is differentiated from focal infiltration when the affected area does not appear to have a clear center or focal point of highest hemocyte concentration and hemocytes are abundant and distributed broadly over a large section of tissue (Ellis et al. 1998b). In this study, instances of hemocytic infiltration were observed mostly in the connective tissues.
Animals with observed cases of focal hemocytic infiltration were most common at stations 1, 5, and 8 (Table 6); prevalences reached or exceeded 90% at these stations. In contrast, the frequency of focal hemocytic infiltration was highest at stations 1, 7, and 9, where intensity averaged near or above 2.5 observations per clam tissue subsection. These stations had highest prevalences of nematodes and subsequent statistical analyses support the belief that the two, nematodes and focal infiltration of hemocytes (Plate 6), often are associated. Prevalence of diffuse hemocytic infiltration was highest at stations 1, 7, and 9 (Table 6), where prevalence reached or exceeded 50%. Frequency of occurrence in individual clams, however, was highest at stations 2, 3, and 7. The occurrence of diffuse hemocytic infiltration was not obviously associated with either of the common parasites, nematodes or cestodes.
Association of Parasites, Pathologies, and Other Indicators of Health
We assumed that condition index was a good overall indicator of animal health and examined the relationship between condition index and the common parasites, pathologies and other tissue disorders. We focused on infection intensity, rather than prevalence. Condition index is the ratio of wet weight to length. However, this ratio is not constant over all size classes. Typically, the shell growth form changes with age, such that shell width increases disproportionately with shell length. As a consequence, larger clams typically have a disproportionately larger weight per centimeter of length, and, accordingly, condition index tends to average higher. Preliminary analyses confirmed that some histopathological variables were better explained by shell length than by weight or condition, as a consequence of the dichotomous nature of length. For this reason, we first used principal components analysis (PCA) to separate the simple relationship between weight and length, encompassed in the measure of condition, from the additional effect of length, presumably reflecting the change in allometric growth form. This PCA provided two significant factors. Factor 1, hereafter referred to as the condition factor, combined the simple measurement of weight with condition index. The variable length was split, as anticipated, relatively evenly between factors 1 and 2, the latter hereafter referred to as the additional length factor.
We also used PCA analysis to generate variables describing the relationships of the various parasites, pathologies, and other tissue disorders because preliminary analyses indicated that many pairwise correlations were significant (Spearman's rank correlation, [alpha] = 0.05). Three PCA factors were significant. Factor 1, hereafter referred to as the nematode factor, combined the variables of nematode infection intensity and the frequency of focal hemocytic infiltration, thereby supporting a relationship between this parasite-tissue pathology pair. Factor 2, hereafter referred to as the abnormality factor, was principally determined by the mean intensity of gonadal abnormality scores. Cestode infection intensity loaded about evenly between these first two factors, probably because cestode prevalence and cestode infection intensity tended to be somewhat differentially distributed (Table 6). Factor 3, hereafter referred to as the atrophy factor, was primarily determined by the degree of digestive gland atrophy. Diffuse hemocytic infiltration did not contribute significantly to any of these three PCA factors.
ANOVAs were run using the condition and length factor scores as dependent variables, the nematode, abnormality, and atrophy factor scores as independent variables, and using sex and gametogenic stage compressed into the three categories of developing gonad, ripe gonad, and spawning or partially spent gonad as added main effects. The condition factor was significantly influenced by the abnormality factor (P = 0.0038). Low condition indices were associated with high levels of abnormal gonadal development (Fig. 2). Cestode infection intensity also loaded on this factor, and the highest cestode infection intensities were associated with a small reduction in condition index (Fig. 2), however, not to the extent observed for gonadal abnormalities (Fig. 2).
[FIGURE 2 OMITTED]
The length factor described that part of the variation in length not encompassed by the simple relationship of weight and length as expressed by condition. The length factor was significantly influenced by the degree of digestive gland atrophy, as expressed by the atrophy factor scores (P = 0.015). Highest digestive gland atrophy scores occurred in the smallest animals (Fig. 3). The same trend was present with condition index (Fig. 3), but this trend was not statistically significant when analyzed by comparison of the appropriate PCA scores. The main effects of sex and gametogenic stage were not significant.
[FIGURE 3 OMITTED]
The nematode factor, representing nematode infection intensity and the frequency of focal hemocytic infiltration, and partially explaining cestode infection intensity, did not significantly influence either the condition or the length factor (Fig. 4), nor were the main effects of sex or gametogenic stage significant.
[FIGURE 4 OMITTED]
We reserved the analysis, taking the nematode, abnormality, and atrophy factors as dependent variables and the length and condition factors as independent variables to determine the degree to which condition, length, gametogenic stage, or sex influenced the occurrence of parasites and pathologies. Sex and compressed gametogenic stage were again included as main effects. Not surprisingly, the atrophy factor as a dependent variable and the length factor as an independent variable were significantly related (P = 0.0074). The intensity of digestive gland atrophy varied with clam length (Fig. 3). The atrophy factor was not significantly influenced by sex nor, as might be expected, was it significantly influenced by gametogenic stage, or the condition factor. The abnormality factor, that expressed the severity of gonadal abnormality and, to a certain extent, cestode infection intensity, was significantly influenced by the condition factor (P = 0.0034). Higher gonadal abnormality scores occurred in animals with lower condition index (Fig. 2). Gametogenic stage also significantly influenced the abnormality factor scores (P = 0.02). An a posterior LS means test revealed that gonadal abnormalities, as expressed by the factor scores, were more severe within gametogenic stages in which evidence of spawning was present (S stages, Table 4) than with stages of gamete development (D stages, Table 4) (P = 0.03) or ripe gonads without evidence of spawning (stage 5, Table 4) (P = 0.0074). Animals rated as ready to spawn had lower gonadal abnormality scores than those in which some evidence of the initiation of spawning was present (Fig. 5). Cestode infection intensity varied little with gametogenic stage (Fig. 5), indicating that the primary effect determining the relationship between the abnormality factor and gametogenic stage was the degree of gonadal abnormality.
[FIGURE 5 OMITTED]
Factor one, jointly describing nematode infection intensity and the frequency of focal hemocytic infiltration, plus some portion of cestode infection intensity, was significantly influenced only by sex. Nematode factor scores were higher in males than in females (P = 0.043), as were nematode infection intensities (Fig. 6). The frequency of focal infiltration of hemocytes was also elevated, although to a lesser degree in males (Fig. 6).
[FIGURE 6 OMITTED]
We investigated the health of surf clams taken along the "mortality" line running southeast off the Delmarva Peninsula that separates stations that yielded no living surf clams in the 2002 NMFS survey (NEFSC 2003) from those where living surf clams were collected. Condition index may serve as a good overall indicator of animal health, once gametogenesis is taken into account, as condition normally varies with the gametogenic cycle (Beninger & Lucas 1984, Choi et al. 1993, Choi et al. 1994, Loesch & Evans 1994). Condition declines for many reasons, including low nutrition produced by restricted food supply (Engle & Chapman 1953, Deslous-Paoli & Heral 1988, Bielefeld 1991, Rheault & Rice 1996, Honkoop & Beukema 1997, Smith et al. 2000, Kraeuter et al. 2003) and by the influence of parasites and disease (Plana et al. 1996, Perez Camacho et al. 1997, Olivas Valdez & Caceres-Martinez 2002, Hine 2002).
The most northern stations, 4, 5, and 6, had the highest condition indices, the lowest gonadal abnormality scores, with one exception, and the lowest digestive gland atrophy scores. Animals at the stations with lowest average condition index had body weights less than 65% of the mean animal taken at station 6 with the highest condition index. We assume, from Weinberg et al. (2002), that surf clams at station 6 already averaged lower in condition index than clams from more northern climes, as condition index is normally lowest off the Delmarva Peninsula. The condition indices we recorded from clams at the southernmost stations occupied in this study were extremely low in comparison to values recorded by Loesch and Evans (1994) for the nadir of the normal seasonal cycle. Loesch and Evans (1994) recorded a drop in condition index of 20-25% in the late fall from summertime highs. Though exceptions exist (e.g., Heral & Deslous-Paoli 1983 Garton & Haag, 1993), most bivalves lose about 20-25% of their body weight upon spawning (Browne & Russell-Hunter 1978, Powell & Stanton 1985, Choi et al. 1994, DiBacco et al. 1995), so the observations of Loesch and Evans (1994) are typical of bivalves.
Larger reductions in condition index in bivalves, of the order observed at the more southern stations in this study, are often related to nutritional challenge. Perez Camacho et al. (1997), for example, record an approximately 50% decline in condition in parasitized Mytilus edulis. Beninger and Lucas (1984) record reductions in excess of 50% in Tapes clams during periods of reduced food supply, particularly over winter. Similar results are reported by Honkoop and Beukema (1997), Olivas-Valdez and Caceres-Martinez (2002), Barber et al. (1988), and others. Although a number of experiments subjected bivalves to long-term deprivation of food (e.g., Holland & Spencer 1973, Riley 1976, Riley 1980, Hawkins et al. 1985, Bielefeld 1991, Chase & McMahon 1994, Hummel et al. 1995), all of which show decreases in condition or body components related to condition, the degree to which bivalves can recover from a 30% to 50% loss of somatic tissue is poorly known. Leighton and Boolootian (1963) recorded one of the few measures of mortality due to starvation. They report that abalone began to die after a weight loss of 12-24% over a two- to three-month time period. Nevertheless, condition indices much below 30% of normal, as observed in this study at the southernmost stations, particularly during the summer months when condition should be at or above the long-term mean value (Loesch & Evans 1994), strongly imply that malnourished clams were common along the "mortality" line.
Additional evidence of malnutrition accrues from the tendency for stations yielding clams in lowest condition to also yield clams with above normal scores for abnormal gonadal development. In studies of the surf clam gametogenic cycle, neither Ropes (1968), Jones (1981), nor Chintala and Grassle (1995) figure gonadal conditions of this type. Although the origin of the gonadal abnormalities observed in these clams is unknown, as is the accuracy of their designation as abnormal, an unusual degree of gonadal resorption or loss of gonadal integrity does seem a likely cause. Gonadal resorption often occurs at the end of the gametogenic cycle (e.g., Ropes 1968, Griffiths 1977, Chung & Kim 1994. Ellis et al. 1998a), but resorption is also a frequent indicator of malnutrition (Riley 1976, Bielefeld 1991, Hofmann et al. 1992, Barber 1996, Delgado & Perez Camacho 2003). The correlation between low condition index and higher degrees of gonadal abnormality in this study suggests that the latter originates in the same causative factors that produce the unusually low condition indices.
Digestive gland atrophy also is normally associated with factors compromising nutritional status. In this study, highest scores of digestive gland atrophy tended to occur in smaller animals (Spearman's rank correlation, P = 0.0045). Smaller animals were collected at the more southern stations and these stations also were characterized by low condition index. Why digestive gland atrophy should be more significantly influenced by the additional length factor rather than the factor encompassing weight and condition is unknown.
A syndrome would appear to emerge from this data analysis. Animals with low condition are often animals with higher scores of gonadal abnormality and higher scores of digestive gland atrophy. Among the factors often associated with reduced condition, as well as impacting gonadal development (e.g., Powell et al. 1999, Arnold et al. 2002, Park et al. 2003), is parasitism and disease. Two parasites were commonly observed in the surf clams: nematodes and cestodes. Parasites of this type are rarely associated with overt pathologies, beyond the frequently observed inflammatory response characterized by focal hemocytic infiltration. Infection intensities were routinely higher than recorded in mussels and oysters from the east coast, however (Kim et al. 1998). Two pathologies were also recognized, local and diffuse hemocytic infiltration. One, focal infiltration of hemocytes, would appear to be related to the presence of worms, particularly parasitic nematodes.
Neither of the two parasites nor either of the pathologies, however, was significantly correlated with condition index or length, as expressed by comparisons between the appropriate PCA factor scores, save for the influence of cestode infection intensity in the PCA factor principally describing the occurrence of gonadal abnormality. By comparison, the PCA factors representing the disorders denoted as gonadal abnormality and digestive gland atrophy significantly influenced one or both of the condition and length factors. Nematodes and the frequently associated cases of focal hemocytic infiltration were not obviously more common in the southern stations where condition index was low. Cestodes tended to be more common at sites where condition index was low, but not consistently so. Infection intensity was high at station 6, for example, where the highest condition index was also recorded. One cannot fully exclude disease as an underlying cause of the malnourished state, however, although no disease-causing organisms were observed in this study. Many disease-causing organisms are readily identified, but cases that are otherwise, such as the withering syndrome of abalones in which the etiological agent was not easily confirmed (VanBlaricom et al. 1993, Friedman et al. 1993. Moore et al. 2001, Moore et al. 2002), are well-known. Nevertheless, parasites and disease do not seem to be likely mediators of the syndrome that appears to evince a malnourished state observed in surf clams along the mortality line.
Sex and gametogenic stage also offered little explanatory information. Sex was unrelated to any condition save possibly the presence of nematodes. Gonadal abnormalities were more common in clams with gonads that showed evidence of the initiation of spawning, suggesting that abnormal development may become more likely or more recognizable as the gametogenic cycle progresses. Digestive gland atrophy and condition index were not so associated. Many bivalves, even when malnourished, attempt to complete gametogenesis (e.g., Riley 1976, Bielefeld 1991, Delgado & Perez Camacho 2003), though not necessarily successfully, and surf clams seem to be no exception, based on the limited information presented here.
Ready alternatives as causative factors producing a malnourished slate do exist, however. A rise in temperature can restrict scope for growth, particularly in the temperature range above optimal where respiratory rate continues to increase, but filtration rate begins to decline (Ali 1970, Newell et al. 1977, Winter 1978, Newell & Branch 1980, Brock & Kofoed 1987). Variations in climate and oceanographic conditions might also directly influence food supply (e.g., Lehman 2000). The combination of rising temperature and reduced rood for such large animals as surf clams requiring substantial food resources to maintain their bulk could be lethal (Taylor 1960, Powell et al. 1995). Unfortunately, sufficient information is not available to investigate further the origin of the malnutrition observed. The evidence does suggest, however, that the regional mortality event observed by NEFSC (2003) in 2002 may be continuing, that animals in nutritionally limiting situations continue to exist over a wide area off the Delmarva Peninsula, and that many of these animals are in sufficiently poor condition that recovery is not necessarily assured, should the environmental conditions leading to malnourishment relax.
The evidence suggests, therefore, that factors compromising scope for growth, either a direct reduction in food, factors reducing the ability to acquire food, or factors increasing the energy requirements of maintenance, offer potential as the underlying cause of malnutrition. Range shifts are often determined by extreme events, particularly along the trailing edge (e.g., Taylor 1934, Kennedy 1990). Range expansion occurs by recruitment. Range contractions in short-lived animals can occur by the failure thereof. For long-lived animals, such as surf clams, rapid contractions in range require increased adult mortality along the trailing boundary and such contractions may occur more rapidly than the expansion along the leading edge (Kennedy 1990). Starvation brought on by environmental shifts mismatching food supply and feeding rate with the energy demands of tissue maintenance otters one potential way this might occur. The malnourishment syndrome identified here, low condition index associated with increased frequency of gonadal abnormality and increased levels of digestive gland atrophy, may evidence such a process.
TABLE 1. Average surf clam length, wet meat weight, and condition index, modal gametogenic stage, and the number of females and males analyzed from each station. * Weight Length Condition Station (g) (mm) (g [mm.sup.-1]) 1 112.8 138.1 0.81 2 77.6 133.1 0.58 3 91.7 137.9 0.66 4 133.9 154.9 0.86 5 125.6 143.4 0.87 6 135.0 148.5 0.91 7 103.1 141.7 0.72 8 80.1 134.2 0.60 9 69.0 117.0 0.55 Modal Gametogenic Number Number Station Stage Female Male 1 S3,5 7 6 2 S4,5 10 5 3 S3 10 5 4 D4 4 6 5 5 3 7 6 S4,5 5 5 7 D4 6 9 8 S3,D4 6 9 9 S3,D4 2 0 * Modal gametogenic stage is the most common gametogenic stage at the station. TABLE 2. Semiquantitative scale used for the evaluation of digestive gland atrophy, adapted from Ellis et at. (1998b). Score Description 0 Normal epithelial thickness in most tubules (0% atrophy), lumen nearly occluded, few tubules even slightly atrophied. 1 Average epithelial thickness less than normal, but greater than one-half normal thickness: most tubules showing some atrophy, some tubules still normal. 2 Epithelial thickness averaging about one-half as thick as normal. 3 Epithelial thickness less than one-half of normal: most tubule epithelia significantly atrophied, some epithelia extremely thin (fully atrophied). 4 Epithelium extremely thin (100% atrophied); nearly all tubules affected. TABLE 3. Semiquantitative scale used for the evaluation of abnormal gonadal development. Score Description 0 Normal gonad. 1 Less than half the follicles are affected. 2 About half the follicles are affected. 3 More than half the follicles are affected. 4 All follicles affected. TABLE 4. Stages used to describe the surf clam gametogenic cycle, adapted from Ellis et al. (1998a). Stage Description Resting/spent gonad Stage 0 Inactive or undifferentiated. Developing gonad Stage D1 Gametogenesis has begun; no ripe gametes visible. Stage D2 Ripe gametes present: gonad developed to about one-third of its final size. Stage D3 Gonad increased in mass to about half the fully ripe condition; each follicle contains, in area, about equal proportions of ripe and developing gametes. Stage D4 Gametogenesis still progressing, follicles contain mainly ripe gametes. Ripe gonad Stage 5 Gonad fully ripe, early stages of gametogenesis rare; follicles distended with ripe gametes; ova compacted into polygonal configurations; sperm with visible tails. Spawning gonad Stage S4 Active emission has begun; sperm density reduced; ova rounded off as pressure within follicles is reduced. Stage S3 Gonad about half empty. Stage S2 Gonadal area reduced; follicles about one-third full of ripe gametes. Stage S1 Only residual gametes remain: some may be undergoing cytolysis. TABLE 5. Frequency of observation of each gametogenic stage defined in Table 4. Gametogenic Stage D1 D2 D3 D4 5 S4 S3 S2 S1 Number of observations 1 0 3 25 25 15 29 6 1 Instances of abnormality 1 0 3 12 8 6 19 5 1 TABLE 6. Prevalence and infection intensity of the common parasites, pathologies, and tissue disorders observed. * Nematode Nematode Cestode Cestode Station Prevalence Intensity Prevalence Intensity 1 0.54 4.14 0.85 5.09 2 0.20 2.00 0.47 2.14 3 0.40 2.17 0.67 2.50 4 0.50 3.00 0.50 2.00 5 0.40 3.50 0.50 1.60 6 0.30 2.67 0.80 6.25 7 0.60 2.56 0.87 4.31 8 0.60 2.67 0.80 7.75 9 0.50 2.00 1.00 12.00 Focal Focal Diffuse Diffuse Hemocytic Hemocytic Hemocytic Hemocytic Infiltration Infiltration Infiltration Infiltration Station Prevalence intensity Intensity Intensity 1 0.92 2.75 0.46 1.17 2 0.40 2.00 0.40 1.33 3 0.87 1.46 0.27 1.75 4 0.60 1.17 0.10 1.00 5 0.90 2.00 0.00 0.00 6 0.80 2.25 0.40 1.25 7 0.87 2.46 0.53 1.50 8 0.93 2.29 0.27 1.00 9 0.50 5.00 0.50 1.00 Digestive Abnormal Station Gland Atrophy Gonadal Development 1 2.13 0.62 2 2.40 0.60 3 2.25 1.13 4 1.50 0.30 5 1.60 0.20 6 1.90 0.20 7 1.80 0.93 8 2.14 1.60 9 3.00 0.00 * The tissue disorders denoted as digestive gland atrophy and abnormal gonadal development are shown as the mean of their semiquantitative scale values. Calculation of prevalence and infection intensity for the parasites and pathologies is described in the "Materials and Methods" section.
The authors thank the captain and crew of the F/V Betty C. for help in sample collection and J.H. Miles & Co., Inc., for providing the vessel. We appreciate the help of J. Weinberg in providing station locations and catch statistics from the 2002 NMFS-NEFSC survey. This research was supported by the National Fisheries Institute Clam Committee and the North American Clam Association. We appreciate the support and logistical help from both chairmen, Dave Wallace (NACA) and Daniel Cohen (NFI-CC).
Ali, R. M. 1970. The influence of suspension density and temperature on the filtration rate of Hiatella arctica. Mar. Biol. (Berl.) 6:291-302.
Arnold, W. S., D. C. Marelli, M. Parker, P. Hoffman, M. Frischer & J. Scarpa. 2002. Enhancing hard clam (Mercenaria spp.) population density in the Indian River Lagoon, Florida: a comparison of strategies to maintain the commercial fishery. J. Shellfish Res. 21:659-672.
Axiak, V., J. J. George & M. N. Moore. 1988. Petroleum hydrocarbons in the marine bivalve Venus verrucosa: accumulation and cellular responses. Mar. Biol. (Berl.) 97:225-230.
Barber, B. J. 1996. Gametogenesis of eastern oysters. Crassostrea virginica (Gmelin, 1791) and Pacific oysters. Crassostrea gigas (Thunberg, 1793) in disease endemic lower Chesapeake Bay. J. Shellfish Res. 15:285-290.
Barber, B. J., S. E. Ford & H. H. Haskin. 1988. Effects of the parasite MSX (Haplosporidium nelsoni) on oyster (Crossostrea virginica) energy metabolism. I. Condition index and relative fecundity. J. Shellfish Res. 7:25-31.
Beninger, P. G. & A. Lucas. 1984. Seasonal variations in condition, reproductive activity, and gross biochemical composition of two species of adult clam reared in a common habitat: Tapes decussatus L. (Jeffreys) and Tapes philippinarum (Adams & Reeve). J. Exp. Mar. Biol. Ecol. 79:19-37.
Bielefeld, U. 1991. Histological observation of gonads and digestive gland in starving Dreissena polymorpha (Bivalvia). Malacologia 33:31-42.
Brock, V. & L. H. Kofoed. 1987. Species specific irrigatory efficiency in Cardium (Cerastoderma) edule (L.) and C. lamarcki (Reeve) responding to different environmental temperatures. Biol. Oceanogr, 4:211-226.
Browne, R. A. & W. D. Russell-Hunter. 1978. Reproductive effort in molluscs. Oecologia (Berl.) 37:23-27.
Cable, W. D. & W. S. Landers. 1974. Development of eggs and embryos of the surf clam, Spisula solidissima, in synthetic seawater. Fish. Bull. 72:247-249.
Cake, E. W., Jr. 1977. Larval cestode parasites of edible mollusks of the northeastern Gulf of Mexico. Gulf Res. Rpts. 6:1-8.
Cerame-Vivas, M. J. & I. E. Gray. 1966. The distribution pattern of benthic invertebrates of the continental shelf off North Carolina. Ecology 47: 260-270.
Chase, R. & R. F. McMahon. 1994. Effects of starvation at different temperatures on dry tissue and dry shell weights in the zebra mussel, Dreissena polymorpha (Pallas). Proc. 4th Intern. Zebra Mussel Conf., Madison, Wisconsin. pp. 501-514.
Chintala, M. M. & J. P. Grassle. 1995. Early gametogenesis and spawning in "juvenile" Atlantic surfclam, Spisula solidissima (Dillwyn, 1819). J. Shellfish Res. 14:301-306.
Choi, K.-S., D. H. Lewis, E. N. Powell & S. M. Ray. 1993. Quantitative measurement of reproductive output in the American oyster, Crassostrea virginica (Gmelin), using an enzyme-linked immunosorbent assay (ELISA). Aquacult. Fish. Manage. 24:299-322.
Choi, K.-S., E. N. Powell, D. H. Lewis & S. M. Ray. 1994. Instantaneous reproductive effort in female American oysters, Crassostrea virginica, measured by a new immunoprecipitation assay. Biol. Bull. 186:41-61.
Chung, E.-Y. & B.-S. Kim. 1994. Histological and ultrastructural studies on gonadal development and germ cell development of the purplish Washington clam, Saxidomus purpuratus (Sowerby). Bull. Coastal Res. Kusan Natl. Univ. 6:1-15.
Clotteau, G. & F. Dube. 1993. Optimization of fertilization parameters for rearing surf clams (Spisula solidissima). Aquaculture 114:339-353.
Cook, T., M. Folli, J. Klinck, S. Ford & J. Miller. 1998. The relationship between increasing sea-surface temperature and the northward spread of Perkinsus marinus (Dermo) disease epizootics in oysters. Estuar. Coast. Shelf Sci. 46:587-597.
Delgado, M. & A. Perez Camacho. 2003. A study of gonadal development in Ruditapes decussatus (L.) (Mollusca, Bivalvia), using image analysis techniques: Influence of food ration and energy balance. J. Shellfish Res. 22:435-441.
Deslous-Paoli. J.-M. & M. Heral. 1988. Biochemical composition and energy value of Crassostrea gigas (Thunberg) cultured in the bay of Marennes-Oleron. Aquat. Living Resour. 1:239-249.
DiBacco, C., G. Robert & J. Grant. 1995. Reproductive cycle of the sea scallop Placopecten magellanicus (Gmelin, 1791) on northeastern Georges Bank. J. Shellfish Res. 14:59-69.
Ellis, M. S., R. D. Barber, R. E. Hillman & E. N. Powell. 1998a. Gonadal analysis. In: G.G. Lauenstein and A. Y. Cantillo (eds.), Sampling and analytical methods of the National Status and Trends Program Mussel Watch Project: 1993-1996 update. NOAA Tech. Mem. NOS ORCA 130:216-227.
Ellis, M. S., R. D. Barber, R. E. Hillman, Y. Kim & E. N. Powell. 1998b. Histopathology analysis. In: G. G. Lauenstein and A. Y. Cantillo (eds.), Sampling and analytical methods of the National Status and Trends Program Mussel Watch Project: 1993-1996 update. NOAA Tech. Mem. NOS ORCA 130:198-215.
Engle, J. B. & C. R. Chapman. 1953. Oyster condition affected by attached mussels. Natl. Shellfish. Assoc. Conv. Add. 1951:70-78.
Ford, S. E. & M. R. Tripp. 1996. Diseases and defense mechanisms. In: V.S. Kennedy, R.I.E. Newell & A.F. Eble (eds.), The Eastern Oyster: Crassostrea virginica. College Park, MD: Maryland Sea Grant College Program, pp. 581-659.
Friedman, C. S., W. Roberts, G. Kismohandaka & R. P. Hedrick. 1993. Transmissibility of a coccidian parasite of abalone, Haliotis spp. J. Shellfish Res. 12:201-205.
Garton, D. W. & W. R. Haag. 1993. Seasonal reproductive cycles and settlement patterns of Dreissena polymorpha in western Lake Erie. In: T. F. Nalepa & D. W. Schloesser (eds.), Zebra Mussels Biology, Impacts, and Control. Boca Raton: Lewis Publishers. pp. 111-128.
Goldberg, R. 1989. Biology and culture of the surf clam. Dev. Aquacult. Fish. Sci. 19:263-276.
Gold-Bouchot, G., R. Sima-Alvarez, O. Zapata-Perez & J. Guemez-Ricalde. 1995. Histopathological effects of petroleum hydrocarbons and heavy metals on the American oyster (Crassostrea virginica) from Tabasco, Mexico. Mar. Pollut. Bull. 31:439-445.
Griffiths, R. J. 1977. Reproductive cycles in littoral populations of Choromytilus meridionalis (Kr.) and Aulacomya ater (Molina) with a quantitative assessment of gamete production in the former. J. Exp. Mar. Biol. Ecol. 30:53-71.
Hawkins, A. J. S., P. N. Salkeld, B. L. Bayne, E. Gnaiger & D. M. Lowe. 1985. Feeding and resource allocation in the mussel Mytilus edulis: Evidence for time-averaged optimization. Mar. Ecol. Prog. Ser. 20: 273-287.
Heral, M. & J. M. Deslous-Paoli. 1983. Valeur energetique de la chain de l'hur;aftre Crassostrea gigas estimee par measures microcalorimetriques et par dosages biochimiques. Oceanologica Acta 6:193-199.
Hine, P. M. 2002. Severe apicomplexan infection in the oyster Ostrea chilensis: A possible predisposing factor in bonamiosis. Dis. Aquat. Org. 51:49-60.
Hofmann, E. E., J. M. Klinck, E. N. Powell, S. Boyles & M. Ellis. 1994. Modeling oyster populations II. Adult size and reproductive effort. J. Shellfish Res. 13:165-182.
Hofmann, E. E., E. N. Powell, J. M. Klinck & E. A. Wilson. 1992. Modeling oyster populations. III. Critical feeding periods, growth and reproduction. J. Shellfish Res. 11:399-416.
Holland, D. L. & B. E. Spencer. 1973. Biochemical changes in fed and starved oysters, Ostrea edulis L., during larval development, metamorphosis and early spat growth. J. Mar. Biol. Assoc. U.K. 53:287-298.
Honkoop, P. J. C. & J. J. Beukema. 1997. Loss of body mass in winter in three inter-tidal bivalve species: An experimental and observational study of the interacting effects between water temperature, feeding time and feeding behaviour. J. Exp. Mar. Biol. Ecol. 212:277-297.
Hummel, H., R. H. Bogaards, C. Amiard-Triquet, G. Bachelet, M. Desprez, J. Marchand, H. Rybarczyk, B. Sylvand, Y. de Wit & L. de Wolf. 1995. Uniform variation in genetic traits of a marine bivalve related to starvation, pollution and geographic clines. J. Exp. Mar. Biol. Ecol. 191: 133-150.
Jones, D. S. 1981. Reproductive cycles of the Atlantic surf clam Spisula solidissima, and the ocean quahog Arctica islandica off New Jersey. J. Shellfish Res. 1:23-32.
Kennedy, V. S. 1990. Anticipated effects of climate change on estuarine and coastal fisheries. Fisheries 15:16-24.
Kim, Y., E. N. Powell, T. L. Wade, B. J. Presley & J. Sericano. 1998. Parasites of sentinel bivalves in the NOAA Status and Trends Program: Distribution and relationship to contaminant body burden, Mar. Pollut. Bull. 37:45-55.
Kraeuter, J. N., S. Ford & W. Canzonier. 2003. Increased biomass yield from Delaware Bay oysters (Crassostrea virginica) by alternation of planting season. J. Shellfish Res. 22:39-49.
Lehman, P. W. 2000. The influence of climate on phytoplankton community biomass in San Francisco Bay estuary. Limnol. Oceanogr. 45:580-590.
Leighton, D. & R. A. Boolootian. 1963. Diet and growth in the black abalone, Haliotis cracherodii. Ecology 44:227-238.
Lichtenfels, J. R., F. G. Kern, D. E. Zwerner, J. W. Bier & A. Madden. 1976. Anaskid nematode in shellfish of Atlantic continental shelf of North America. Trans. Am Microsc. Soc. 95:265-266.
Lichtenfels, J. R., J. W. Bier & P. A. Madden. 1978. Larval anisakid (Sulcascaris) nematodes from Atlantic molluscs with marine turtles as definitive hosts, Trans. Am. Microsc. Soc. 97:199-207.
Loesch, J. G. & D. A. Evans. 1994. Quantifying seasonal variation in somatic tissue: Surfclam Spisula solidissima (Dillwyn. 1817)--a case study. Y. Shellfish Res. 13:425-431.
Loesch, J. G. & J. W. Ropes. 1977. Assessment of surf clam stocks in nearshore waters along the Delmarva Peninsula and in the fishery south of Cape Henry. Proc. Natl. Shellfish. Assoc. 67:29-34.
Loosanoff, V. L. & H. C. Davis. 1963. Rearing of bivalve molluscs. Adv. Mar. Biol. 1:1-136.
Marigomez, J. A., V. Saez, M. P. Cajaraville & E. Angulo. 1990. A planimetric study of the mean epithelial thickness (MET) of the molluscan digestive gland over the tidal cycle and under environmental stress conditions. Helgol. Meeresunters. 44:81-94.
Merrill, A. S. & J. W. Ropes. 1969. The general distribution of the surf clam and ocean quahog. Proc. Natl. Shellfish. Assoc. 59:40-45.
Miller, A. C. & S. E. Lawrenz Miller. 1993. Long-term trends in black abalone, Haliotis cracherodii Leach, 1814, populations along the Palos Verdes Peninsula, California. J. Shellfish Res. 12:195-200.
Moore, J. D., C. A. Finley, T. T. Robbins & C. S. Friedman. 2002. Withering syndrome and restoration of southern California abalone populations. CCOFI Rep. 43:112-117.
Moore, J. D., T. T. Robbins, R. P. Hedrick & C. S. Friedman. 2001. Transmission of the rickettsiales-like prokaryote "Candidatus xenohaliotis californiensis" and its role in withering syndrome of California abalone, Haliotis spp. J. Shellfish. Res. 20:867-874.
NEFSC. 2002. Fishermen's report surfclam/ocean quahog. NOAA Northeast Fisheries Science Center. 16 pp.
NEFSC. 2003. 37th northeast regional stock assessment workshop (37th SAW): Stock assessment review committee (SARC) consensus summary of assessments. Northeast Fisheries Science Center Ref. Doc. 03-16:603.
Newell, R. C. & G. M. Branch. 1980. The influence of temperature on the maintenance of metabolic energy balance in marine invertebrates. Adv. Mar. Biol. 17:329-396.
Newell, R. C., L. G. Johnson & L. H. Kofoed. 1977. Adjustment of the components of energy balance in response to temperature change in Ostrea edulis. Oecologia (Berl.) 30:97-110.
O'Beirn, F. X., R. L. Walker, D. H. Hurley & D. A. Moroney. 1997. Culture of surf clams Spisula solidissima sp., in coastal Georgia: Nursery culture. J. Shellfish Res. 16:157-160.
Olivas-Valdez, J. A. & J. Caceres-Martinez. 2002. Infestation of the blue mussel Mytilus galloprovincialis by the copepod Pseudomyicola spinosus and its relation to size, density, and condition index of the host. J. Invertebr. Pathol. 79:65-71.
Otto, S. V., J. C. Harshbarger & S. C. Chang. 1979. Status of selected unicellular eucaryote pathogens, and prevalence and hispathology of inclusions containing obligate procaryote parasites, in commercial bivalve mollusks from Maryland estuaries. Haliotis 8:285-295.
Palmer, R. E. 1979. A histological and histochemical study of digestion in the bivalve Arctica islandica L. Biol. Bull. 156: 115-129.
Park, M. S., C.-K. Kang, D.-L. Choi & B. Y. Lee. 2003. Appearance and pathogenicity of ovarian parasites Marteilioides chungmuensis in the farmed Pacific oysters, Crossostrea gigas, in Korea. J. Shellfish Res. 22:475-479.
Payne, W. L., T. A. Gerding, R. G. Dent, J. W. Bier & G. J. Jackson. 1980. Survey of the U.S. Atlantic coast surf clam, Spisula solidissima, and clam products for anisakine nematodes and hyperparasitic protozoa. J. Parasitol. 66:150-153.
Perez Camacho, A., A. Villalba, R. Beiras & U. Labarta. 1997. Absorption efficiency and condition of cultured mussels (Mytilus edulis galloprovincialis Linnaeus) of Galicia (NW Spain) infected by parasites Marteilia refringens Grizel et al. and Mytilicola intestinalis Steuer. J. Shellfish Res. 16:77-82.
Perkins, F. O. 1979. Cell structure of shellfish pathogens and hyperparasites in the genera Minchinia, Urosporidium, Haplosporidium, and Marteilia--taxonomic implications. Mar. Fish. Rev. 41:25-37.
Perkins, F. O., D. E. Zwerner & R. K. Dias. 1975. The hyperparasite, Urosporidium spisuli sp. n. (Haplosporea), and its effect on the surf clam industry. J. Parasitol. 61:944-949.
Plana, S., G. Sinquin, P. Maes, C. Paillard & M. le Pennec. 1996. Variations in biochemical composition of juvenile Ruditapes philippinarum infected by a Vibrio sp. Dis. Aquat. Org. 24:205-213.
Powell, E.N. 2003. Maryland inshore surf clam, Spisula solidissima, survey August 2003 cruise report. Final report to J.H. Miles & Co., Inc. Port Norris, NJ: Haskin Shellfish Research Laboratory. 19 pp.
Powell, E.N., R.D. Barber, M.C. Kennicutt II & S.E. Ford. 1999. Influence of parasitism in controlling the health, reproduction and PAH body burden of petroleum seep mussels. Deep-Sea Res. (I Oceanogr. Res. Pap.) 46:2053-2078.
Powell, E. N., J. M. Klinck & E. E. Hofmann. 1996. Modeling diseased oyster populations. II. Triggering mechanisms for Perkinsus marinus epizootics. J. Shellfish Res. 15:141-165.
Powell, E. N.. J. M. Klinck, E. E. Hofmann, E. A. Wilson-Ormond & M. S. Ellis. 1995. Modeling oyster populations. V. Declining phytoplankton stocks and the population dynamics of American oyster (Crassostrea virginica) populations. Fish. Res. 24:199-222.
Powell, E. N. & R. J. Stanton, Jr. 1985. Estimating biomass and energy flow of molluscs in paleo-communities. Palaeontology (Lond.) 28:1-34.
Rheault, R. B. & M. A. Rice. 1996. Food-limited growth and condition index in the eastern oyster, Crassostrea virginica (Gmelin, 1791), and the bay scallop, Argopecten irradians irradians (Lamarck, 1819). J. Shellfish Res. 15:271-283.
Riley, R. T. 1976. Changes in the total protein, lipid, carbohydrate, and extracellular body fluid free amino acids of the Pacific oyster, Crassostrea gigas, during starvation. Proc. Natl. Shellfish. Assoc. 65:84-90.
Riley, R. T. 1980. The effect of prolonged starvation on the relative free amino acid composition of the extracellular body fluids and protein bound amino acids in the oyster Crossostrea gigas. Comp. Biochem. Physiol. A Comp. Physiol. 67:279-281.
Ropes, J. W. 1968. Reproductive cycle of the surf clam, Spisula solidissima, in offshore New Jersey, Biol. Bull. 135:349-365.
da Ros, L., M. G. Marin, N. Nesto & S. E. Ford, 1998. Preliminary results of a field study on some stress-related parameters in Tapes philippinarum naturally infected by the protozoan Perkinsus sp. Mar. Environ. Res. 46:249-252.
Smith, E. B., K. M. Scott, E. R. Nix, C. Korte & C. R. Fisher. 2000. Growth and condition of seep mussels (Bathymodiolus childressi) at a Gulf of Mexico brine pool. Ecology 81:2392-2403.
Spruck, C. R., R. L. Walker, M. L. Sweeney & D. H. Hurley. 1995. Gametogenic cycle in the non-native Atlantic surf clam, Spisula solidissima (Dillwyn, 1817), cultured in the coastal waters of Georgia. Gulf Res. Rpts. 9:131-137.
Taylor, C. C. 1960. Temperature, growth, and mortality--the Pacific cockle. J. Cons. Int. Explor. Mer. 26:117-124.
Taylor, W. P. 1934. Significance of extreme or intermittent conditions in distribution of species and management of natural resources with a restatement of Liebig's law of minimum. Ecology 15:374-379.
Theroux, R. B. & R. L. Wigley. 1983. Distribution and abundance of east coast bivalve mollusks based on specimens in the National Marine Fisheries Service Woods Hole Collections. NOAA Tech. Rpt. NMFS-SSRF 768:1-172.
VanBlaricom, G. R., J. L. Ruediger, C. S. Friedman, D. D. Woodard & R. P. Hedrick. 1993. Discovery of withering syndrome among black abalone Haliotis cracherodii Leach, 1814, populations at San Nicolas Island, California. J. Shellfish Res. 12:185-188.
Walker, R. L., D. H. Hurley & D. A. Moroney. 1997. Culture of juvenile Atlantic surfclams, Spisula solidissima solidissima and Spisula solidissima similis, in forced-flow upwellers in a bivalve hatchery in coastal Georgia. J. World Aquacult. Soc. 28:27-33.
Wallace, D. H. & T. Huff. In press. Use of hydraulic clam dredges in benthic habitat off the northeast United States. Symposium of Effects of Fishing on Benthic Habitat, Tampa, FL.
Winter, J. E. 1978. A review of the knowledge of suspension-feeding in lamel-libranchiate bivalves, with special reference to artificial aquaculture systems. Aquaculture 13:1-33.
Weinberg, J. R. 1998. Density dependent growth in the Atlantic surfclam, Spisula solidissima, from Georges Bank to the Delmarva Peninsula, USA. Mar. Biol. (Berl.) 130:621-630.
Weinberg, J. R. 1999, Age-structure, recruitment, and adult mortality in populations of the Atlantic surfclam, Spisula solidissima from 1978-1997. Mar. Biol. (Berl.) 134:113-125.
Weinberg, J. R., T. G. Dahlgren & K. M. Halanych. 2002. Influence of rising sea temperature on commercial bivalve species of the U.S. Atlantic coast. Am Fish. Soc. Syrup. 32:131-140.
Winstead, J. T. 1995. Digestive tubule atrophy in eastern oysters, Crassostrea virginica (Gmelin, 1791), exposed to salinity and starvation stress. J. Shellfish Res. 14:105-111.
Winstead, J. T., R. M. Overstreet & L. A. Courtney. 1998. Novel gonadal parasites in the eastern oyster Crassostrea virginica from two Gulf of Mexico bays. J. Shellfish Res. 17:341-342.
YUNGKUL KIM AND ERIC N. POWELL
Haskin Shellfish Research Laboratory, Rutgers University, Port Norris, New Jersey 08349
|Printer friendly Cite/link Email Feedback|
|Author:||Powell, Eric N.|
|Publication:||Journal of Shellfish Research|
|Date:||Aug 1, 2004|
|Previous Article:||Sand elimination by the Asiatic hard clam Meretrix meretrix (L.): influences of temperature, salinity and season.|
|Next Article:||Reproductive cycle of the stout razor clam, Tagelus plebeius (Lightfoot, 1786), in the Mar Chiquita Coastal Lagoon, Argentina.|