Condition index of the Eastern Oyster, Crassostrea virginica (Gmelin, 1791) in Sapelo Island Georgia--effects of site, position on bed and pea crab parasitism.

ABSTRACT The condition index (CI) is a tool that has been used to estimate the effect that different environmental factors have on oyster meat quality. The CI of oysters in five beds in Sapelo Island and the Doboy Sound (Georgia, United States) were calculated using three different methodologies. Values from each site were used to: (1) compare two sites located in relatively large systems (river/ sound) and three sites in a small creek to test for differences due to system size and related nutrient availability; (2) determine the effect of a parasite, the pea crab (Pinnotheres spp.), on oyster CI; and (3) determine the effect of differential position of oysters on a bed, with respect to CI (oysters were collected from areas of the bed that are permanently submerged and areas with the longest dry periods between tidal cycles). With respect to the three analyses mentioned earlier, it was found that oyster CIs for sites in larger systems (river and sound sites) were significantly higher than those in sites with lower flux and width (creek sites) and that the presence of pea crabs as parasites can reduce CI by ~50%. In addition, no difference in CI was found between oysters collected from different positions in the oyster bed, indicating that the CI was not altered within a site from effects of exposure. This relatively unusual finding is discussed but suggests the robustness of CI as an intersite analysis tool. Not all differences found in the comparisons were significant for all CIs used, but qualitative results among them were consistent. These variations in significance and the adequacy of each method for analysis are briefly discussed.

KEY WORDS: Crassostrea virginica, Sapelo Island, condition index, parasitism, tidal exposure, Pinnotheres, pea crab

INTRODUCTION

The condition index (CI) of the Eastern Oyster, Crassostrea virginica (Gmelin 1791) has commonly been used to evaluate how these organisms are affected by their environment (Van Dolah et al. 1992, Rheault & Rice 1996). The index has been most important in the use of oysters as indicators of environmental pollution (Lauenstein & O'Connor 1988, Lytle & Lytle 1990, Yevich & Zaroogian 1990, Pridmore et al. 1990, Palmer et al. 1993). The use of CI as an environmental monitoring tool is based on the effect that environmental conditions and different pollutants have on the oyster's growth (Lawrence & Scott 1982, Scott & Lawrence 1982, Rosas et al. 1983, Marcus et al. 1989). It compares the dry meat weight of the animal to the interior volume of the shell, and given the physiologic changes suffered by the oyster in terms of carbohydrate and protein fractions, and lipid and mineral contents, it has been related to pollution effects (Austin et al. 1993). The CI is an inexpensive, quick, representative and responsive tool for monitoring pollution (Scott & Lawrence 1982) and has also been used to estimate growth differences among oysters living in environments subject to different salinities and temperature regimes (Austin et al. 1993, Schumacker et al. 1998). Other conditions that could cause differences in oyster CI are the presence of parasites or commensal organisms living in association with oysters and the relative exposure to desiccation of oysters located at different tidal heights (Cheung & Tse 1993). Parasites and commensals are known to reduce the input of vital resources to a host, thereby reducing its growth and reproductive potential (Stauber 1945, Bierbaum & Shumway 1988, Schmidt & Roberts 1996). The amount of time that an oyster remains above water during tidal lows relates to the period of food intake available to the individual; consequently, oysters that remain under water for longer periods of time could potentially have increased growth (Littlewood 1988, Crosby et al. 1991, Bartol et al. 1999).

The evaluation of the CI of oysters in and around the Sapelo Island National Estuary Research Reserve (SINERR) on Sapelo Island (Georgia, United States) was the main focus of this study. SINERR is part of a protected barrier island with plentiful oyster beds in the rivers and creeks that surround it (Walker & Cotton 2001). Oyster beds in 3 locations were studied: Marsh Landing Dock, Meridian Dock, and Dean Creek. The Marsh Landing Dock in the Dulpin River on Sapelo Island and the dock in Meridian are located in large water systems and are subject to constant boat traffic. The Doboy Sound and the Dulpin River receive nutrient inputs from a large system of marshes. Dean Creek in the SINERR is a smaller tidal system that receives nutrient inputs from one marsh on the island and has a comparatively low water flow. Sapelo Island as a whole has no obvious source of contaminants to the surrounding estuaries and although sections of the island were exposed to varying degrees of human activity in the past, it has remained in a natural state for the past 100 y. Therefore, impacts of anthropogenic origin on oysters are not suspected.

Given the variety of conditions that different oyster beds are subject to in the systems described earlier, the CI was used to observe differences in the fatness of oysters in 3 locations on Sapelo Island: Dean Creek, the Doboy Sound, and the Dulpin River. In addition, CI values were compared between oysters hosting pea crabs (Pinnotheres spp.) and "uninhabited" oysters to test the effect of parasitism on oyster meat quality. The pea crab gains shelter and food from its host oyster and reduces oyster food availability (Warner 1977). The presence of this parasite has been suspected of having effects on oyster growth (Kennedy et al. 1996) and meat content (Haven 1959) and has been related to a reduced gametic development in C. virginica (O'Beirn & Walker 1999) and Mytilus edulis (Bierbaum & Shumway 1988), but little else is known about other effects it could have. Finally, differences in CI values from oysters located at different heights of an oyster bed (i.e., subtidal vs. highest intertidal) were also investigated.

MATERIALS AND METHODS

Oyster beds at four different sites on Sapelo Island (31[degrees]N; 81[degrees]W) and one at the Meridian Dock (Meridian, Georgia) were selected for the study in late October 2003. Three of the sites on Sapelo Island were located in Dean Creek (Sites 1-3, Fig. 1), a small tidal creek emptying into the Doboy Sound (mean width -8 m, ~20 m wide at mouth, 3 km long, mean discharge ~1.75 [m.sup.3]/s). One site was located in the Marsh Landing of Sapelo Island (Site 4) and one last site was located in Meridian Dock (Site 5), a mainland dock located in Meridian (GA) (Fig. 1). Both sites 4 (>300 m wide at mouth) and 5 (300 m wide at mouth, 11 km long, mean discharge >2.13 [m.sup.3]/s) (values from Diebel, unpublished data) are subject to boat traffic and are located in large aquatic systems and flush a large network of marshes.

[FIGURE 1 OMITTED]

Oysters were hand-collected at low tide. Most of the oysters collected were of commercial size (height [greater than or equal to] 76 mm). Shell height was considered as the distance from the umbo to the farthest posterior end of the shell. In sites 2 and 3, oysters were collected from different sections of the oyster bed; half were collected from the highest section of the bed, and half were collected from the lowest portion of the bed. In this way, both oysters that remain submerged permanently and those with longest exposure were collected. Shortly after being collected, all oysters were cleaned of fouling and commensal organisms and washed with tap water. After cleaning, oysters were kept in water and then blotted dry before being measured. Measurements made on each individual oyster included total weight (nearest 0.001 g), total length (to the nearest 0.05 mm), and wet shell weight (nearest 0.001 g). After shucking and examination for Pinnotheres spp., shells and tissue were individually dried at 60[degrees]C for at least 48 h. The dry shell and dry tissue were then weighed to the nearest 0.001 g. The following condition indices were calculated: (1) CI 1 = [dry tissue weight (g) / shell cavity volume] x 100, (Abbe & Albright 2003); (2) CI 2 = [dry tissue weight (g) / dry shell cavity volume] x 100 (Abbe & Sanders, 1988); and (3) CI 3 = [dry tissue weight (g) x 100 / dry shell weight (g)] (Rainer & Mann 1992). These indices have been considered by Hickman and Illingworth (1980) and Davenport and Chen (1987) as some of the most precise. For CI 1 and 2 shell cavity volume is equal to the difference between the weight of the whole oyster (g) and the weight of the empty valves (g) (Abbe & Sanders 1988, Crosby & Gale 1990). CI 1 considered the weight of the empty shells immediately after shucking whereas CI 2 used the weight of the shells after a period of drying (see Abbe & Albright 2003). For all analyses, condition indices were used where shell volume was calculated by a gravimetric method. These methods have been shown to be linearly related to those where CI is calculated by a volumetric method (i.e., by water displacement of the shells) (Schumacker et al. 1998).

For analysis, using each of the CIs above, the following comparisons were made: (A) between all sites, (B) between pea crab-occupied and unoccupied oysters, and (C) between oysters in high and low positions on the oyster bed. An analysis of variance (ANOVA) and t-tests were used for comparison A; t-tests were made among groups in comparisons B and C. All statistical analyses were done in Minitab V. 14 (Minitab Inc. 2004).

RESULTS

The number of oysters collected and size descriptors are included in Table 1. Descriptors for the condition indices calculated per site and per CI formula are shown in Table 2. No relationship between oyster size and condition was observed.

Condition Index Differences Among Sites

Site 4 (Marsh Landing) produced the highest oyster CI among all sites, followed by sites 5 (Meridian Dock) and 3. Site 1 (Dean Creek) had the lowest CI among all sites (Fig. 2). ANOVA on CI 1 values indicated no difference among sites (F = 2.27; P = 0.066). ANOVA on CI 2 values showed significant differences among sites (F 3.43; P = 0.011). Specifically, Site 4 showed higher CI than Site 1 (T = -2.85, P = 0.01). The ANOVA using CI 3 showed differences among sites (F = 2.74; P = 0.032). Again, Sites 1 and 4 were responsible for this difference (T= -2.86, P = 0.012). When grouped, Sites 1-3 showed a lower CI than Sites 4-5 (CI 1: T = 2.46, P = 0.015; CI 2: T = -2.61, P = 0.01; CI 3: T = -2.09, P = 0.039).

[FIGURE 2 OMITTED]

Comparison of Oyster Positions in Bed

Thirty-three oysters were collected from permanently submerged areas in Sites 2 (n = 14) and 3 (n = 19). Twenty-six oysters were collected from high sections of these same oyster beds, 10 in Site 2 and 16 in Site 3. No differences were found in CI values (all methods) between oysters located in high positions in an oyster bed (Means CI 1 = 5.78, CI 2 = 5.2, CI3 = 2.62) and those located in areas of the bed that are permanently submerged (Means CI 1 = 6.03, CI 2 = 4.40, CI 3 = 2.37). Nonsignificant results were also obtained when CI of high versus low oysters were compared per individual site.

Parasitism Effects on CI Among Sites

Prevalence of pea crab presence was low (2.4%) with only three parasitized oysters. Two of these three oysters were found in Site 2 and one in Site 1. Comparisons of CI 1 values between inhabited and uninhabited oysters showed decreased CI values in oysters with pea crabs. For CI 1, T = -5.47 P = 0.032. The mean CI 1 for inhabited oysters was 3.57 versus 6.19 for uninhabited oysters. CI 2 and CI 3 values showed no significant differences between these same groups (T = -2.92, P = 0.1; and T = -0.92, P = 0.456), but also presented a higher CI for uninhabited oysters.

DISCUSSION

Condition indices for oysters in larger systems (Doboy Sound and Dulpin River) were significantly higher than those of oysters from sites in a smaller system (Dean Creek). The higher CIs observed in sites 4-5 could result from increased channel size and nutrient availability. Sites 1-3 were located in Dean Creek, a small tidal creek, whereas Sites 4 and 5 were located very near the Doboy Sound, a larger body of water (see Fig. 1) that transports more nutrients from a more extensive system of salt marshes. This increase in nutrients could in turn result in higher CIs observed in these oyster beds.

CI was not influenced by height in the oyster bed irrespective of the CI calculation method used. Time of exposure to dry conditions does not affect oyster fatness in this system, and this result was unexpected. Previous studies suggest that higher tidal exposure would result in a lower CI given a shorter period for feeding in oysters from this section of the oyster bed. Such a relationship has been observed for CI, reproductive potential, and growth in oysters (Baird 1966, Littlewood 1988, Crosby et al. 1991, Bartol et al. 1999) and other bivalves (Yamada 1989, Seed & Suchanek 1992, Cheung & Tse 1993, Walker & Heffernan 1994). However, it has been demonstrated that some bivalves exhibit physiologic compensations for the reduced feeding time that is associated with living high in the intertidal zone (Charles & Newell 1997). In addition, Phillips (2002) reported no difference in growth of juvenile mussels located in high intertidal and subtidal positions and suggested a higher concentration of nutrients in upper levels of water as a probable cause. These results offer possible explanations for the lack of difference in CI between oysters from subtidal and intertidal areas in this study. Another explanation is that the height between the two areas (<2 m) was not sufficiently different to affect fatness of the oysters. This finding suggests that CI in this context could be useful for intersite comparisons and will not be affected by changes within a single oyster bed, due to the position of the individual collected. However, other factors that could affect oyster fatness should be considered in future comparisons.

The effect of parasitism by pea crabs (Pinnotheres spp.) was suggested by a lower C! on inhabited oysters. Female pea crabs establish inside an individual oyster as larvae, mature and complete their life cycle there. These organisms "steal" the oyster's food by picking mucus food strings before the oyster can consume them (Warner 1977), and can cause damage to gills and other organs (Stauber 1945). Although in low prevalence, this study's results suggest that parasitic pea crab presence can reduce an oyster's CI by about 50% (based on the results obtained using CI 1 values). Pea crabs were the only symbiotic organisms examined in oysters but it is known that their CI can also be affected by other parasites or commensals (e.g., Perkinsus marinus, Haplosporidium nelsoni, and the oyster mud worm) (Littlewood et al. 1992, Kennedy et al. 1996, Dittman et al. 2001). The reduction in CI of C. virginica infected by pea crab is consistent with the findings by Andrade and Andrade (1980); however, they studied the congener Crassostrea rhizophorae, in Brazilian mangroves. Bierbaum and Shumway (1988) also found reduced filtration and oxygen consumption rates in mussels parasitized by pea crabs and it is feasible that the same happens in oysters that could contribute to a lowering in their CI. Although the reduction in CI for oysters hosting pea crabs was not significant using CI 2 and CI 3, it is important to mention that qualitatively the trends observed were similar to those of CI 1. An ulterior power analysis (at [alpha] = 0.05) on the values obtained for CI 2 showed that as many as 27 infected oysters would have to be collected for differences among the two groups to be significant. For CI 3, sample size would need to be much higher (~243 infected and uninfected oysters).

Inconsistent results were obtained among CIs for the analysis of the effects of study site and the effects of parasitism. In the first analysis, significant differences were obtained using CI 2 and CI 3, but differences in the same data were not significant using CI 1. For the effects of parasitism, CI 1 was the only index that offered significant results. All CIs were consistent in rejecting any effect on CI of the oyster's position in the bed. Rainer and Mann (1992) called attention to the difficulties in the comparison and intercalibration of condition indices obtained through different calculation methods. CI 1 (Abbe & Albright 2003), 2 (Abbe & Sanders 1988), and 3 (Rainer & Mann 1992), based on shell cavity volume (calculated by a gravimetric method) and shell weight, have utility in reflecting biochemical or nutritive status (Rainer & Mann 1992). All three CIs used here compare a sensitive numerator, dry meat weight, with a relatively stable numerator, shell weight or volume. The correlation coefficient between CI 1 and CI 2 ([r.sup.2] = 0.761) suggests these 2 CIs could be intercalibrated when used in comparative studies. Intercalibration between CI 1 or CI 2 with CI 3, however, is not straightforward ([r.sup.2] = 0.427 for CI 1; [r.sup.2] = 0.508 for CI 2). In the among-sites comparison of CIs, the P value for the ANOVA on CI 1 is almost significant (P = 0.06), whereas that of CI 2 is clearly significant (P = 0.03). The main difference between CI 1 and CI 2 was whether the empty shells were weighed immediately after shucking or after a period of drying (Abbe & Sanders 1988). Abbe and Albright (2003) established that weighing the shells immediately after processing was a more accurate estimator of cavity volume whenever shells lost >3% of their weight after drying because of water loss. Artificial drying of the shells increases shell cavity capacity and decreases CI. These authors suggest that this methodology should be favored when dealing with oysters with rugged shells, such as those used here. This evidence suggests that CI 1 used here should be favored in future comparative studies in Sapelo Island. In any case, as stated in Rainer and Mann (1992), care is advised when using the CI values obtained here in a comparison with other sources.

While the comparison of condition indices of oysters in this region is limited for the reasons discussed above, CI values found here are somewhat similar to those obtained in other studies along the eastern coast of the United States (i.e., Marcus et al. 1989, Rainer & Mann 1992, Van Dolah et al. 1992). Aside from the difficulties in the methodologic comparisons, it should be noted that a temporal difference is also expected between the mentioned references and this study. Oyster condition is also dependent on temperature, salinity, and reproductive stage. However, temperature and salinity were relatively constant among all study sites, oscillating between mean 26[degrees]C to 23[degrees]C and mean 26 [per thousand] to 29 [per thousand] at the time of study, reducing the possibility that they affected the comparisons made here. Reproductive stage of oysters was not assessed for the oysters collected, but it is possible that the impact of its effect in the results could be small, as October is considered the end of the oyster spawning season in Georgia.

Although this analysis of oysters in Sapelo Island has shown no effect on CI from human activities, it provides an analytical tool that may become useful as the eastern coast of the United States, specifically the Georgia coast, sees increased development. The information contained here is valuable for future analyses of oyster populations in SINERR and for the understanding of how oysters in the Georgia coast can be affected by the numerous environmental and biologic factors they are subjected to. Future studies of the distribution of oyster beds along the Georgia coast (such as Drake 1891 and Walker & Cotton 2001) and of the impact of erosive processes and harvesting, might also benefit from an indicator of the health of oyster beds in specific geographical areas, especially in reserves and parks.

TABLE 1.
Oyster collection data and measurement summary.

Site   N       Weight (g)         Shell Height          Dry Tissue
            Mean [+ or -] SE          (mm)              Weight (g)
                                Mean [+ or -] SE     Mean [+ or -] SE

 1     13     35.22 [+ or         103.33 [+ or         0.4466 [+ or
                 -] 3.33             -] 4.48             -] 0.1618
 2     24     31.31 [+ or          86.30 [+ or         0.4230 [+ or
                 -] 2.03             -] 2.19             -] 0.0322
 3     35     30.04 [+ or          91.25 [+ or         0.4956 [+ or
                 -] 1.74             -] 2.44             -] 0.0386
 4     30     22.64 [+ or          76.46 [+ or         0.4140 [+ or
                 -] 1.21             -] 1.80             -] 0.024
 5     21     39.27 [+ or          79.87 [+ or         0.6311 [+ or
                 -] 2.03             -] 1.34          -] 0.04

                         Cavity Volume *
                        Mean [+ or -] SE
Site
                Wet **                 Dry ***

 1      9.163 [+ or -] 0.714     12.36 [+ or -] 1.13
 2      7.458 [+ or -] 0.476     13.47 [+ or -] 2.03
 3      8.607 [+ or -] 0.582     10.23 [+ or -] 0.655
 4      6.104 [+ or -] 0.328     7.583 [+ or -] 0.425
 5      10.21 [+ or -] 0.551    12.391 [+ or -] 0.58

* Cavity volume is calculated as the difference between the weight of
the whole oyster and the weight of the empty valves, ** weight of the
wet empty valves considered for cavity volume calculation, *** weight
of the dry empty valves considered for cavity volume calculation.

TABLE 2.
Summary of Condition Index values for sites and formulas used. For
details on the formula used, refer to the materials and methods
section.

 Site                    CI 1

             [Mean.sub.(S.E.; Max.; Min.)]
Site 1     [5.076.sub.(0.575; 8.605; 2.116)]
Site 2     [6.006.sub.(0.5; 12.344; 2.664)]
Site 3    [5.874.sub.(0.385; 12.344; 2.664)]
Site 4    [6.937.sub.(0.311; 12.502; 3.652)]
Site 5     [6.176.sub.(0.254; 8.577; 4.459)]

 Site                    CI 2

             [Mean.sub.(S.E.; Max.; Min.)]
Site 1     [3.845.sub.(0.457; 6.471; 1.885)]
Site 2     [4.231.sub.(0.428; 9.04; 0.423)]
Site 3     [5.118.sub.(0.35; 13.844; 2.804)]
Site 4     [5.578.sub.(0.242; 9.568; 3.03)]
Site 5     [5.081.sub.(0.245; 7.216; 3.458)]

 Site                    CI 3

             [Mean.sub.(S.E.; Max.; Min.)]
Site 1     [2.057.sub.(0.236; 3.712; 0.989)]
Site 2     [2.426.sub.(0.116; 3.31; 1.088)]
Site 3     [2.528.sub.(0.117; 4.535; 1.526)]
Site 4     [2.795.sub.(0.104; 3.679; 1.389)]
Site 5     [2.502.sub.(0.178; 4.17; 0.592)]

ACKNOWLEDGMENTS

The author thanks the University of Georgia Marine Institute, Jim Kitchell, Jake Vander Zanden, Emily Stanley, and the 2003 Center for Limnology Sapelo Island crew. The author also thanks K. Rogers and J. Jorgensen who provided assistance in oyster processing; I. Kaplan, M. Adams, C. H. Orr, and two anonymous reviewers who provided valuable suggestions for the preparation of the manuscript; J. T. Maxted who assisted in the elaboration of Figure 1; and M. W. Diebel who assisted with providing physical data of study systems. This work was funded by the University of Wisconsin Sea Grant Institute under grants from the National Sea Grant College Program, National Oceanic and Atmospheric Administration, U.S. Department of Commerce, and from the State of Wisconsin. Federal grant number NA16RG2257 project number E/E-45-SE.

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NORMAN MERCADO-SILVA

Center for Limnology, University of Wisconsin, Madison, 680 N. Park St., Madison, Wisconsin 53706