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The dietary and reproductive consequences of fishery-related claw removal for the stone crab Menippe spp.

ABSTRACT The stone crab, Menippe spp. (Say, 1918), fishery is a large fishery in the southeastern United States. One of the primary regulations for this fishery requires that fisherman only harvest crab claws and return the living crab to the ocean. This regulation was put in place in an effort to reduce the overall mortality of harvested organisms and to promote fishery sustainability; however, fishery-related claw loss is likely to influence the population through multiple pathways. How fishery-related claw loss influenced stone crab diet choice, prey size selection, and consumption over time was examined, in addition to how these factors may influence the reproduction of harvested individuals. The consumption of soft-bodied prey, such as polychaete worms, was not influenced by claw loss. In contrast, claw loss has strong negative impacts on the consumption of more common hard-bodied prey, such as bivalves. Specifically, 1-clawed stone crabs consumed bivalves that were approximately 15% smaller after claw removal and consumed, on average, approximately 50% fewer bivalve prey than 2-clawed stone crabs. These decreases in consumption persisted over time. As a result of these dietary changes, stone crabs are likely to experience energetic constraints after claw removal that may limit the growth, reproduction, and survival of harvested stone crabs.

KEY WORDS: stone crab, Menippe mercenaria, fisheries management, benthic ecology, reproduction

INTRODUCTION

The sustainability of many global fisheries has been questioned (Pauly et al. 2002, Mora et al. 2009). To address sustainability concerns, some fisheries have adopted unique fishing techniques or regulations. Claw-based crab fisheries are one such example. These fisheries occur globally, including fisheries based on the crabs Menippe spp. (Bert et al. 1978), Chaceon affinis (Robinson 2008), Cancer pagurus (Fahy et al. 2004), and Uca tangeri (Oliveira et al. 2000). Rather than harvesting the entire organism, these fisheries harvest crab claws only, with the hope that some declawed individuals may regenerate their claws (Patterson et al. 2009). This fishery approach decreases the instantaneous mortality rate of the harvested crabs relative to fisheries that harvest the entire animal (Davis et al. 1978). This allows surviving harvested crabs to reenter the fishery after they regenerate their claws (Bert et al. 1978), and ideally allows harvested individuals to contribute toward population growth through reproduction.

The stone crab Menippe spp. (Say, 1918) fishery is an example of a claw-based fishery and is the fifth most valuable crab fishery in the United States (National Marine Fisheries Service 2012). This fishery is present along most of the southeast and Gulf coasts of the United States, although the majority of commercial landings come from the state of Florida. The commercial Florida stone crab fishery began during the early 1960s (Bert et al. 1978), and landings quickly increased to a maximum during the late 1990s (Muller et al. 2006), but have decreased since that time despite rapid increases in fishing effort throughout the 1990s (Muller et al. 2011). Two current fishery regulations initiated during the 1970s in Florida may be particularly problematic for stone crabs: first, allowing the removal of both claws (Muller et al. 2011), and second, allowing claw removal from females (Bert et al. 1978).

Stock assessments have determined that the stone crab fishery in Florida has been overfished for at least the past 15 y (Muller & Bert 1997, Muller & Bert 2001, Muller et al. 2006, Muller et al. 2011). In an effort to combat overfishing, the state of Florida implemented the passive reduction stone crab Trap Limitation Program in the 2002 to 2003 fishing season. This program is designed to reduce the number of traps in the stone crab fishery by not selling additional trap certificates and by decreasing the number of trap certificates received when they are transferred between owners. The goal of the program is to reach 600, 000 traps in the fishery, a goal that will take 37 y to reach at the current rate of trap reduction (Muller et al. 2011). The catch per unit effort in pounds of claws per trap has remained consistently low (Muller et al. 2011) despite the decline in traps since this program was implemented (total fishing effort from 2002 to 2010 declined by 16.5%, or roughly 260, 000 traps). The lack of increase in catch per unit effort with the declining number of traps suggests the population is not responding positively to decreased fishing pressure. Thus, current management strategies may not be as sustainable as intended.

Fishery-related claw removal may impact stone crabs negatively by increasing crab mortality directly (Davis et al. 1978, Simonson & Hochberg 1986), or by imposing energetic constraints on growth and reproduction. Energetic constraints may be caused by increasing energetic demands during the process of claw regrowth or by reducing energy intake because of diet or foraging changes after claw removal (Juanes & Hartwick 1990; reviewed in Juanes and Smith [1995]). The goal of this study was to examine the potential negative energetic impacts of claw regeneration and decreased energy intake, and to determine how these consequences of claw loss may influence the energy available for reproduction.

Stone crabs have large claws that represent up to 50% of their body weight (Davis et al. 1978). These large, strong claws allow these crabs to specialize in consuming hard-shell bivalve prey (Yamada & Boulding 1998), the primary food consumed by stone crabs (Gunter 1955, Menzel & Nichy 1958). Claw loss in other crab species is known to reduce consumption rates and alter diet selection (Smith & Hines 1991, Juanes & Smith 1995, Brock & Smith 1998, Patterson et al. 2009, Delaney et al. 2011). Thus, it is likely that removing 1 or more claws will similarly limit the foraging capabilities of harvested stone crabs, causing them to reduce overall consumption, consume smaller prey, or alter their diet qualitatively to consume more manageable foods such as sea grass (Bender 1971) or soft-body prey.

Any negative impacts of claw loss will persist until claw regrowth at the next molt, which in legal-size female stone crabs (carapace width [CW] 88 mm or larger) occurs annually in the fall (Gerhart & Bert 2008). In addition, the molting period of female stone crabs occurs during the early months of the fishing season (Fig. 1), increasing the likelihood that females will lose a claw after the annual molt and that the resulting 1-clawed female stone crabs will not regenerate their claw until after the next spring-summer spawning season. Consequently, any changes in foraging after claw loss are likely to persist leading up to and throughout the spawning season, and such changes may alter the energy available for egg production.

The link between prey consumption and reproductive effort has been demonstrated across a broad range of taxa (e.g., mammals [Ward et al. 2009], reptiles [Shine & Madsen 1997], birds [Holford & Roby 1993], fish [Izquierdo et al. 2001], annelids [Davies & McLaughlin 2003] and crustaceans [Griffen 2014]). In addition, the quality of prey has been linked to reproductive output for some species. For example, the crab Carcinus maenas has a lower reproductive output when it consumes a greater proportion of algal material relative to its preferred bivalve prey (Griffen et al. 2011), and this may be a result of the fact that many crab guts are adapted for a particular diet (Griffen & Mosblack 2011). Stone crabs are primarily bivalve consumers (Gunter 1955, Menzel & Nichy 1958), and the difficulty of opening these hard-shell prey with a single claw may limit the energy intake of crabs that survive fishery capture. This reduced energy intake may impact the growth and reproduction of harvested crabs negatively.

The following hypotheses were tested: (1) that stone crabs will alter their diet to a more readily consumable (i.e., soft-body) food source after claw loss (as suggested by Bender [1971]); (2) that 1-clawed crabs will consume smaller prey after claw removal, and that the consumption of bivalves would occur at a slower rate for individuals with a single claw (as demonstrated for other molluscivorous crabs [Smith & Hines 1991, Brock & Smith 1998, Patterson et al. 2009, Delaney et al. 2011]), therefore decreasing overall nutrient and energy intake; and (3) because many crab species have the capacity to adapt their foraging strategies (Micheli 1995), the hypothesis was tested that individuals with a single claw will become more efficient at consuming prey over time, thus partially compensating for altered diets or reduced foraging after claw loss. Last, the results are used to project the potential negative energetic impacts of claw loss on reproductive effort.

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MATERIALS AND METHODS

A series of experiments was conducted to examine the influence of claw loss on diet choice. The first 2 experiments examined different aspects of qualitative diet changes (i.e., prey switching). The third experiment examined changes in prey size selection after claw loss. The fourth experiment was a long-term experiment to examine the amount of food consumed after claw loss and whether this changed over time. All crabs used in the following experiments were collected from North Inlet estuary, near Georgetown, SC (33[degrees]20' N, 79[degrees] 10' W). Stone crabs in this area are generally hybrids of Menippe mercenaria and Menippe adina (Bert 1985). For the purposes of this study, the hybrids have not been distinguished. Also, approximately 40% of the stone crabs in the sample population had left-handed crusher claws, similar to what has been reported in other areas (Cheung [1976] for Menippe mercenaria). Thus, both left-handed and right-handed crabs have been included haphazardly in the following experiments. These experiments were conducted at the Baruch Marine Field Laboratory, in Georgetown, South Carolina. After the description of these experiments, the translation of observed diet changes into the likely impacts of claw loss on the energy available for reproduction is described.

Diet Choice Experiment 1

A total of 36 stone crabs (22 females [mean] and 14 males; CW [+ or -] SD, 90.7 [+ or -] 10.6 mm) were collected for use in the first experiment. The larger, crusher claw was removed from 19 of these stone crabs within 24 h of their capture. The crabs (each of which survived in the laboratory for several weeks) were housed in individual 5-gal buckets, each provided with a separate flow-through seawater source, allowing water temperature and salinity to fluctuate with ambient conditions. The experiment was conducted over 4 72-h trials (blocked by time) during a 2-wk period. A control, which consisted of a bucket without a crab and the same amount of each food item, was included in each experimental block to account for any consumption-independent changes in biomass of the provided diet items.

Each crab was provided with 6 diet options simultaneously that are commonly found in oyster reefs within North Inlet estuary: eastern oysters (Crassostrea virginica), hard clams (Mercenaria mercenaria), ribbed mussels (Geukensia clemissa), green algae (Ulva spp.), red algae (Gracilaria spp.), and sun sponge (Hymeniacidon heliophila). Because of large differences in the mass-to-volume ratio between these food items, the mass and volume of the different food types provided could not standardized simultaneously. The reasoning was that crabs are consumption limited by the volume of space in the stomach, and therefore an attempt was made to standardize the relative volume of consumable tissue across diet types. They determined the amount of food consumed as the difference between the initial and the final blotted wet weight of each food item throughout the 72-h experiment. Although using wet weights is less accurate than using dry weights, it was necessary because stone crabs were fed living organisms, and the initial dry weight could not be determined without sacrificing the provided organisms. The amount of each food type consumed was analyzed using a multivariate linear mixed effects model (LMER in R), using the logarithm of wet weight consumed for each diet item as response variables, number of claws, sex, and CW as predictor variables, and trial date as a random blocking factor. This was followed by individual linear mixed-effects models using the same variables to examine each diet item separately.

Diet Choice Experiment 2

After finding no evidence of prey switching from bivalve prey to any of the previously mentioned diet items as a result of claw loss (see Results), another series of diet choice studies was conducted to assess the selection of various types and sizes of other prey in June 2013. They did this using 2 sequential experiments with a single set of 24 male stone crabs (mean CW [+ or -] SD, 81.3 [+ or -] 10.6 mm), and examined prey selection before and after removing the larger, crusher claw. Females were not included in these experiments because of low capture rates; however, no differences in consumption between male and female crabs were observed in either diet choice experiment 1 or the long-term consumption experiment. Because the same crabs were used for both experiments, the 2-clawed treatment of each experiment was conducted first (diet choice experiment 2, then prey size selection, as described later), and then the larger, crusher claw was removed from the crabs to conduct the 1-clawed treatment of each experiment (diet choice experiment 2, then prey size selection). Between each experimental treatment, crabs were starved for 48 h to standardize hunger. For both experiments, the crabs were housed in the same individual 5-gal buckets, each provided with a separate flow-through seawater source, allowing water temperature and salinity to fluctuate with ambient conditions. At the end of these 2 experiments, the remaining claw was removed from all crabs to assess the qualitative feeding habits of no-clawed crabs (details provided later).

For diet choice experiment 2, the crabs were provided with 3 small ribbed mussels (between 40 mm and 45 mm) and either 3 acorn barnacles (Balanus spp.) or 3 pieces of polychaete worms (Amphitrite ornata) for 48 h during both the 1- and 2 clawed treatments. These prey items were chosen because they are consumed by stone crabs (Powell & Gunter 1968) and are relatively abundant in the oyster reef in North Inlet estuary. For analysis, the results of 2-clawed and 1-clawed trials for each single crab were paired using a multivariate linear mixed-effects model (binomial distribution) with proportion consumed as the response variable; number of claws, prey type, and crab size as predictors; and crab identification number as the random factor to account for repeated measurements.

Prey Size Selection

A broad size range of mussels was provided to the same 24 male crabs before and after claw removal to determine the impact of claw loss on prey size selection. Each crab was provided with 18 ribbed mussels (collected from North Inlet estuary)--3 from each of 6 different shell length size classes: 30-35 mm, 40-45 mm, 50-55 mm, 60-65 mm, 70-75 mm, and 80-85 mm. The number of mussels from each size class consumed on a daily basis was recorded over the 96-h experiment to determine which mussels were consumed first. The 1-clawed trials were conducted for an additional 24 h (120 h total) to compensate for lower overall feeding rates after claw removal.

The mean shell length of the ribbed mussels provided to the 1-clawed and 2-clawed crabs was 57.16 mm and 57.45 mm, respectively. The mussel shell length-to-crab CW size ratio (mussel-to-CW ratio) was calculated for each mussel to account for the range in crab sizes used in the experiment. The maximum mussel-to-CW ratio provided before and after claw removal was 1.21 and 1.20, respectively. The minimum mussel-to-CW ratio provided was 0.28 for both treatments. A multivariate linear mixed-effects model (Poisson distribution) was used to examine the order of mussel sizes cracked, with a higher ranking indicating they were consumed later. The number of claws, mussel-to-CW ratio, and crab size were included as predictor variables in this analysis, and crab identification number was used as the random factor to account for repeated measurements.

Clawless Crab Feeding Habits

To assess the feeding behaviors of crabs without claws, the remaining claw from the 24 male crabs used in the previous experiments was removed after the conclusion of the prey size selection experiment. The clawless crabs were provided with 6 ribbed mussels (3 in the 30-mm size class and 3 in the 40-mm size class), 3 scorched mussels (Brachidontes exustus), and 3 acorn barnacles for 48 h. Because 2-clawed or 1-clawed crabs were not offered these same options, the data were not analyzed statistically, but qualitative data are included to be expanded on by future studies.

Long- Term Consumption

The 3-mo experiment (June 2012 to August 2012) assessed how claw loss influenced the prey consumption rate by stone crabs and whether 1-clawed stone crabs became more efficient at foraging over time. There was difficulty obtaining the large number of legal-size crabs needed to examine the effects of claw loss while concomitantly accounting for other factors that influence mussel consumption, such as crab size, mussel size, and so forth. This experiment was therefore conducted with a modest number of crabs (13 total: 8 females, 5 males; mean CW [+ or -] SD, 89.1 [+ or -] 6.1 mm). It was expected that the variation in consumption would be greatest for 1-clawed crabs. Therefore crabs were allocated to experimental treatments unevenly, which reflects the desire to maximize the replication of 1-clawed individuals while also attempting to account for differences in size among the available study animals. The considerably lower mussel consumption of 1-clawed crabs relative to 2-clawed crabs (see Results) made the qualitative results unambiguous; however, the low replication means specific quantitative differences in consumption between 1- and 2-clawed crabs in this experiment should be interpreted with caution.

The crabs were housed in individual lobster wire cages (approximate dimensions 152 X 152 X 300 mm), to prevent escape, each within a separate 5-gal bucket that had its own flow-through seawater source, which allowed temperature and salinity to fluctuate with ambient conditions. Stone crabs were divided into 4 different 4.5-mm size classes and were each fed ribbed mussels (Geukensia demissa) ad libitum until declawing. At the start of the experiment (June 4, 2012), the larger, crusher claw was removed from 9 of the 13 stone crabs. Four stone crabs, one from each size class, were not declawed and served as control stone crabs in the experiment.

All stone crabs were provided with a diet of 5 live ribbed mussels daily, and fragments of consumed ribbed mussels were removed after 24 h. Any ribbed mussels not consumed within 1 wk were replaced. The ribbed mussels used in the experiment ranged from 55-75 mm in length and were scaled with respect to the 4 crab size classes. The ribbed mussels provided to each crab were consistent within 1 mm for the duration of the experiment. The length of all ribbed mussels provided was measured prior to placement in the aquaria and each was marked with a small dot of nail polish to allow distinction between individual ribbed mussels.

For each day of the experiment, the total number of mussels cracked was recorded to determine whether crabs would improve in their ability to crack mussels over time. This ability to improve was examined using a generalized mixed-effects model (Poisson distribution), with number of mussels cracked daily as the response variable, days in the experiment as a continuous predictor variable, number of claws and sex as categorical predictor variables, and crab identification number as the random variable to control for repeated measures. The interaction between days in the experiment and the number of claws in the initial analysis was included to determine whether 1 and 2-clawed crabs responded differently to the amount of time in the experiment. The interaction was not significant (Z = 0.137, P = 0.89) and was therefore removed from the analysis. To examine the overall difference in consumption between 1- and 2-clawed crabs, the total number of mussels consumed throughout the length of the experiment was calculated for each crab. A paired t-test (paired by size class) was used to compare the average number of ribbed mussels consumed during the experiment for 1and 2-clawed crabs (data from multiple 1-clawed crabs within a single size class were averaged prior to this analysis).

Reproductive Consequences

Using calorimetry, the potential reproductive consequences of devoting energy to claw regeneration and decreased energy intake resulting from foraging limitations were determined. The energetic cost of claw regeneration was calculated first by calculating the energy necessary to regenerate a crusher claw to full preremoval size, assuming that the energy required to regrow a claw is equivalent to the energy content of the claw itself. This is a conservative assumption if claw loss causes long-term stress that elevates resting metabolic rates. Only the regenerated muscle tissue of the claw was considered in the following calculations, because crabs must regenerate exoskeleton material during molts (Williams et al. 2009) regardless of claw loss. The energetic content of muscle tissue (in kilo-Joules per gram) was determined from stone crab claws using a Parr 6725 micro-oxygen-bomb calorimeter and using triplicate subsamples of claw muscle tissue (mean pellet mass [+ or -] SD, 0.024 [+ or -] 0.002 g) from 10 female stone crabs. There was no trend in the energetic content of muscle tissue with CW ([R.sup.2] = 0.179, P = 0.1295), so average value of 17.5 [+ or -] 1.9 SD kJ/g was used in further calculations.

The mass of crusher muscle (in grams) was determined as a power function of CW (n = 32; Mass (in grams) = 6.022 X [10.sup.-7] C[W.sup.3.55], [R.sup.2] = 0.556) from field-collected crabs. The energetic content of the muscle tissue was multiplied by crusher muscle mass to estimate the total energetic investment (in kilo-Joules) required by claw regeneration to full preremoval size.

To determine the potential energetic consequences of decreased consumption, the amount of energy consumed daily in terms of eastern oysters (Crassostrea virginica, common prey consumed in the natural environment [Menzel & Hopkins 1955]) by 1- and 2-clawed stone crabs was estimated first. Laboratory-based daily consumption rates were used for eastern oysters in these calculations (3.2 oysters/day [Brown & Haight 1992]), because field consumption rates available in the literature were usually confounded with other factors (e.g., disproportionately small prey provided [O'Connor et al. 2008] or multiple prey types provided [Macreadie et al. 2011]). This number was consistent with the ribbed mussels feeding rates of 2-clawed crabs in the current study. It was assumed that 1-clawed individuals of all CWs experience, at a maximum, the same foraging limitation seen in this study (approximately 50%, with no increasing trend over time). This was estimated using the decreases in consumption found in the various components of this study (i.e., diet choice experiment 1, 65%; prey size selection experiment, 45.5%; and long term consumption, 52%; see Results). Thus, the number of eastern oysters consumed daily was decreased by up to 50% for 1-clawed stone crabs. The daily energy consumed (in kilo-Joules) was determined by multiplying the total daily consumption of oyster mass by the energetic content (in kilo-Joules per gram) of its tissue (using the mass [in grams] of a medium-sized oyster [Dame 1972], the number of oysters consumed as described earlier, and the energetic content [Krishnamoorthy et al. 1978]).

The energy content of field-collected egg masses (n = 10, run in triplicate) from 2-clawed female crabs was also determined. All egg masses used in the following calculations were collected in July 2013 or August 2013 and were bright orange, indicating they had been recently extruded. There was no trend in the energetic content of egg tissue with CW (adjusted [R.sup.2] < 0.001, P = 0.7864), so an average value of 25.8 [+ or -] 0.774 kJ/g was used in further calculations. This is almost identical to the energy content of crustacean eggs previously reported for the European green crab Carcinus maenas (24.97 [+ or -] 0.77 kJ/g for extruded eggs; 25.31 [+ or -] 0.86 kJ/g for vitellogenic ovaries [Griffen 2014]). Subsequently the number of eggs in a given egg mass of these same crabs was determined. The eggs were dried for 72 h at 65[degrees]C, and the number of eggs in a preweighed sample (~2 mg) of egg tissue was determined by moistening the eggs, placing the samples onto a gridded counter plate, and counting the eggs using a dissecting scope. The number of eggs in 1 g of tissue was then divided by the energetic content of the eggs to yield the number of eggs per kilo-Joule of energy. There was no trend in the number of eggs per kilo-Joule with CW (adjusted [R.sup.2] < 0.001, P = 0.900), so an average value (mean energetic content [+ or -] SD, 4,469 [+ or -] 418 eggs/kJ) was used in further calculations.

Next, to demonstrate the reproductive consequences of decreased consumption, the energetic loss resulting from claw regeneration or reduced consumption by 1-clawed individuals was converted to its energetic equivalent in eggs. This was calculated by multiplying the average number of eggs per kilo-Joule, as described earlier, by the amount of energy 1-clawed stone crabs will need to allocate to claw regeneration or will not be able to consume after claw removal (consumption of 2-clawed stone crabs less the consumption of 1-clawed stone crabs). A maximum period of 1 y was used with decreased consumption because this is approximately the length of time from the opening of the fishing season until the end of the next spawning season. Shorter periods (1 mo and 6 mo) were also included to represent crabs that are declawed either at the beginning or ends of the fishing season, because these crabs will not have to forage with a single claw for the entire year.

RESULTS

Diet Choice Experiment

Analyses of individual prey types revealed that 1-clawed stone crabs consumed an average of 65% less ribbed mussel tissue (t = -2.231, P = 0.033) and 93% less eastern oyster tissue (t = -2.604, P = 0.0137) than 2-clawed stone crabs (Fig. 2). There was no difference between 1- and 2-clawed crabs for the very minor consumption of hard clams (t = -0.929, P = 0.360), green algae (t = -0.495, P = 0.624), red algae (t = -0.004, P = 0.997), or sun sponge tissue (t = -0.718, P = 0.478). Stone crab sex and CW had no influence on the consumption of any of these prey types (P > 0.2 in all models). Combining all prey types together in a single analysis, 1-clawed stone crabs consumed significantly less than 2-clawed individuals (t = -2.706, P = 0.011).

[FIGURE 2 OMITTED]

Diet Choice Experiment 2

Claw removal appeared to have little impact on diet choice (Table 1). And although stone crabs consistently consumed both bivalve prey and acorn barnacles, both 1- and 2-clawed stone crabs consumed more bivalves than barnacles (Z = 8.41, P < 0.0001). Larger crabs consumed more of both prey types (Z = 3.594, P = 0.0003). All polychaete worms offered were entirely consumed by both 1- and 2-clawed crabs.

Prey Size Selection

Overall ribbed mussel consumption after 96 h was 45.5% greater in the 2-clawed treatment (290 total ribbed mussels consumed) than in the 1-clawed treatment (158 total ribbed mussels consumed). The order in which the ribbed mussels were consumed (their ranking) was dependent on the mussel-to-CW ratio (Z = 18.20, P < 0.001), with larger mussels being consumed later. Furthermore, smaller mussels were consumed first more frequently in the single-claw treatment (Z = 11.00, P < 0.001), but crab size itself did not influence the size of mussels consumed first (Z = 0.320, P = 0.749).

The maximum mussel-to-CW size ratio consumed by stone crabs in the 2-clawed treatment was 1.21, whereas the maximum mussel-to-CW ratio consumed in the 1-clawed treatment was 0.91 (Fig. 3). In both treatments, the first 24 h provided the major trends in ribbed mussel consumption, and the trends became weaker over time as the smaller mussels became depleted. The average mussel-to-CW ratio consumed by stone crabs during the first 24 h for the 1-clawed treatment was significantly less than the 2-clawed treatment (t = -4.69, P < 0.001). This result is consistent with the conclusion that there is approximately a 15% reduction in the size of ribbed mussels consumed by stone crabs after claw removal. After 120 h. the trend remained; the 1-clawed crabs consumed mussels with an average mussel-to-CW ratio that was significantly less than the mussels consumed by the 2-clawed crabs (t = -7.29, P < 0.001).

Clawless Crab Feeding Habits

A few clawless stone crabs (n = 5) were able to consume small ribbed mussels (30-40 mm) by repeatedly damaging them over 48 h; however, most clawless crabs (/? = 19) consumed no ribbed mussels, scorched mussels, or acorn barnacles within the time provided to them.

Long- Term Consumption

Single-clawed stone crabs cracked approximately 52% fewer ribbed mussels than 2-clawed stone crabs during the experiment (P = 0.016; Fig. 4). In addition, the number of ribbed mussels consumed daily varied but did not show an increasing trend with time (Z = 1.198, P = 0.231; Fig. 5). Sex did not influence the number of mussels consumed daily (Z = 0.9824; P = 0.410).

Reproductive Consequences

It was determined that the energetic cost of claw regeneration for a 102-mm-CW crab (the median size for an adult female stone crab) is equivalent to the energy contained in 750,000 eggs. The potential energetic cost of decreased prey consumption was much greater than this. A persistent 50% decrease in bivalve consumption, similar to that seen in the experiments reported here, would represent an annual decrease in energetic intake equivalent to the energy contained in approximately 70 million eggs (Fig. 6).

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DISCUSSION

Energy Intake

Stone crabs drastically reduce energy intake by decreasing bivalve consumption after claw removal. In each of the experiments, 1 -clawed crabs consumed less food by eating smaller prey, and approximately 50% fewer prey after claw loss, and these trends persisted over time. These data also suggest that 2-clawed stone crabs are able to consume a variety of bivalve sizes, but that 1-clawed crabs are limited to smaller prey sizes, presumably as a result of either the mechanical limitation of the remaining cutter claw (Cheung 1976) or simply as a result of reduced handling capabilities with a single claw. It is likely that this level of reduced consumption (50% fewer prey consumed) will continue until the next molting event, when a new claw is regenerated (~ 1 y [Gerhart & Bert 2008]). and could greatly limit the energy available for both reproduction and growth during claw regeneration. Decreased consumption may also extend beyond the initial regenerative molt as a result of the reduced size of the regenerated claw, as demonstrated by Elner (1980) for Carcinus maenas.

[FIGURE 4 OMITTED]

There was no evidence that stone crabs switch their diet to consume more soft-body prey or plant material after claw removal despite finding a decreased amount of bivalves consumed and smaller bivalve prey selected. In contrast, previous studies have suggested that stone crabs also consume seagrass material (Bender 1971), and other crab species change their diet to include more soft-body prey after claw loss (Juanes & Smith 1995). Patterson et al. (2009) found that single-clawed Cancer pagurus (a molluscivorous crab) consumed more fish and fewer bivalves after claw loss, demonstrating that crabs will primarily consume their preferred prey, but may consume other prey out of necessity after claw loss. Both 1- and 2-clawed crabs in our experiment consumed all polychaetes offered. In addition, although not used in the current experiments, 1- and 2-clawed stone crabs will consume tunicates in the laboratory (Hogan unpubl.). Although it has been shown that stone crabs will consume soft-body prey opportunistically in laboratory conditions, it is unclear whether these crabs are able to consume enough soft-body prey in natural field conditions to compensate for the decrease in consumption of their preferred bivalve prey.

[FIGURE 5 OMITTED]

Reproductive Consequences of Claw Loss

The annual fecundity of a median legal-size female stone crab (CW, 102 mm) is around 2 million eggs (assuming a linear relationship between CW and egg production [Ros et al. 1981] and 5 egg broods annually [Porter 1960]). The energetic cost of claw regrowth is approximately 37.5% of the annual reproductive output for this size of crab; however, if the decreases in consumption observed here persisted for an entire year (a likely scenario for females harvested near the start of the fishing season), the cumulative reduction in food consumption would contribute to much greater reproductive energetic constraints.

The energetic cost of reduced consumption is substantial, even if it is less than what is noted here. The energetic cost of altered foraging was calculated assuming 30%, 15%, 5%, and 1% reductions (much less than the 50% reduction observed here). Each of these values still represent a considerable energetic cost relative to annual fecundity (Fig. 6). The magnitude of this energetic cost is highly dependent on when a crab is harvested during the fishing season, and therefore how long the crab is forced to forage with a single claw prior to molting and claw regeneration. These conclusions are conservative in that they could be exacerbated further by the energetic requirements of claw regeneration, the imperfect assimilation efficiency of consumed food, or changes in the nutritional content of the food consumed after claw loss. The potential energetic cost of altered food consumption after claw loss relative to the annual energetic investment in egg production is therefore considerable. These results suggest the harvesting of stone crab claws has the potential to lower the reproductive success of legal-size female stone crabs.

Consistent with the negative predicted impact of claw loss on reproductive success, Wilber (1995) found that female (and male) crabs that were regenerating claws were less likely to be found in mating pairs, and that females regenerating claws had reproductive patterns that peaked later and ended earlier, suggesting a constrained reproductive season (i.e., fewer clutches) and an overall decrease in reproductive effort for harvested female crabs. It remains unclear whether clutch size in stone crabs is also influenced negatively by claw loss as it is for other crab species (e.g., a 45% decrease for Necora puber that were missing limbs [Norman & Jones 1987]). Decreased

reproductive effort after claw loss appears to be a general pattern across crab species (reviewed in Juanes and Smith [1995]); however, 1-clawed gravid female stone crabs are observed in the field. This confirms that individuals are able to compensate in some way for the energetic constraints after claw loss.

[FIGURE 6 OMITTED]

One way that individual crabs may compensate for claw loss to maintain some reproductive output is to alter the allocation of energy between reproduction, growth, and maintenance. Changes in energetic allocation appear to occur in stone crabs. For example, field-collected stone crabs regenerating a single claw grow 11 % less than stone crabs with 2 normal-size claws, and stone crabs regenerating 2 claws grow 31 % less (Savage & Sullivan 1978). This decreased annual growth will further decrease future reproductive output because stone crabs, similar to most crab species, have size-dependent fecundity (Ros et al. 1981, Hines 1982). These results and conclusions call into question just how much harvested stone crabs will contribute to population growth via reproduction, especially stone crabs with both claws harvested, as is legal in Florida (Muller et al. 2011).

Implications for Management

Decreased consumption will limit the energy available for growth and reproduction of stone crabs regenerating 1 or 2 claws. The extent of this energetic constraint will depend on many factors, including the number of claws removed, crab size, and the degree and duration of decreased foraging capabilities. If the energetic costs of decreased consumption and claw regrowth are even a fraction the size of those calculated here, the impacts on reproduction could be substantial.

One-clawed stone crabs are considered primarily in the current study; however, harvesting both claws is legal in Florida (Muller et al. 2011). Stone crabs with both claws harvested are likely to be affected to a much greater extent by further reductions in foraging ability and increased predation risk. In areas where it is a legal practice to remove both claws from legal-size stone crabs, harvested stone crabs will be completely dependent on foraging with their walking legs, which will intensify foraging limitations because these crabs are strongly limited in their ability to crack bivalves. This is consistent with the clawless crab-feeding habits observed in this study. Crabs were not able to crack bivalve prey, but had to damage prey repeatedly to consume even very small bivalves. This indicates that no-clawed crabs will be highly dependent on either weak/ damaged prey, small bivalves, or soft-body prey for food. This, in addition to the much greater mortality rate of individuals with both claws harvested (47% for 2-claw removal compared with 28% for 1-claw removal [Davis et al. 1978]), makes it unlikely that clawless individuals will contribute to population growth. Furthermore, mating is competitive in stone crabs (Wilber 1989b) making it unlikely that clawless male stone crabs will be able to compete for mates successfully. Although the current stone crab fishery regulations were established to promote the reentry of harvested crabs to the stock population, the results of this study and previous studies suggest that harvesting both stone crab claws may limit this possibility.

ACKNOWLEDGMENTS

The authors thank the staff at the Baruch Marine Field Lab for their assistance during this research. This work was supported by grants from the National Science Foundation (grant no. OCE-1129166), the Lerner Grey Memorial Fund of the American Museum of Natural History, and the Slocum-Lunz Foundation.

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JESSICA M. HOGAN (1) * AND BLAINE D. GRIFFEN (1, 2)

(1) Marine Science Program, University of South Carolina, 701 Sumter Street, EWS 617, Columbia, SC 29208; (2) Department of Biological Sciences, University of South Carolina, 715 Sumter Street, Columbia, SC 29208

* Corresponding author. E-mail: jess.mary.hogan@gmail.com DOI: 10.2983/035.033.0314
TABLE 1.

The proportion of ribbed mussels (Geukensia demissa), acorn
barnacles (Balanus spp.), and polychaete worms (Amphitrite
ornata) consumed by 2- and 1-clawed crabs during diet choice
experiment 2.

No. of      Proportion of prev consumed
claws
         Ribbed    Acorn     Polychaete
         mussel   barnacle      worm

Two       0.73      0.49
          0.89                  1.0
One       0.94      0.24
          0.86                  1.0

Rows represent the different experimental comparisons.
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