SpAwNINg BIOLOgy OF ThE BLUE CRAB ...

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May 11, 2005 - Gary H. dickinson, daniel Rittschof, and Catherine latanich. ABSTRACT. The blue crab, Callinectes sapidus Rathbun, supports valuable ...
BULLETIN OF MARINE SCIENCE, 79(2): 273–285, 2006

Spawning Biology of the Blue Crab, Callinectes sapidus, in North Carolina Gary H. Dickinson, Daniel Rittschof, and Catherine Latanich ABSTRACT

The blue crab, Callinectes sapidus Rathbun, supports valuable fisheries in many Atlantic and Gulf Coast states. We studied the spawning biology of female crabs hand-captured in the Carrot Island Embayment, central North Carolina. Crabs were retained sub-tidally in submerged, partially buried minnow traps and fed daily. Of 124 experimental animals, 66% had two or more clutches of eggs with three individuals producing seven clutches over 18 wks. The longer the crabs were held, the more clutches they produced. We infer that an average size crab (127 mm carapace width) would produce eight clutches over a 25-wk spawning period. Since larger crabs had larger clutches but produced them less frequently than smaller crabs, reproductive output over 18 wks of the spawning season was statistically similar for most size groups. Lipofuscin index values were higher for crabs that had recently molted to maturity than for crabs that had been spawning for 18 wks. Sponge damage of 2307 crabs, determined by the degree of deviation from the rounded form of an intact sponge, indicated that animals caught by crab-pots had significantly more sponge damage than hand-captured crabs. Sponge damage was most extensive during mid-summer and the extent of damage differed among the smallest and largest size groups during this time. Our finding that reproductive output is similar for most size groups brings into question management plans that suggest the release of the largest mature females.

The blue crab, Callinectes sapidus Rathbun, is common on the western Atlantic, Gulf and Caribbean coasts from Massachusetts to Brazil (Van Engel, 1958). Blue crab is the most valuable fishery for several Atlantic coast states including Maryland and North Carolina (NMFS, 2003). Recent decreases in total catch (Chesapeake Bay Program, 1997; Chesapeake Bay Commission, 2003), and abundance of spawning crabs and larvae (Lipcius and Stockhausen, 2002) within the Chesapeake Bay has lead to concerns over sustainability of the fishery. Among common strategies for management of the fishery are measures to protect the spawning stock of mature females, which have been employed in the Chesapeake Bay (Chesapeake Bay Program, 1997) and recently in North Carolina (NCDMF, 2004). To effectively manage the spawning stock using predictive models, an understanding of blue crab spawning biology is necessary. Mating occurs with the female terminal molt and females may store sperm sufficient for over a dozen clutches of eggs (Hines et al., 2003). Quantity and viability of stored sperm are independent of female body size (Wolcott et al., 2005). Females generate mature ovaries in warm months in about six weeks. In central North Carolina, spawning occurs from April to November and to the greatest extent during summer months of June, July, and August (Dudley and Judy, 1971). Females with clutches of eggs remain in, or move to, high salinity waters (Van Engel, 1958; Mangum and Towle, 1977; Tankersley et al., 1998; Turner et al., 2003) using ebb-tide transport (Tankersley et al., 1998; Hench et al., 2004; Carr et al., 2004). In the Beaufort Inlet region of central North Carolina, crabs move offshore through the inlet (Dudley and Judy, 1971; Carr et al., 2004). Work by Hench et al. (2004) and Forward et al. (2005) suggest that blue crabs continue to Bulletin of Marine Science

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move seaward using ebb-tide transport following larval release, contrary to previous models suggesting a shift towards the estuary using flood-tide transport after larval release. Due to the mobile nature of mature female blue crabs, gaps exist in our basic knowledge of blue crab spawning biology. The relationship between crab size and clutch size has been well established for brachyuran crabs (Hines, 1982; Prager, 1990), but other aspects of blue crab spawning biology, including an accurate estimate of how many clutches a spawning female will produce in a given season, are not well understood. Although local fishermen believe that blue crabs have only one clutch of eggs, there is evidence that blue crabs produce multiple clutches of eggs (Van Engel, 1958; Tagatz, 1968; Millikin and Williams, 1984; Prager et al., 1990; Hines et al., 2003). The potential influence of the fishery on reproductive output of captured and released ovigerous crabs is also not well understood. Ovigerous crabs captured in crab-pots are often observed damaging their own sponge by picking at it with their chelipeds (Rittschof, pers. obs.). This response is likely due to stressful environmental conditions, lack of food, and confinement with other crabs. Depending on the number of clutches produced and the extent of sponge damage, a considerable portion of a crab’s lifetime reproductive output may be lost due to trap stress even if the crab is released. Our primary objective for this study was to quantify several spawning parameters for mature female blue crabs using crabs that were hand-captured in the vicinity of the Carrot Island Embayment and retained in the field in submerged minnow traps. Specifically, we addressed: (1) the total number of clutches produced during 18 wks of the spawning season; (2) the relationship between crab size and clutch volume; (3) differences in clutch production interval (number of weeks per clutch) among size classes; (4) differences in the reproductive output among size classes and; (5) since age is an important determinant of fecundity, we evaluated whether spawning parameters (number of clutches, clutch volume, clutch production interval, and reproductive output) vary with lipofuscin index, which is a proxy of age in blue crabs (Ju et al., 1999; 2001; 2002). Secondly, we analyzed the extent to which trap stress due to potting may alter reproductive output using survey data on sponge damage (the degree of deviation from the smooth rounded form of an intact sponge). Materials and Methods Two separate but related experiments were conducted in the vicinity of the Beaufort Inlet, central North Carolina. These consisted of (1) field spawning trials with animals retained in submerged, half-buried minnow traps (June–October 2004), and (2) a survey of sponge damage of crabs in three locations (June 2000–November 2002). Data from both the field spawning trials and the sponge damage survey were analyzed using SigmaStat version 2.03. Crab Collection For Field Spawning Trials.­—Our experimental design for the field spawning trials entailed collecting 25 crabs in each of four months of May, June, July, and August 2004 for a total of 100 crabs. This experimental design was chosen based on the number of crabs we predicted we would be able to hand collect over a 2–3 d interval each month, and to allow us to discern a seasonal trend in clutch production among crabs collected in different months. We deviated from this design slightly due to an inability to collect 25 crabs in May, and in order to replace crabs that died. During June, July, August, and September, at least 25 ovigerous crabs were collected by hand around the Carrot Island Embayment in the Rachael Carson Estuarine Research Reserve, Beaufort, NC (latitude, 34°42′50″ N, longitude, 76°40′31″

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W). The July sample of 32 crabs included 18 crabs migrating at the surface at night from the Morehead City turning basin (lat. 34°42′55″ N, long. 76°41′39″ W), approximately 1 km from the Rachael Carson Estuarine Research Reserve. Upon collection, each crab was labeled using a plastic poker chip with a unique identification number attached across the back of the crab by looping and twisting coated 18-gauge copper wire around the large lateral spines. Carapace width (CW) was measured as the distance between the tips of the large lateral spines. Crabs were examined for external eggs (a sponge), and sponge dimensions (width-left/right, length-anterior/posterior, depth-dorsal/ ventral) were taken. Sponge color was noted and embryos from late-stage (brown or black) sponges were sampled and examined using a dissecting microscope to determine viability. Eggs with viable embryos are spherical, the exterior is dark yellow, and a dark brown/black developing embryo can be seen in the interior. Non-viable eggs appear as a shriveled dark yellow mass or are spherical but contain no dark embryo in the interior (hollow). Eggs were taken from each of four quadrants of the sponge (upper left, upper right, lower left, lower right), and stored in alcohol at room temperature. The first fifteen eggs encountered in each quadrant sample were scored for viability. Experimental Procedure For Field Spawning Trials.—Crabs were confined in half buried minnow traps below the low tide line (Ziegler, 2002) on the western side of Pivers Island, Beaufort, NC. Minnow traps, 42 cm long and 23 cm in diameter, were buried vertically in the sediment to a depth of approximately 20 cm to allow crabs to bury. Each trap consisted of identical cylindrical halves hinged on one side and tapered to an inverted funnel measuring 2.5 cm at either end and flattened on the bottom half of the trap that was buried. Traps were buried in sediment that was shallow enough to be accessible but deep enough to remain submerged at low tide (10–30 cm). A single female was confined to each trap and traps were wired shut with 18-gauge coated copper wire. Each trap was assigned a number (1–100) and tagged for reference. Tags and cages were periodically cleaned with a wire brush to remove fouling. Crabs were fed daily with fresh and frozen baitfish (pinfish, croaker, spot, mullet, and menhaden). In addition to the scheduled feedings, crabs caught and ate fish that entered the traps. The experiment ran from June through mid-October of 2004. Water temperature over the course of the experiment ranged from 29.6 °C in early August to 21.0 °C in mid-October. Each crab was sampled weekly for the presence of an egg sponge. Previous laboratory observations have shown that egg development (from extrusion to release) takes at least seven days (Hines et al., 2003; Rittschof, pers. obs.). Therefore, a weekly sampling interval ensured that all extruded sponges were observed, although this interval was not frequent enough to discern differences in the rate of development. Minnow traps were sampled for a total of 18 wks of the spawning season. Examinations in the field took place at low tide. Crabs were handled with a dip net and padded tongs. A cylindrical (61 cm height × 66 cm diameter) 1.0 cm galvanized hardware cloth screen was placed around each trap to prevent crabs from escaping as they were removed from the traps. Sponge dimensions and embryo viability samples were taken as described above. The extent of external fouling on crabs was noted. Crabs that died during the course of the experiment were replaced, so as to maintain one crab in each trap for the duration of the experiment. Lipofuscin Analysis of Animals Used in Field Spwaning Trails.—To determine if any of the spawning parameters studied (number of clutches, clutch volume, clutch production interval and reproductive output) vary with crab age, at the conclusion of the field spawning trials (mid-October, 2004), 23 crabs that had been used in field spawning trials were sacrificed for lipofuscin analysis, which is a proxy for age in blue crabs (Ju et al. 1999; 2001; 2002). For comparison, ten female and ten male crabs that had recently molted to maturity (determined by examination of the abdomen) were collected by crab-pot in the North River (lat. 34º45′36″ N, long. 76º36′09″ W) and subjected to lipofuscin analysis. Crabs were anesthetized on ice and carapace width and type/extent of fouling was recorded. The carapace was removed and the presence of mature ovaries and gill parasites was noted.

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Lipofuscin analysis was based on Ju et al. (1999) with minor modifications. Using forceps and a sharp razor blade, external eyestalks were prepared for lipofuscin extraction by removing the internal eyestalk and all retinal tissue. External eyestalks were cut lengthwise. The inner neural tissue was retained and placed in a 50 ml conical polypropylene tube. The chitonous outer coating was discarded. Total lipofuscin was extracted using HPLC grade dichloromethane (2.66 ml) and methanol (1.33 ml). Samples were sonicated using a microprobe sonicator at 20 watts for 2 min and then centrifuged at 800× g for 10 min. The supernatant was transferred to a clean glass test tube, dried under nitrogen to remove solvents, and the resulting pellet re-dissolved in 4 ml methanol. Lipofuscin was quantified using a quinine sulfate standard (dissolved in 0.1 N H2SO4) and analyzed on a Shimadzu RF-5301PC spectroflourophotometer with a 3 ml cuvette. Total protein analysis was conducted on the remaining 1 ml of sample. Samples were dried in a speed vac to remove methanol, and the pellet was re-dissolved in 470 µl nanopure water. Total protein was analyzed using a Pierce Mirco BCA kit with BSA standard, and quantified on a Molecular Devices SpectraMAX 190 spectrophotometer. Lipofuscin index (LI) was calculated as the extractable lipofuscin concentration calibrated vs quinine sulfate (µg ml–1) divided by the total protein concentration (mg ml–1). Sponge Damage Survey.—Between June 2000 and November 2002, 2307 ovigerous crabs were caught, marked, and released in three locations in central North Carolina: the Carrot Island Embayment (lat. 34°42′50″ N, long. 76°40′31″ W), the North River (lat. 34°45′36″ N, long. 76°36′09″ W), and the Newport River (lat. 34°45′36″ N, long. 76°42′09″ W). The survey consisted of 341 crabs in the Carrot Island Embayment, 976 crabs in the North River, and 990 crabs in the Newport River. Carrot Island Embayment crabs were caught by hand. North River and Newport River crabs were caught in crab-pots in the crab fishery. Carrot Island Embayment crabs were collected June through November of each year. North River crabs were collected in early summer (June and July) of each year, and Newport River crabs were collected in mid-summer (July and August) of each year. All crabs were marked using a plastic poker chip as described for the field spawning trails. CW was measured and each sponge was examined visually and assigned a score for sponge damage where: 100%–71% of sponge remaining was given a score of five; 70%–50% remaining, a four; 49%–41% remaining, a three; 40%–25% remaining, a two; and < 25% remaining, a one. Blue crab sponges follow a characteristic smooth rounded form. The degree of deviation from this form was used to determine extent of sponge damage.

Results Spawning.—Blue crabs were found to have multiple clutches of eggs within a single spawning season. Individuals that began spawning in June had as many as seven clutches by October. Animals held in captivity for a longer period of time produced more clutches than crabs held for short periods (One-way ANOVA: P < 0.001; Fig. 1). Of 124 experimental animals, 81 (66%) had at least two clutches, 50 (40%) at least three, 33 (27%) at least four, 9 (7%) at least five, and 7 (6%) individuals had six or more clutches. Of the 43 individuals producing only one clutch while in captivity, over half (56%) spent two weeks or less in captivity. Using the relationship between total number of clutches produced and total time in captivity (Fig. 1) and assuming a 25-wk spawning period, we infer that average size crabs (127 mm CW) that are mature at the beginning of the spawning period produce eight clutches of eggs during a spawning season (6.5–9.3 clutches, 95% C.I.). The assumption of a 25-wk spawning period (May 15–November 1) is based on: (1) observations of ovigerous crabs in the Carrot Island Embayment by mid-May; (2) the existence of crabs with sponges in mid-October; and (3) observation of mature ovaries in the majority of crabs (91%) sacrificed for lipofuscin analysis in mid-October,

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Figure 1. Total time in captivity vs number of clutches produced by blue crabs retained in the field in submerged minnow traps. Mean value for all individuals held a given number of weeks is shown with standard error bars. Points with no error bars represent data for a single crab. Line of best fit (solid) and 95% confidence interval (dashed) is shown. The x-axis is extended to 25 wks to allow estimation of clutch production over a full spawning season. Regression is significant (P < 0.001).

indicating their potential to continue clutch production into November. We were not able to discern a seasonal trend in clutch production. Egg viability analyses were conducted on 98 late-stage sponges from 87 individuals. Viability was between 93%–100% for all sponges sampled. In late August, three sponges were produced without embryo development (sponge did not change color or was lost over a seven day interval). This occurred on the second clutch in captivity for one animal and on the fourth clutch for two animals. Fouling and parasitism will affect a crab’s ability to move and forage freely. Of animals used in spawning trials and sacrificed at the conclusion of the experiment, 80% were fouled (any hard or soft fouling) and 96% of animals (22 of 23) had gill parasites (parasitic gooseneck barnacle, Octolasmis muelleri Coker). Clutch Volume.—Crabs producing three or more clutches showed a gradual decrease in clutch volume over successive clutches (Fig. 2). Between the first and the seventh clutch, volume decreased by 56%. Of individuals having only two clutches (n = 43), 77% had a decrease in clutch volume (average decrease from first to second clutch, 25%), while 23% had an increase in clutch volume (average increase from first to second clutch, 18%). Since we were only able to sample each sponge once, these calculations do not discriminate between stages of sponge development. Larger crabs had larger clutches of eggs (Fig. 3). Regression of clutch volume on carapace width was significant for clutches 1, 2, 3, and 4 (One-way ANOVA: P < 0.001). As clutch number increased, the change in clutch volume per change in CW decreased (Fig. 3). The difference in volume of clutches between large and small crabs decreased by 9% from clutch one to clutch four, with large crabs producing relatively smaller clutches on the fourth clutch than they did earlier. Crab size vs Clutch Production Interval.—Total time an individual crab spent in captivity divided by the total number of clutches that individual produced while in captivity was taken as the clutch production interval. Clutch production interval was longer for larger crabs than for smaller crabs (Fig. 4). Crabs were grouped into seven size classes, each with a 15 mm range in CW: 72–86 mm (n = 6), 87–101 mm (n = 8),

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Figure 2. Mean clutch volume (± SE) over successive clutches for blue crabs producing more than two clutches in captivity. All clutch stages and all crab sizes are included. Crabs were retained in the field in submerged minnow traps.

102–116 mm (n = 21), 117–131 mm (n = 36), 132–146 mm (n = 26), 147–161 mm (n = 13) and 162–176 mm (n = 10). The largest size group corresponds to crabs exceeding the maximum size limit (171 mm CW, with 5% tolerance) proposed by the North Carolina Blue Crab Fisheries Management Plan (NCDMF, 2004). Clutch interval differed significantly among size groups (Kruskal-Wallis one-way ANOVA on ranks: P < 0.001). Clutch interval was significantly longer in the largest group (162–176 mm CW) than in the two smallest groups (72–86 mm and 87–101 mm CW) and significantly longer in the 132–146 mm CW group than in the smallest group (72–86 mm CW; Dunn’s Method post-hoc test on ranks: P < 0.05). Reproductive Output.—Reproductive output (calculated as an individual’s clutch frequency (inverse of clutch interval) multiplied by that individual’s average clutch volume) over 18 wks of the spawning season differed significantly among groups (Kruskal-Wallis one-way ANOVA on ranks: P < 0.001; Fig. 5). The 147–161 mm CW group differed significantly from the three smallest groups (72–86 mm, 87–101 mm and 102–116 CW mm), whereas all other group comparisons indicated a statistically similar reproductive output (Dunn’s Method post-hoc test on ranks: P < 0.05). Lipofuscin Analysis.—None of the spawning parameters considered (numbers of clutches, clutch volume, clutch production interval, and reproductive output) varied significantly with lipofuscin index. Lipofuscin index values did not differ significantly between the left and the right eyestalk, and did not vary with CW. Lipofuscin index differed significantly among groups (Kruskal-Wallis one-way ANOVA on ranks: P < 0.001; Fig. 6), being significantly higher for recently molted females and males than for spawning females (Dunn’s method post-hoc test on ranks: P < 0.05). Sponge Damage Survey.—Of 2307 ovigerous crabs examined, extent of sponge damage was significantly greater for crabs caught by crab-pots than for crabs caught by hand (t-test: P < 0.001; Fig. 7). The majority of crabs caught by crab-pot (52% in the Newport River, 51% in the North River) had 50%–70% of the sponge remaining, whereas 97% of hand-captured crabs had 100% of the sponge remaining. Crabs were grouped by size class as described for the field spawning trials, however, a 177–191 mm CW group was added to accommodate larger animals and the 72–86 mm CW group was eliminated since no animals in the sponge damage survey were < 90 mm

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Figure 3. Carapace width vs clutch volume for the first four clutches produced after capture by individual blue crabs retained in the field in submerged minnow traps. Best-fit lines for each of the four clutches are shown on one plot for comparison. Regressions for all four clutches are significant (P < 0.001).

CW. Sponge damage differed significantly among size groups for crabs caught in the Newport River (crab-pot, mid-summer) (Kruskal-Wallis one-way ANOVA on ranks: P < 0.001). The smallest group, 87–101 mm CW, was excluded from post-hoc analysis due to very low sample size (2 crabs). The 102–116 mm CW group differed significantly from the 132–146 mm, 147–161 mm and the 162–176 mm CW groups (Dunn’s Method post-hoc test on ranks: P < 0.05). Sponge damage was statistically similar for all size groups within a site for animals caught in the North River (early summer) in the Carrot Island Embayment (June–November). Discussion Blue crabs produce multiple clutches of eggs within a single spawning season. From our data, we deduce that on the central North Carolina coast an average sized crab (127 mm CW) that is mature at the beginning of the spawning season produces eight clutches within a 25-wk spawning season. Larger crabs produce larger clutches but produce them less frequently than do smaller crabs. Therefore, reproductive output (incorporating clutch volume and clutch frequency) is statistically equivalent for most crabs. Crabs caught in crab-pots show significantly more sponge damage than

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Figure 4. Mean clutch production interval (± SE) in weeks per clutch for blue crabs with carapace width between 72–86 mm (n = 6), 87–101 mm (n = 8), 102–116 mm (n = 21), 117–131 mm (n = 36), 132–146 mm (n = 26), 147–161 (n = 13), and 162–176 (n = 10). Clutch production interval is the total number of weeks an individual spent in captivity divided by the total number of clutches produced by that individual while in captivity. Crabs were retained in the field in submerged minnow traps. Groups marked with different letters are significantly different as shown by Dunn’s Method post-hoc analysis on ranks. The largest group, 162–176 mm carapace width, is crabs exceeding the seasonal maximum size limit proposed for spawning stock protection in the North Carolina Blue Crab Fisheries Management Plan (2004).

do hand-captured animals. The extent of sponge damage differs among size classes in animals caught by crab-pots during mid-summer, with most larger animals having more damage than the smallest animals. Our primary objective was to determine if blue crabs collected within the Carrot Island Embayment, central North Carolina, have multiple clutches within a single spawning season. Most local fishermen believe that blue crabs produce one clutch of eggs and then die whereas trawl surveys in the Chesapeake Bay (Van Engel, 1958; Millikin and Williams, 1984; Prager et al., 1990) and Florida (Tagatz, 1968) suggest that crabs may have two and at maximum three clutches in some years. Recently, Hines et al. (2003), using crabs taken from the Sebastian Inlet, Florida, and kept in large tanks, demonstrated that crabs may have up to seven clutches within a single spawning season, and inferred that Florida crabs may have up to 18 clutches within a lifetime. Carrot Island Embayment crabs kept for 18 wks in the field under optimal conditions (fed daily, free from predators) also had up to seven clutches. Based on the tight relationship of increasing clutch production with time in captivity, we infer that over a full 25-wk spawning period, average sized crabs (127 mm CW) have eight clutches if they are mature at the beginning of the spawning season. From the 95% confidence interval of the regression, this estimate has a range of 6.5–9.3 clutches, corresponding to large and small crabs, respectively. Since most of our crabs were infected with gill parasites, we are hesitant to infer a lifetime clutch production for Beaufort crabs similar to that suggested by Hines et al. (2003) for Florida crabs. Gill parasites prevent crabs from burying, which may lead to incapacitation by growth of fouling organisms (Rittschof, pers. obs.). All but one crab dissected at the conclusion of the experiment had gill parasites (parasitic gooseneck barnacle, O. muelleri). Thus, crabs were unlikely to live through another spawning season.

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Figure 5. Mean reproductive output (± SE) over 18 wks of the spawning season for blue crabs with carapace width (CW) between 72–86 mm (n = 6), 87–101 mm (n = 8), 102–116 mm (n = 21), 117–131 mm (n = 36), 132–146 mm (n = 26), 147–161 (n = 13), and 162–176 (n = 10). Reproductive output is the average clutch volume (cm 3) multiplied by clutch frequency (total number of clutches divided by total time in captivity) produced by individual crabs after capture. Groups marked with different letters are significantly different as shown by Dunn’s Method post-hoc analysis on ranks. The largest group, 162–176 mm CW, is crabs exceeding the seasonal maximum size limit proposed for spawning stock protection in the North Carolina Blue Crab Fisheries Management Plan (2004).

Multiple clutch production should be considered within the context of blue crab life history. Following mating, female blue crabs migrate to, or remain in, high salinity waters to facilitate offshore larval development of salinity sensitive larvae (Millikin and Williams, 1984). Benefits proposed for larval development offshore include reduced predation (Morgan, 1990) and increased survivorship in high salinity waters due to physiological limitations (Costlow and Bookhout, 1959; Mangum and Towle, 1977). Movement to higher salinity water is achieved through ebb-tide transport (Tankersley et al., 1998; Carr et al., 2004; Hench et al., 2004). Production of multiple

Figure 6. Mean lipofuscin index (± SE) for recently molted blue crab males and females, and spawning females. Lipofuscin index is the concentration of extractable lipofuscin in µg ml–1 (calibrated against quinine sulfate) divided by total protein concentration in mg ml–1. Groups marked with different letters are significantly different as shown by Dunn’s Method post-hoc analysis on ranks.

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Figure 7. Mean sponge damage (± SE) for blue crabs in the Carrot Island Embayment, North River, and Newport River. Crabs from Carrot Island embayment were collected by hand. Crabs from the North River and Newport River were caught in pots. Sample sizes are displayed for each size group. Newport River groups marked with different letters are significantly different as shown by Dunn’s Method post-hoc analysis on ranks. The 87–101 mm carapace width group was not included in post-hoc analysis due to very small sample size. North River and Embayment showed no significant difference between groups within a site.

clutches is consistent with recent work by Hench et al. (2004) and Forward et al. (2005) suggesting that females continue to move seaward using ebb-tide transport after the release of a clutch. Continued movement offshore ensures that successive clutches are released in conditions favorable to larval survival. Reproductive output over the 18 wks of our study was similar for most size groups, a finding consistent with recent work by Wolcott et al. (2005) showing that the quantity and viability of stored sperm is independent of female CW. Reproductive potential, therefore, should be independent of size. Larger crabs produce larger clutches of eggs (Hines, 1982; Prager et al., 1990), and based on interspecific comparisons of brachyuran crabs, Hines (1982) suggests that body size is the principal determinant of reproductive output. In the Hines (1982) study, however, the number of broods produced was not related to body size, a pattern that emerged from our data. Further, Hines (1982) notes a trade-off between the number of eggs per brood and the number of broods per year. Although physiological constraints will limit the size of each clutch, given the same complement of sperm, smaller crabs will generate the same reproductive output as larger crabs by producing clutches at a quicker rate. Therefore, two independent lines of evidence support the notion that all spawning females have similar reproductive potential: (1) all sizes of blue crabs store comparable amounts of viable sperm (Wolcott et al., 2005), and (2) most size groups were shown to have similar reproductive output over 18 wks of the spawning season (this study). Various authors have suggested that lifetime reproductive potential of blue crabs is sperm-limited (Kendall and Wolcott, 1999; Kendall et al., 2001; Hines et al., 2003). Direct evidence for sperm limitation was shown in Florida crabs (kept in tanks) where 25% of fifth clutches and 50% of sixth clutches were infertile (Hines et al., 2003). Although in our study all sponges at a mature stage of embryo development were at or near 100% viable, three sponges were observed at the end of the season that did not develop, suggesting sperm limitation in some Beaufort crabs. Because

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all females store comparable amounts of sperm (Wolcott et al., 2005), and this level of sperm storage is sufficient to produce more than 6–9 clutches, we suggest that sperm limited crabs are those who have already reached their lifetime reproductive potential and are in their second year of spawning. Given that blue crabs produce multiple clutches of eggs over the course of their lifetime, and that age is important in estimating fecundity, it would be useful to determine how spawning parameters change as spawning crabs age. However, the relationship between lipofuscin index (a proxy for age in blue crabs; Ju et al., 1999; 2001; 2002), and the spawning parameters we examined (numbers of clutches, clutch volume, clutch production interval and reproductive output) varied widely and no clear trends emerged. Lipofuscin values for recently molted (pre-spawning) female and male crabs were significantly higher than that of spawning females, indicating that lipofuscin may not be useful in determining age in spawning female blue crabs at the resolution of interest (within 6 mo). Using lipofuscin to age spiny lobsters, Maxwell et al. (2006) also showed a large degree of variation in lipofuscin derived age estimates for spawning females. We also considered the potential influence of the fishery on reproductive output of crab-pot captured and released ovigerous crabs. The extent of sponge damage was more severe in crabs captured by crab-pots than crabs captured by hand. On average, crabs captured by crab-pots were found with 50%–70% of their sponge remaining, whereas hand-captured crabs were rarely found with damaged sponges. Although the relationship between the extent of sponge damage and crab size was not dramatic, crabs collected during mid-summer showed a size-specific difference in the extent of sponge damage, with the smallest crabs showing the lowest levels of sponge damage. The degree to which sponge damage reduces reproductive output is directly dependent on the number of clutches produced. As larger crabs produce fewer, but larger clutches than do smaller crabs, the potential decrease in reproductive output due to sponge damage is most significant in larger crabs. For small crabs estimated to produce nine clutches within a year, the decrease in reproductive output would be minimal if the crabs were released to continue clutch production. Results of this study showing that reproductive output is similar for most size groups and that the loss of reproductive output due to sponge damage during potting is more severe in larger crabs, brings into question spawning stock protection strategies that call for the release of the largest mature females (> 171 mm CW). This management strategy is based on the relation of sponge size increasing with CW but does not take into account differences among sizes in the overall number of clutches produced. A more sensible management strategy that would protect the spawning stock but impose minimal loss in profit to fisherman may be to release medium sized mature females but retain animals in the largest size group, as these animals are the most profitable. Further studies assessing reproductive output of blue crabs in other locations, assessing reproductive potential later into the year and over multiple spawning seasons, and further investigations into the effect of trap stress on reproductive output should be undertaken to fully describe the reproductive biology of blue crabs. Based on our results we suggest a reworking of blue crab population models utilizing a fecundity parameter based on multiple clutches rather than a single clutch. In models such as Miller (2001), small changes in fecundity result in substantial changes in the intrinsic rate of population increase. Therefore, a realistic estimate of fecundity is essential to an accurate population model.

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Acknowledgements We would like to thank J. Miles for assistance with data processing and lipofuscin procedure, M. Vandersea for use of the spectroflourometer, and T. Ziegler, C. Tepper and L. Nichols for helpful comments on drafts. We thank two anonymous reviewers who provided valuable comments and suggestions on the manuscript. Funding was provided by NC Sea Grant (NCSU Subaward 2004-1772-15), and NC Sea Grant 03-Bio-04.

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Date Accepted: 1 May, 2006.

Addresses: (G.H.D.) University Program in Ecology, Nicholas School for the Environment and Earth Sciences, 135 Duke Marine Lab Rd., Beaufort, North Carolina 28516. (D.R.) University Program in Ecology, Department of Biology, Nicholas School for the Environment and Earth Sciences, 135 Duke Marine Lab Rd., Beaufort, North Carolina 28516. (C.L.) Nicholas School for the Environment and Earth Sciences, 135 Duke Marine Lab Rd., Beaufort, North Carolina 28516. Corresponding Author: (D.R.) E-mail: .