Effects of claw autotomy on green crab (Carcinus maenas) feeding rates

Journal of Sea Research 103 (2015) 113–119

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Effects of claw autotomy on green crab (Carcinus maenas) feeding rates Paula S. Tummon Flynn, Cassandra L. Mellish, Tyler R. Pickering, Pedro A. Quijón ⁎ Department of Biology, University of Prince Edward Island, 550 University Avenue, Charlottetown, Prince Edward Island C1A 4P3, Canada

a r t i c l e

i n f o

Article history: Received 13 March 2015 Received in revised form 16 June 2015 Accepted 3 July 2015 Available online 15 July 2015 Keywords: European green crab Autotomy Predation Shellfish Atlantic Canada

a b s t r a c t The European green crab (Carcinus maenas) is a voracious non-indigenous predator and a threat to Atlantic Canada's shellfish industry. Its foraging ability, however, may be affected by the occurrence of injuries such as the loss of a cheliped (claw). Given that green crab claws are differentiated into a major crusher and a minor cutter, we argue that autotomy (the reflexive loss of a limb) affects feeding rates, and that this effect depends on which particular claw is lost. We examined the incidence of injuries in two green crab populations of the southern Gulf of St. Lawrence during July–October, 2012. Then we experimentally assessed the influence of the loss of each type of claw upon crab feeding rates over two size-classes of American oysters (Crassostrea virginica) and soft-shell clams (Mya arenaria). Field injury surveys showed that 12.4% of the green crabs collected were missing a claw (the cutter and/or crusher claw). Injury rates increased linearly with crab size, and were found to vary with location. Laboratory experiments showed that, compared to intact crabs, the loss of the crusher claw reduced oyster mortality rates by ~93–100%. The loss of the crusher also reduced feeding on small soft-shell clams but only temporarily. The loss of the cutter claw had little impact on green crab feeding rates on oysters and soft-shell clams of either size. Combined, these results suggest that the loss of a claw has an effect on the ability of green crabs to consume commercially important species but this effect depends on which claw is lost and which prey is targeted. It follows that injury rates should be taken into consideration when monitoring and forecasting the potential impacts of green crab populations, particularly on oyster beds. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Most decapod crustaceans have the ability to autotomize their appendages in response to injury or the threat of injury (Juanes and Smith, 1995; Maginnis et al., 2014). Autotomy is the reflexive selfamputation of an appendage at a predetermined breaking point and is usually related to agonistic interactions or the handling associated with fishing (Juanes and Smith, 1995; Lindsay, 2010; Pickering and Quijón, 2010). Although casting off limbs helps to evade predators and limit more serious injuries (McVean, 1982), it may also involve costs such as a reduced foraging efficiency (Davis et al., 2005; Patterson et al., 2009). In most decapod crustaceans, it requires two or three molts for regenerated appendages to attain their pre-autotomized sizes (Savage and Sullivan, 1978) and the regenerating limbs can be significantly weaker than their full size counterparts (Brock and Smith, 1998). The loss of a cheliped (claw), the most common type of injury among decapods (Abello et al., 1994; Delaney et al., 2011; McVean, 1976; Smith and Hines, 1991a), may be particularly disadvantageous. Claws are used during agonistic interactions and for capturing and handling prey (Mariappan et al., 2000). The loss of a claw has been found to reduce foraging efficiency (Davis et al., 2005; Patterson et al., 2009), as

⁎ Corresponding author. E-mail address: [email protected] (P.A. Quijón).

http://dx.doi.org/10.1016/j.seares.2015.07.002 1385-1101/© 2015 Elsevier B.V. All rights reserved.

well as growth, reproduction, competitive ability, and survival (Abello et al., 1994; Juanes and Smith, 1995; Pickering and Quijón, 2010). Changes in the density of predators like crabs and lobsters are intuitively expected to influence their potential effects on prey (Quijón and Snelgrove, 2005; Delaney et al., 2011). However, injury rates, which are known to alter predator feeding abilities (Davis et al., 2005), have only recently begun to gain attention among monitoring groups (C. MacKenzie, DFO-Newfoundland; Pers. Comm.). Considering that the potential impact of these species depends on their condition and ability to consume prey (e.g. Floyd and Williams, 2004; Dittel and Epifanio, 2009), it is surprising that there has been relatively little effort devoted to the description of the prevalence of injuries and their influence on the role of these species as predators. The European green crab (Carcinus maenas) is a voracious predator of a broad range of bivalves (Elner, 1981; Grosholz et al., 2000; Tan and Beal, 2015). Outside its native range the green crab has higher predation rates on bivalves than some native predators (Walton et al., 2002), and has been linked to the decline of several shellfish resources in the North Atlantic (Ropes, 1968; Smith and Chin, 1951), the Pacific coast (Grosholz and Ruiz, 1995; Grosholz et al., 2000), and the shores of Australia (Walton et al., 2002). Small bivalves are especially vulnerable to green crab predation because they are easier to handle than larger ones and entail lower risk of claw damage (Pickering and Quijón, 2011; Smallegange et al., 2008). Since the establishment of green crabs in Prince Edward Island (hereafter PEI) in the 1990s (Audet et al., 2003), this

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species has been considered a threat to commercially important shellfish like soft-shell clams (Mya arenaria), American oysters (Crassostrea virginica) and blue mussels (Mytilus edulis) (Miron et al., 2005; Pickering and Quijón, 2011; Tan and Beal, 2015), among others. While green crab populations continue to grow and spread in the region (Audet et al., 2008), their effects have been assessed on prey populations (Floyd and Williams, 2004; Miron et al., 2005; Pickering and Quijón, 2011; Tan and Beal, 2015), benthic communities (Gregory and Quijón, 2011), and critical habitats (Malyshev and Quijón, 2011). The potential influence of claw injuries, however, remains under-studied in the region and elsewhere in its broad distributional range. This study measured the incidence of limb injuries in green crab populations from two PEI locations and assessed the potential influence of injury on their feeding rates upon oysters and soft-shell clams. Given that green crab claws are differentiated into a minor (cutter) and a major (crusher) claw (Mariappan et al., 2000), we argue that the effect of injury may depend on which claw has been lost. Previous studies have removed either the crusher (e.g. Delaney et al., 2011) or the cutter claw (e.g. Matheson and Gagnon, 2012) in order to document the effect of individual injuries. However, to our knowledge no previous studies have explicitly compared feeding rates of intact green crabs with those of crabs missing either the crusher or the cutter in a same systematic design involving multiple prey. Our working (null) hypothesis was that individual prey mortality levels are similar among prey exposed to intact and injured crabs. However, the literature (e.g. Delaney et al., 2011; Patterson et al., 2009), suggests that higher prey mortality rates should be expected from intact (un-harmed) crabs. These results were combined with data collected from the injury surveys to assess the influence of autotomy on the potential impact of this invasive species.

Gulf of St. Lawrence

PEI

Canada 41 N 61 W

US

PEI MB BB

SR 25 km

NR

2. Material and methods 2.1. Study area and crab injury surveys To assess injury rates in green crabs, intensive trapping surveys were conducted during June–October of 2012 in Souris River and North River, PEI (Fig. 1). Souris River is located on the eastern end of the island and drains into Colville Bay, while North River is on the south shore of PEI and drains into the Hillsborough Bay. Both areas are shallow (up to ~ 3 m deep) estuaries with b2 m tidal ranges and are characterized by mainly sandy bottoms, eelgrass beds and fringing salt marshes. In each area, crabs were collected weekly using 5 Fukui traps (60 cm × 45 cm × 20 cm high, with a 40 cm opening at each end) placed approximately 5 m apart. Traps were baited with Atlantic mackerel (Scomber scombrus) and deployed below the lower intertidal zone for 24 h in North River and 2 h in Souris River. The shorter soak time used in Souris River is related to the much higher density of green crabs in that area (see Gregory and Quijón, 2011). Based on preliminary observations, a 2-hour soak period was considered appropriate for the sole purpose of collecting a representative number of crabs in Souris River (we did not intend to statistically compare between locations); a longer soak time may have resulted in trap saturation and the escape of crabs after the bait was consumed (Miller, 1980). Crabs collected were measured from tip to tip at the widest points of the carapace to the nearest mm and data on crabs per trap, carapace width (CW), sex, and injuries (missing and regenerating limbs) were recorded. A total of 13 samples from Souris River and 12 from North River were collected. 2.2. Collection of specimens for experimental manipulations Using Fukui traps, intact male green crabs (60–80 mm CW) were collected from Souris River to be used in laboratory trials during the same season. Green crabs were held and starved for 48 h before each trial to standardize hunger levels (Mascaró and Seed, 2001). Two shellfish species were used as prey: American oysters (C. virginica) and soft-shell

Fig. 1. Map of Prince Edward Island (PEI) in the Gulf of St. Lawrence, Atlantic Canada, with the approximate locations of Souris River (SR), North River (NR), Brackley Bay (BB) and Malpeque Bay (MB).

clams (M. arenaria). We used two prey size ranges: small (15–25 mm shell length or SL) and medium-sized bivalves (25–35 mm SL). Oysters were obtained from a commercial oyster lease in Malpeque Bay whereas soft-shell clams were collected manually from the mid-intertidal zone of Brackley Bay (Fig. 1).

2.3. Laboratory experiments and crab injury treatments Feeding trials were conducted in glass tanks (21.6 cm × 41 cm × 25 cm high) filled with prepared seawater (~25 ppt, 18 °C) and aerated with airstones. After each individual trial, predator and prey were replaced, tanks were cleaned and the seawater drained and replaced. The top of the tanks was always covered with a hood to prevent crab escape and their sides were covered to maintain a dark environment and decrease distracting visual stimuli (Pickering and Quijón, 2011). Thirty oysters or soft-shell clams of one size class were placed in the tanks and given an hour to acclimatize before the inclusion of a predator. Once the predator was added, trials lasted 72 h and observations of prey mortality were recorded every hour for the first 3 h and then every 24 h. We qualified shellfish mortality as the crushing or complete opening of a bivalve shell. A few trials in which the green crab unexpectedly died or showed signs of molting were not considered. Experiments conducted with intact (un-injured) green crabs were paralleled with experiments conducted with crabs missing the cutter (left) claw or the crusher (right) claw (Table 1). Uncommon “lefthanded” crabs were not used in this study. Claw autotomy was induced 1 h before the beginning of a trial by squeezing the merus of the cheliped with pliers until the crab spontaneously dropped the claw (see Smith, 1990). The number of trials/replicates carried out for each

P.S. Tummon Flynn et al. / Journal of Sea Research 103 (2015) 113–119

Soft-shell clams

Small Medium Small Medium

Green crab condition (treatments) Intact

Missing crusher

Missing cutter

11 13 13 10

15 12 18 9

12 12 11 9

treatment (intact, missing cutter and missing crusher) and each type of prey (shellfish species and size ranges) is summarized in Table 1. 2.4. Statistical analyses For the green crab surveys, rates of injury were estimated as the proportion of green crabs exhibiting injuries (missing at least one limb) by sex, location and type of injury (which limbs were missing). Two-sample tests of equal proportions were used to compare injury occurrence between sexes as well as to compare both limb loss and regeneration frequencies of cutter and crusher claws. The relationship between the proportion of injured crabs and the size class (CW to the nearest mm) was analyzed using linear regressions for the pooled dataset and for data separated by location and sex. Only size classes with ≥15 crabs were used to calculate injury proportions. Between 13 and 56 size classes were used in each regression where the size classes fell between 23 and 78 mm CW. For the experiments assessing shellfish mortality due to intact or injured green crabs, repeated-measures ANOVAs could not be performed due to repetitive violation of ANOVA assumptions, particularly homoscedasticity. Consequently, separate one-way ANOVAs were performed to compare cumulative mortality near the beginning (3 h) and at the end of the trials (24 and 48 h). Statistical analyses were not performed at 72 h, because some of the treatment groups reached the maximum prey mortality after 48 h, precluding the use of ANOVAs. In cases where significant differences were detected between treatments (intact versus missing crusher versus missing cutter), a Tukey's a posteriori test was used to further discriminate which treatments were significantly different. For all ANOVAs assumptions of normality and equal variance were assessed using the Shapiro–Wilk and the Levene's tests, respectively. In the cases where these assumptions could not be met, logarithmic or square root transformations were applied. If assumptions of normality were not met, a Kruskal–Wallis test was performed to compare mortality between the three treatments. When significant differences were found further tests were performed to compare two of the three treatments (intact and cutter lost): two-sample t-tests if normality and homoscedasticity assumptions were met or a two-sample Wilcoxon rank-sum (Mann–Whitney) test if these assumptions were violated. Because differences in cumulative mortality were statistically compared at three time periods (3, 24, and 48 h), a Bonferroniadjusted significance level of 0.0167 was calculated to account for the increased possibility of type-I error. 3. Results 3.1. Injury surveys A total of 4453 green crabs of a size range of 20 to 86 mm CW were collected in North River and Souris River. Overall, 997 (22.4%) of the crabs were missing one or more appendage(s) and 228 (5.1%) had one or more regenerating limbs. The most common injury was the loss of one or more walking leg(s) (630 crabs, 14.1%), followed by the loss of a cheliped (the cutter and/or crusher claw; 552, 12.4%). The loss of the crusher claw (350, 7.9%) occurred only slightly more frequently than the loss of the cutter (304, 6.8%) and the difference was not significant (two-sample test of proportions; z = 1.87, p = 0.62).

0.9

Arcsin (sqrt % crab injured)

American oysters

Size

0.8

A

0.7 0.6 0.5 0.4 0.3 0.2 0.1 20

Arcsin (sqrt % males injured)

Prey

This was also true for the incidences of regenerating crusher (97, 2.2%) and cutter claws (92, 2.1%) found (two-sample test of proportions; z = 0.05, p = 0.96). Only 2.3% of crabs (103) were found to be missing both claws. Male crabs were larger than females (x = 54.3 ± 14.8 mm SD; x = 44.9 ± 10.6 mm SD, respectively) and showed a significantly higher occurrence of injury (two-sample test of proportions, z = 2.63, p = 0.008; 23.7% versus 20.4%, respectively). Despite large temporal variations of injury incidence (8–47%), Souris River had a consistently higher percent of injured crabs than North River (30.4% and 17.1%, respectively). Differences in injury frequency between sexes were also related to location. In Souris River, females had a higher occurrence of injury than males (35.5% and 28.8%, respectively). Conversely, in North River, males (18.3%) had a slightly higher occurrence of injury than females (16.0%). The two sites had a similar percent loss of cutter and crusher claws (~6–8%). We found a significant (positive) linear relationship between carapace width (CW) and the overall incidence of injuries (p (regression) b

30

40

50

60

70

80

30

40

50

60

70

80

0.9 0.8

B

0.7 0.6 0.5 0.4 0.3 0.2 0.1 20 0.5

C

0.4

% females injured

Table 1 Number of trials conducted for each predator treatment and prey type (species and size).

115

0.3 0.2 0.1 0.0 20

30

40

50

60

70

Carapace width (mm) Fig. 2. Incidence of green crab injuries in relation to carapace width. (A): % of crabs missing appendages; (B): % of male crabs missing appendages; (C): % of female crabs missing appendages. All data plotted across locations (Souris River and North River) and survey date (June–October). For (A) and (B) the data were arcsin square root transformed to meet normality assumptions. Linear regressions have been added to the plots. Detailed results of these and similar regressions for separate locations are summarized in Table 2.

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Table 2 Results of linear regressions depicting the relationship between green crab carapace width and the incidence (%) of injuries in Souris River and North River, PEI. Significant p-values are bolded; data sets were arcsin square-root transformed to meet assumptions with the exception of the data sets for females at both locations and at North River. Sample sizes are indicated by N (number of size classes with ≥ 15 crabs) and n (total number of crabs grouped into N size classes for each regression). Both locations

Souris River

2

r = 0.72, p b 0.001; N = 56, n = 4417; y = 0.134 + 0.00697x r2 = 0.67, p b 0.001; N = 55, n = 2607; y = 0.123 + 0.00702x r2 = 0.58, p b 0.001; N = 39, n = 1757; y = −0.0898 + 0.00664x

Proportion injured crabs Proportion injured males Proportion injured females

0.001, r2 = 0.72) (Fig. 2A, Table 2). Similar relationships were found for data separated by gender: males (p(regression) b0.001, r2 = 0.67), and females (p(regression) b0.001, r2 = 0.58) (Fig. 2B,C, Table 2). Similar positive relationships were also found when data were separated by location, with a large majority of the regressions being significant (although r2 values were relatively low; Table 2). 3.2. Feeding experiments The influence of injury on the feeding ability of green crabs changed depending on the type of prey and the type of predator's injury. For experiments using both small- and medium-sized oysters, by 48 h the loss of the crusher claw reduced oyster mortality by approximately 98% and 100%, respectively (Fig. 3; Table 3). At the 3 h point, the loss of the crusher already had an influence on crab feeding rates, but only on medium-sized oysters (Fig. 3). Meanwhile, the loss of the cutter claw did not affect green crab feeding rates (Fig. 3). At 48 and 72 h,

2

r = 0.36, p b 0.001; N = 32, n = 1616; y = 0.238 + 0.00571x r2 = 0.62, p b 0.001; N = 29, n = 1242; y = −0.171 + 0.0115x r2 = 0.14; p = 0.206; N = 13, n = 310; y = 0.154 + 0.00931x

North River r2 = 0.48, p b 0.001; N = 44, n = 2575; y = 0.175 + 0.00552x r2 = 0.37, p b 0.001; N = 42, n = 1158; y = 0.163 + 0.00580x r2 = 0.32, p b 0.001; N = 37, n = 1349; y = −0.00908 + 0.004x

crabs missing the cutter exhibited slightly higher feeding rates than intact crabs, but this difference was not significant (Fig. 3). The loss of either claw did not appear to impede feeding on small or medium soft-shell clams as considerably (Fig. 4). However, the loss of the crusher reduced the rate of feeding on small-sized clams during the first 24 h (by 62% at 3 h and 27% at 24 h), but approached 100% mortality by 48 h (Fig. 4; Table 3). Feeding rates on medium-sized clams were only significantly affected by claw loss at 3 h, where the loss of either claw reduced mortality by ~50% (Fig. 4). 4. Discussion This study shows that injury is common among green crab populations and its incidence varies depending on crab size and location. The influence of injury on green crab feeding rates was also found to depend on the type of prey and the nature (type of limb lost) of the injury. 4.1. Injury surveys

35

Intact Cutter lost Crusher lost

prey mortality (#)

30 25 20 15 10 5 0 0

1

2

3

24

48

72

48

72

hours 30

prey mortality (#)

25 20 15 10 5 0 0

1

2

3

24

hours Fig. 3. Mean (±SE) cumulative mortality of small (15–25 mm; top panel) and medium (25–35 mm; bottom panel) American oysters due to green crab predation during the 72 h laboratory feeding experiments.

Our estimates of injury incidence (22.4%) were similar to the ones reported for other green crab populations (McVean and Findlay, 1979; 20%) but fall well below the injury rates of males (53.7%) reported by McVean (1976). For this and other studies, the use of traps to capture crabs has implicit biases (Quijón and Snelgrove 2005) such as the risk of overestimating rates of autotomy due to the temporary confinement of the crabs. However, we argue that this potential bias was likely minimized by limiting the soaking of traps to 2 h in the area where green crab populations are known to be more abundant (Gregory and Quijón, 2011). Injury incidence increased with carapace size, a relationship also found in green crab populations studied elsewhere (e.g. Juanes and Smith, 1995; Mathews et al., 1999). This linear relationship may be the result of multiple factors. Larger (older) crabs have a longer time to accumulate injuries and, as intermolt periods become also longer with age, have fewer opportunities to regenerate limbs (Smith and Hines, 1991a; Spivak and Politis, 1989). Furthermore, most decapods, including the green crab, have limited growth and stop molting when they reach terminal anecdysis, a state occurring about ten molts after puberty (Carlisle, 1957). Autotomy may also be less frequent in small crabs simply because attacks on them are more likely to result in mortality than in non-lethal injury, as suggested by Delaney et al. (2011). The relationship between carapace size and injury frequency may account for some of the differences observed between North River and Souris River, as larger crabs were usually caught in the latter location. Delaney et al. (2011) expected a similar increase in injury rates in locations where green crabs were more abundant, but could not establish a significant relationship between both variables. Our results are, however, consistent with most other studies that have found that the incidence of injury varies among geographic locations with different population densities (Delaney et al., 2011; Juanes and Smith, 1995). In decapods injury frequency is thought to be independent of sex (Juanes and Smith, 1995) but the evidence is not consistent for green crabs. Some studies have reported a higher incidence of injuries in females (Mathews et al., 1999; McVean, 1976) while others have found it in males (Abello et al., 1994; McVean and Findlay, 1979). This

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Table 3 Results of one-way ANOVAs, Kruskal–Wallis and two-sample t-tests assessing differences in shellfish mortality rates among predator treatments: intact versus missing crusher versus missing cutter claw for ANOVAs and Kruskal–Wallis; intact versus missing cutter for two-sample t-tests and two-sample Wilcoxon rank sum tests. Results are presented for three observation periods only (3, 24 and 48 h; see Materials and methods section). Bolded values highlight significant differences (p b 0.0167). Prey species

Time (h)

American Oysters

3 24 48 3 24 48

Soft-shell clams

Prey size Small

Medium

x2(2) = 5.61, p = 0.060 x2(2) = 25.94, p b 0.001; z = 1.77, p = 0.078 x2(2) = 29.82, p b 0.001; z = 1.81, p = 0.070 F(2, 39) = 56.79, p b 0.001 x2(2) = 19.13, p b 0.001; z = 1.33, p = 0.184 x2(2) = 6.86, p = 0.032; z = 0.92, p = 0.358

x2(2) = 13.06, p b 0.002 t(23) = 1.124, p = 0.273 x2(2) = 23.28, p b 0.001; t(23) = 0.80, p = 0.432 x2(2) = 25.15, p b 0.001; t(23) = 2.21, p= 0.038 F(2, 25) = 5.34, p = 0.012 F(2, 25) = 1.91, p = 0.169 F(2, 25) = 1.63, p = 0.216

study agrees with the latter, finding that males had a higher, although only slightly, incidence of injuries (23.7%) than females (20.4%). Regardless of gender, the incidence of claw loss was considerable, which agrees with most literature that identifies these losses to be one of the most frequent types of injury in decapods (Juanes and Smith, 1995). Jachowski (1974) offered an explanation for this: crabs respond to threats with outstretched claws, which makes these appendages vulnerable and can lead to physical conflict. Claws are directly involved in foraging and agonistic encounters in which the major crusher is used more often in aggression than the minor cutter (Mariappan et al., 2000). As discussed below, the loss of the crusher is also more influential on the potential effects of green crab populations.

35

prey mortality (#)

30 25 20 15 10

Intact Cutter lost Crusher lost

5 0 0

1

2

3

24

48

72

48

72

hours 35

prey mortality (#)

30 25 20 15 10 5 0 0

1

2

3

24

hours Fig. 4. Mean (±SE) cumulative mortality of small (15–25 mm; top panel) and medium (25–35 mm; bottom panel) soft-shell clams due to green crab predation during the 72 h laboratory feeding experiments.

4.2. Influence of injury on feeding rates Several studies have found that a missing claw is disadvantageous to capturing prey, particularly of large size. For example, feeding experiments with Hemigrapsus sanguineus found that when missing a cheliped, crabs preferentially fed on small mussels (Davis et al., 2005). The time required by a crab to crush a prey typically increases exponentially with prey size, and therefore, capturing and breaking large prey requires more energy and likely stronger claws (Elner and Hughes, 1978; Juanes and Hartwick, 1990). The results of this study suggest that the loss of the cutter does not reduce green crab feeding rates on either species or size of shellfish. However, the loss of the crusher had a strong influence on the feeding rates upon oysters and, to some extent, upon soft-shell clams. These results can likely be explained by differences in claw function and prey shell thickness. The crusher is known to yield more force than the cutter (Mariappan and Balasundaram, 1997) so it likely plays a more important role when feeding on hard-shelled prey. In contrast, the cutter has been found to play only a minor role in green crab feeding (e.g. Delaney et al., 2011; Matheson and Gagnon, 2012). Considering that shell thickness is a fairly good indicator of shell strength (Pickering and Quijón, 2011) this factor alone should explain why the loss of the crusher resulted in a serious impediment for the feeding on oysters: in comparison to intact crabs, those with a missing crusher had feeding rates ~98–100% lower. Considering the relatively small size of the prey used in this study (up to 35 mm SL), the limitation imposed by this type of injury is expected to become even more severe with larger sizes of oysters. The influence of the crusher loss had less clear effects on the more fragile (i.e. thinner shell; see Pickering and Quijón 2011) soft-shell clams. For small prey the loss of the crusher claw reduced feeding rates for about 24 h but afterwards those rates approached the ones shown by intact crabs. Although feeding rates were significantly slowed down by the loss of the crusher, we argue that green crabs were still able to break the shells of the clams using their cutters. These results suggest that for bivalve prey green crabs may not necessarily require the combined use of both claws to capture, handle, and effectively consume shellfish. However, if the crabs had limited time to forage on a prey item before being outcompeted or chased away (see Rossong et al., 2011), the early time point (3 h) may reflect more natural conditions and challenges and the reduced feeding rate at this time could be the more realistic measurement. We are also cautious about these results as the limited influence of crusher loss may be biased by the inability of the soft-shell clams to seek refuge into a sediment bottom in the experimental tanks, as they would in a more natural environment (Flynn and Smee, 2010; Ropes, 1968). Likely the lack of a more natural habitat also affected the predator behavior, as habitat type and complexity would influence the handling behavior that crabs exhibit in the field (Wong, 2013). Pickering and Quijón (2011) found that green crabs from this region preferentially chose soft-shell clams over mussels and oysters in tanks and off-bottom experiments. However, in field experiments conducted directly on the seafloor, mussels and soft-shell clams

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were equally preferred (Pickering and Quijón, 2011) or mussels were preferred over soft-shell clams and oysters (Miron et al., 2005). Smith and Hines (1991b) conducted a similar experiment using blue crabs (Callinectes sapidus), which also have dimorphic chelipeds, and where soft-shell clams that were allowed to bury into a layer of sand. These authors found that when the crusher claw was removed foraging rates after 48 h were no different to those of healthy crabs. Despite the lack of sediment in our tanks, our results after 48 h are consistent with those reported by Smith and Hines (1991b). Prey digging (Flynn and Smee, 2010) may not represent a limitation for consumption of species that live attached to hard substrates, such as oysters (Bushek, 1988). In our trials the oysters were not naturally positioned (and attached to a substratum), which we recognize as an experimental limitation. However, we are confident that our results are still meaningful: had this bias affected the feeding rates of crabs missing the crusher, we would have expected an increase in their feeding rates rather than the evident reduction we detected. In cases like this (low mobility of prey) a predator may not critically need a second claw in order to hold a prey while trying to open or crush the shell. However, our experiments may have underestimated the influence of the crusher loss on the feeding rates upon mobile prey like soft-shell clams. Therefore, whether the loss of the crusher delays or prevents feeding on a given prey, the results of this study suggest that this type of injury may have substantial effects on the role played by these predators. As 6–8% of the crabs sampled were missing crusher claws, the impact of this species on oysters could be up to 8% less than what would be predicted from information on crab density alone. However, in populations that suffer higher rates of claw loss, the impact could be reduced much further. We are cautious about extrapolating though, as the large variation found in the temporal incidence of autotomy (8–47%) also suggests that the effect of green crabs may fluctuate widely, probably due to local conditions affecting autotomy incidence. An additional implication of these results relate to vigilance programs aiming to monitor and predict the potential impact of green crabs moving into new areas. Such monitoring programs should not focus exclusively on crab numbers, size and gender, and give also consideration to crab injury rates.

Acknowledgments Funding was provided by NSERC through USRAs (PSTF & CLM) and a Discovery Grant (PAQ) in addition to a MRG from UPEI's Research Office (PAQ). We are grateful of Jeff Davidson and Sophie St-Hilaire (Atlantic Veterinary College, UPEI) and two anonymous reviewers for their valuable comments on earlier versions of this manuscript. We are also grateful of Henrik Stryhn (Atlantic Veterinary College, UPEI) for his advice on the statistical analyses. In addition, Meghan Boswall and Elizabeth Teixeira (Biology, UPEI) were of great assistance in the field and the laboratory. Collection, handling and procedures employed to handle crabs and shellfish species followed UPEI Animal Care protocols.

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