The invasive green crab and Japanese shore crab - Springer Link

Biol Invasions (2007) 9:837–848 DOI 10.1007/s10530-006-9085-6

ORIGINAL PAPER

The invasive green crab and Japanese shore crab: behavioral interactions with a native crab species, the blue crab James A. MacDonald Æ Ross Roudez Æ Terry Glover Æ Judith S. Weis

Received: 15 May 2006 / Accepted: 5 December 2006 / Published online: 20 March 2007 Springer Science+Business Media B.V. 2007

Abstract Blue crabs, Callinectes sapidus (Rathbun), are an ecologically and commercially important species along the East coast of North America. Over the past century and a half, blue crabs have been exposed to an expanding set of exotic species, a few of which are potential competitors. To test for interactions with invasive crabs, juvenile C. sapidus males were placed in competition experiments for a food item with two common non-indigenous crabs, the green crab Carcinus maenas (L.) and the Japanese shore crab, Hemigrapsus sanguineus (De Haan). Agonistic interactions were evaluated when they occurred. In addition, each species’ potential to resist predators was examined by testing carapace strength. Results showed that C. maenas was a

J. A. MacDonald J. S. Weis Graduate Program in Ecology, Evolution, and Natural Resources, Rutgers University-New Brunswick, 14 College Farm Road, Cook Campus, New Brunswick, NJ 08901, USA J. A. MacDonald (&) R. Roudez J. S. Weis Department of Biological Sciences, Rutgers University, 195 University Ave, Newark, NJ 07102, USA e-mail: [email protected] T. Glover Division of Social and Behavioral Sciences, Bloomfield College, Bloomfield, NJ 07003, USA

superior competitor to both C. sapidus and H. sanguineus for obtaining food, while the latter two species were evenly matched against each other. Regarding agonism, C. sapidus, was the ‘‘loser’’ a disproportionate number of times. C. sapidus carapaces also had a significantly lower breaking strength. These experiments suggest that both as a competitor, and as potential prey, juvenile blue crabs have some disadvantages compared with these common sympatric exotic crab species, and in areas where these exotics are common, juvenile native blue crabs may be forced to expend more energy in conflict that could be spent foraging, and may be forced away from prime food items toward less optimum prey. Keywords Agonism Behavior Callinectes sapidus Carcinus maenas Juvenile competition Hemigrapsus sanguineus Marine invasion

Introduction Invasive species are a great concern to biologists and resource managers globally, as the appearance of invasives often leads to a decline in abundance or diversity of native species as well as other ecological problems. Many examples of this process are known in the eastern United States, especially among terrestrial plants. In marine and estuarine systems, invasion may further compound many

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other stressors already present in estuaries (Ruiz et al. 1999). One possible contributing mechanism is competitive interactions between the invasive species and indigenous species that have not previously contended with such competition. The green crab, Carcinus maenas, (L.) a well known and widespread coastal invader, first arrived on the New England coast from Europe in the early 1800s and has expanded its range considerably along the Atlantic coast of the US and Canada (Audet et al. 2003). It has subsequently invaded several other coastlines around the world, including California in 1989 (Jensen et al. 2002). C. maenas has been recognized as an effective predator where it invades, and can have negative effects on biodiversity and fisheries around the world. (Cohen et al. 1995; McDonald et al. 2000; Lohrer and Whitlatch 2002a). A more recent crustacean invader, the Japanese shore crab, Hemigrapsus sanguineus (De. Haan), first found in New Jersey in 1988 (Williams and McDermott 1990) spread rapidly and within 10 years could be found from Cape Cod to Cape Hatteras (McDermott 1998). Their native habitat is primarily but not exclusively rocky intertidal. They prefer animal prey, particularly mussels (Brousseau and Baglivo 2005). The extent to which H. sanguineus overlaps in habitat with C. sapidus is less obvious than with C. maenas. While the former species generally inhabits rocky areas and the latter soft-bottom environments, at Union Beach NJ, H. sanguineus and C. sapidus are both found in the same marsh area, in the vicinity of a mussel bed. H. sanguineus are found frequently in areas with sand and stones (Lohrer et al. 2000) and have also been found occupying fiddler crab burrows in Spartina marshes (Brousseau et al. 2003), habitats often used at high tide by foraging C. sapidus. H. sanguineus is also highly mobile, moving many meters each night from its rocky hiding places to forage (Brousseau et al. 2002); these journeys may take H. sanguineus into areas typically occupied by C. sapidus and make encounters more likely. As these two invasive crab species expand their range and populations they overlap more and more with C. sapidus, which can act as a keystone species and top predator in salt marshes (Hines et al. 1990;

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Silliman and Bertness 2002). C. maenas and C. sapidus have overlapped for many decades already, while any interactions between C. sapidus and H. sanguineus are fairly recent. All three species utilize shellfish and juvenile crustaceans as prey, raising the possibility that the three species will be in direct competition for resources. McDonald et al. (2000) examined effects of C. maenas on juvenile Dungeness crabs (Cancer magister) in Washington State, where C. maenas is a relatively recent arrival. This study showed that C. maenas consistently ‘‘won’’ one-on-one foraging experiments versus C. magister and consistently out competed C. magister for preferred shelter. McDonald et al.’s (2000) study suggests that behavioral characteristics of C. maenas may well contribute to its global success and may come into play in interactions with C. sapidus. Jensen et al. (2002) examined competitive interactions between C. maenas and both exotic and local species of Hemigrapsus shore crabs in Oregon. C. maenas was consistently dominant over a local species of shore crab (H. oregonensis) in competition for a single bivalve (although possibly not an ideal prey item), but not for shelter. Lohrer and Whitlatch (2002a) demonstrated that C. maenas is a more efficient predator of bivalves than any local predator and are also capable of eating substantially more than C. sapidus of equivalent size. Another potential competitive advantage for some species may be that they are better defended against predation than others. Barshaw et al. (2003) showed in a study on lobsters that stronger armor was a more effective defense against predation than weaponry (e.g. claws) or weaker but sharper armor (e.g. spikes or spines). C. sapidus has spikes on its carapace, as well as agility and sharp claws for escape and defense. If C. maenas or H. sanguineus have stronger shells than C. sapidus, this may make the invaders less vulnerable to predation or damage. The present study examines behavioral mechanisms by which C. maenas and H. sanguineus may compete with blue crabs. If in competition C. maenas and/or H. sanguineus can obtain and consume food significantly faster than C. sapidus, these species have the potential to out-compete C. sapidus during random encounters while

The invasive green crab and Japanese shore crab

foraging. In this case, C. sapidus would need effective attacks on the exotic species to drive them away from contested prey items; unsuccessful attack might likewise help the exotics outcompete the native species. Our objectives in this study are to investigate competition of the two invasive species with C. sapidus under controlled conditions. The hypotheses are that juvenile C. maenas and H. sanguineus can out compete C. sapidus for food based on superior abilities to capture food, and that the two invasive species have stronger carapaces than C. sapidus, which protect them better from attacks by predators or competitors. The investigation has three components. Feeding studies examined the time required for individuals of each species alone to detect and find a food item, which species was fastest to find and consume food in pair-wise contests with each other species and the time required to obtain the food during those contests. Agonistic studies, recording which species instigated and which won each fight, were conducted during feeding trials where the crabs also fought. Defense against predators was examined by determining the average carapace strength of each species.

Methods Competition for food Male individuals of H. sanguineus and C. sapidus and male and female individuals of C. maenas were collected from sites in Long Island and New Jersey in the summers of 2004 and 2005 and maintained in the laboratory in aerated aquaria in 30 ppt sea water and a 14/10 light cycle. Only individuals that had both chelipeds and all walking legs intact were included. (Both male and female C. maenas were used because preliminary tests showed no differences in responses between males and females of this species, but differences were observed in male and female C. sapidus. H. sanguineus exhibits strong sexual dimorphism in size and chelal shape between males and females.) After being unfed for 24 h, they were placed in a test aquarium and videotaped. The test aquarium consisted of a 20 gallon tank (32 · 76.5 cm, 2448 cm2 area) covered

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on the bottom with 2 cm of sand and finely crushed shells too small to hide under, and a single food item anchored in the center. The water in the aquarium was at room temperature (~23C), 7 cm (5 cm above the substrate) depth and 30 ppt salinity. Crabs were initially introduced into opaque containers at opposite ends of the aquarium where they acclimated to the tank for 10 min; these were opened simultaneously at the beginning of each trial. The food was placed in the tank immediately after the crabs were first confined. Trials were all run in the late afternoon in dim light (the video camera could not record in the dark) in a secluded room with no outside disturbances. Observers viewed the video from a monitor outside. The food item was usually a ribbed mussel (Geukensia demissa-Dillwyn), but on occasion was a small silverside (Menidia menidia-L.). No species exhibited a significantly different response to either type of food compared to the other, so food type was not a factor in the outcome of the trials. The food was anchored to a large plexiglass plate buried beneath the substrate, forcing crabs to feed on the food item in place. Food items were small, (50 mm maximum length), so competitors could not simultaneously feed on the item without interacting. The water was circulated by means of air stones (placed on opposite sides of the tank, creating a current away from the food) for 10 min prior to the start of the experiment to disperse the food scent throughout the aquarium. The air was turned off prior to the experiment. Before each trial, the tank was washed and the water replaced. All three crabs have different carapace shapes; C. sapidus are longer mediolaterally and flatter dorsoventrally, while C. maenas are thicker dorsoventrally and more truncated across the carapace, having a more compact but solid shape. Carapaces of male H. sanguineus are a shape somewhere in between that of the other two species, and generally smaller, but have massive chelipeds which contain a higher proportion of their bulk. As a result, C. maenas and H. sanguineus are more massive than C. sapidus of similar size. C. sapidus have long spines at the lateral tips of their carapace. Therefore, crabs were matched

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by mass rather than by carapace width, which would have put C. sapidus at a disadvantage. Observers (from videotape) recorded the percentage of the time the food was taken, which crab took the food first, how long it took to find it, and whether that crab retained control of the food. The time an individual needed to find the food was defined as the time starting at release from isolation until the point at which an individual crab began to consume the food item. The behavior of the second crab was also recorded. If it took some food away from the first crab, or if the first crab dropped it and the second crab took it, that time was recorded. If neither crab contacted or otherwise showed any interest in the food by the 30 min time limit, the trial was discarded from analysis of feeding interractions, but was analyzed for agonistic interactions. All three possible pairwise competitions between species were tested; C. sapidus v. C maenas (n = 13), C. sapidus v. H. sanguineus (n = 16 total; 5 discarded from feeding analysis), and C. maenas v. H. sanguineus (n = 11). Individuals of all three species were also tested alone in the aquarium with the food to obtain baseline data for each species. This was used to determine if and how the presence of another crab affects their speed and ability to encounter and consume the food item. Each species was also tested with an equal-sized conspecific, to determine whether responses change depending on the species of the competitor. Each crab was only used once. The first crab to both encounter and begin to consume the food was deemed the ‘‘winner’’ of the feeding competition, referred to as the first to feed, or FTF. The other crab, which did not find the food first, was dubbed for convenience the second to finish (STF), whether or not it actually consumed any of the food item. Agonistic interactions In some of the food competition experiments described above, the two crabs fought. We noted how often fights occurred between each pair of species, which crab initially attacked, and which crab ‘‘won’’ each fight. A ‘‘win’’ was defined as (1) gaining control of the food from a competitor, i.e., successfully stealing the food, displacing the

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feeding crab; (2) for crabs in control of the food, successfully repelling a displacement attempt by a competitor; or (3) in fights where food was not the immediate factor, forcing the other crab to withdraw or retreat, regardless of which crab instigated the conflict. Contests that ended ambiguously were analyzed separately. Contests that took place without any agonistic encounters between the crabs were not counted in this analysis, but were counted only in the feeding analysis. Defense against predators Intermolt crabs of each species were frozen in mid-late October. Following a similar procedure to Barshaw et al. (2003), the carapace shatter strength of each species was recorded using an InstronTM 1011 load cell. A 5 mm edge was attached to the cell and pressed against the center axis of the carapace of a thawed, previously frozen crab until failure; the load at the point where the carapace fractured was recorded by the cell. From each crab tested, a 1 cm · 1 cm segment of carapace was removed from along the fracture line, air-dried, weighed, and its thickness measured with digital calipers. The thickness was also measured for a sample of carapace taken from the side of the right claw. For both samples, the average of four separate thickness measurements was recorded. Statistical analysis Feeding competitions The first comparison was the proportion of each species that found the food during the trials. These data were analyzed with Chi Square tests. The likelihood of each species to find the food was also compared separately between solo trials and trials with a conspecific competitor by means of Fisher’s Exact Tests. The times for individuals that successfully encountered the food were compared using one-way ANOVA followed by Tukey’s pairwise comparison tests. The success rate of each species in consuming some of the food even if they were not the first to encounter it


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The mean number of separate agonistic encounters per contest, the mean number of victories and the mean number of encounters that were instigated by each species were each compared with 2way ANOVA (wins, instigations, or victories by species and contest type) followed by Tukey tests. The mean percentage of interactions per contest that were won, lost or tied for each species were compared using the non-parametric Kruskal– Wallis one way ANOVA.

taking an average of 5.99 min. C. maenas found the food 100% of the time (13 trials), taking an average of 1.19 min, in both cases slightly shorter than their solo times. H. sanguineus found the food 100% of the time (7 trials) taking an average of 10.55 min, a slight increase from the solo time recorded for this species. For all three species, the difference in the time it took to find the food was not significantly different versus conspecific competitors than it was in the solo trials. Neither C. sapidus nor C. maenas was more likely to find the food when they were alone or with a conspecific; H. sanguineus, however, was more likely to find the food with a conspecific competitor than alone (Fisher’s exact test, P £ 0.026).

Defense against predators

Interspecific trials

The ratios of the carapace breaking strength, shell thickness, and claw shell thickness to the carapace width of the crab for each species were separately compared by one-way ANOVA. The ratio of breaking strength to carapace width and the relative rate of increase in breaking strength as a function of carapace width were also analyzed for each species by linear regression.

There was a significant difference in total number of contests won between all three species, with C. maenas winning most often (v2 = 10.406, df = 2, P £ 0.002, n = 35 13 contests of C. maenas v. C. sapidus, 11 contests of C. sapidus v. H. sanguineus 11 contests of C. maenas vs. H. sanguineus) (Fig. 2). C. maenas was significantly more likely to consume the food item first than either C. sapidus (Fisher’s exact test with Bonferroni correction, P £ 0.001) or H. sanguineus (Fisher’s exact test with Bonferroni correction, P £ 0.001). There were no differences between C. sapidus and H. sanguineus, either over all or in a contest specifically between those species (n = 11). C. sapidus did win a greater share of contests against H. sanguineus than against C. maenas, but the difference was not quite significant (Fisher’s exact test, P £ 0.08) In terms of the overall outcome of the contests, no species was able to prevent a competitor from eating some of the food more than any others (Fig. 2). The results of interspecific contests were not significantly different from contests between conspecific individuals as described above. Crabs that encountered the food first (FTFs) were much more likely to eat something during the contest. With the exception of C. maenas, crabs that were not first to finish were less likely to eat anything at all. Those C. maenas that were second to finish, including those in intraspecific trials, were more likely to eat some of the food

was compared using Chi Square tests. In all cases, Bonferroni corrections were used as necessary. Agonistic encounters

Results Feeding trials Solo trials C. maenas was significantly more likely to encounter the food within the trial time (30 minutes) than either C. sapidus or H. sanguineus (v2 = 15.56, P £ 0.001, n = 26 C. sapidus, 36 C. maenas, 20 H. sanguineus) (Fig. 1a). C. maenas also found and consumed the food item significantly faster than either C. sapidus or H. sanguineus under all experimental circumstances (1 way ANOVA, F = 17.135, P £ 0.001) (Fig. 1b). There was no significant difference in the time required to find the food between solo and competition trials. Intraspecific trials When competing against a conspecific, C. sapidus found the food 57% of the time (4 of 7 trials),

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Fig. 1 Trials against each opponent. The x axis refers to the opponent; Cs = C. sapidus, Cm = C. maenas, and Hs = H. sanguineus. ‘‘None’’ = solo trials. Dark bars = C. sapidus, Checked bars = C. maenas, and light bars = H. sanguineus. Letters indicate significant differences between species, but not between individual trial types for each species. Error bars = 1 SE. (A) Percentage of trials in which food was located by individuals of each species. Percentages indicate that in many cases the food item was not located. (B) Mean time, in seconds, required for each species to locate the food item against each different opponent

item than either second place C. sapidus or H. sanguineus (v2 = 7.00, df = 2, P £ 0.05, n = 56 20 C. sapidus, 16 C. maenas, and 20 H. sanguineus. Follow up tests: Fisher’s exact test with Bonferroni correction P £ 0.02, P £ 0.03 for C. maenas compared to C. sapidus and C. maenas compared to H. sanguineus respectively) (Fig. 2).

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Effect of size Size had no significant effect on either the time to find the food or the outcome of a contest. There was no significant correlation between crab size and the time required to find the food under any circumstances. For instance, in solo trials of


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Fig. 2 Percentage of trials where each species found and ate the food first, before the competitor) (grey bars); successfully consumed any part of the food (dark bars); or did not find the food item first, but still consumed some of it (light bars). Letters and numbers indicate significant differences between groups for each condition indicated

C. sapidus, there was little correlation of mass to encounter time (r2 = 0.012); for solo trials of C. maenas, (r2 = 0.027); and for solo trials of H. sanguineus (r2 = 0.194). Similarly, for solo trials, the size of crabs that did find the food item was not significantly different from crabs that did not: C sapidus, 2 sample T-test, P £ 0.31), H. sanguineus, (2 sample T-test, P £ 0.12). C. maenas almost always found the food or won the contest, so there was no basis for comparison. Agonistic interactions In 191 separate instances during 40 total interspecific feeding trials, the crabs fought. C. sapidus fought C. maenas 88 times during 13 trials; C sapidus fought H. sanguineus 65 times over 16 trials; and C. maenas fought H. sanguineus 38 times during 11 trials. Of those encounters, H. sanguineus was significantly more likely to be the instigator than C. maenas no matter the opponent, (Kruskal Wallis one-way ANOVA, K–W statistic = 10.42, P £ 0.005). C. sapidus did not instigate significantly more or fewer agonistic encounters, regardless of opponent, than either of the other two species. However, C. sapidus lost a significantly higher percentage of fights overall, regardless of opponent than either C. maenas or H. sanguineus (Kruskal Wallis one way ANOVA, K–W statistic = 17.859, P £ 0.0001) (Fig. 3). Within all three types of interspecific contests performed, the greatest number of fights was won

by C. maenas over C. sapidus (two-way ANOVA, F = 5.486, P £ 0.02, Tukey’s test, P £ 0.001). There was no significant difference in the total mean number of fights observed with any particular combination of crabs; no pairing led to more agonistic encounters than any other, including trials with conspecifics. There was also no significant correlation between starting fights and being first to find and consume the food item, or between starting fights and eating at all, either first or second, during the contest. There was likewise no significant correlation between winning fights and eating in the contests—crabs that won fights were no more likely to eat some of the food than those that lost.

Defense against predators C. sapidus (n = 15) had the lowest carapace breaking strength/carapace width, with a mean breaking strength of 0.104 kg/mm carapace. C. maenas (n = 25) have the next strongest shells relative to size, with a mean of 0.230 kg/mm carapace, while H. sanguineus (n = 18) has the strongest shells relative to size with a breaking strength of 0.265 lbs/mm carapace. The breaking strength of C. sapidus was significantly weaker than the other two (one-way ANOVA, F = 27.74, P £ 0.0001). For all three species, increase in carapace width correlated to an increase in breaking strength (Fig. 4).

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Fig. 3 Mean percentage of fights instigated won per contest by each species. Some fights (not shown) ended without a clear winner- there were no significant differences in the proportion of ties between contests. Error bars represent ± 1 SE. Letters indicate significant differences between groups

H. sanguineus had the thickest shells relative to crab size at 0.015 mm thickness/mm carapace width (CW) for the carapace and 0.018 mm/mm CW for the claw. C. maenas had the next thickest carapace and claws at 0.008 and 0.009 mm/mm CW respectively. C. sapidus had the thinnest shells at 0.006 mm/mm CW for the carapace and 0.005 mm/mm CW for the claw. The difference was significant between all species (one-way ANOVA, F = 122.52 carapace, 173.41 claw; P £ 0.0001, df = 2, n = 51). However, except for C. sapidus, the thickness of the carapace was not a

good predictor for its strength. The correlation of carapace thickness with breaking strength for C. sapidus was R2 = 0.578; for C. maenas, 0.188; and for H. sanguineus, 0.313.

Fig. 4 Relationship between breaking strength (kg) and carapace width (mm) for H. sanguineus (triangles), C. maenas (squares), and C. sapidus (open circles). The slopes of the regression lines are y = 0.528, (R2 = .551, P £ 0003),

y = 0.382 (R2 = .442, P £ 0001) and y = 0.169 (R2 = 0.5682, P £ 0.0007) for H. sanguineus, C. maenas, and C. sapidus, respectively. Error bars represent the 5% error term of the InstronTM load cell

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Discussion In feeding trials, C. maenas was the fastest to find and consume the food out of the three species under all experimental conditions. H. sanguineus by itself was the slowest to find the food and


frequently did not find it at all when alone. In interspecific competitions, C. maenas out-competed both C sapidus and H. sanguineus. This is in slight contrast to the study of DeGraaf and Tyrrell (2004), in which the feeding rates of shore crabs were found to be higher than green crabs on intact blue mussels (Mytilus edulis). However, their experiment did not include direct competition of individuals of each species. Jensen et al. (2002) found that on the western coast of the US, C. maenas lost to H. sanguineus in competition for food. This is different from our findings. Some differences were that the bivalves (Mytilus or Tapes) used in their study were a different species than the ribbed mussels, Geukensia demissa, used in this study. In addition, their trials were performed in the dark, while ours were in dim light. Regarding agonism, the relative lack of feeding success in C. sapidus compared to the frequency of agonistic encounters is similar to a situation observed by Clark et al. (1999), who determined that in C. sapidus, as aggressive encounters increased, the rate of feeding decreased. That same study found that increased periods of agonism and feeding activity overlap, so C. sapidus is most likely to be involved in agonism at the time when it is most likely to be feeding, and our results suggest that in interspecifc agonistic encounters C. sapidus is at a disadvantage. Furthermore, in many trials, the C. sapidus went into an aggressive display with its claws out while the other species found the food. Since C. maenas eat at a high rate with or without agonism, they may increase their feeding success at the expense of C. sapidus. The finding that crabs that won fights did not necessarily find and consume the food item first, or even at all, suggests that the most proficient fighters are not automatically the most proficient foragers. This finding is surprising, especially for H. sanguineus, which won the highest percentage of its fights yet was successful only about half the time in consuming some of the food item. In terms of percentage of fights instigated, H. sanguineus was the most aggressive species, which in previous studies, as in this one, correlates to a greater likelihood of prevailing in a conflict (Huntingford et al. 1995). This aggressiveness,

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however, did not translate into feeding success in this experiment. C. maenas, on the other hand, usually found the food first and its fighting skills were mostly tested in defense of its meal. These results also suggest that C. maenas may be somewhat more persistent in obtaining food even when a competitor is there first. Virtually all C. maenas succeeded in feeding in some way during the contests; of those who did not find the food item first outright, almost 90% were still able to wrest or steal it from the competitor that found it first. In areas of scarcity, C. maenas may therefore have an advantage, or at least reduce the food available to juvenile C. sapidus, which were not as successful in defending their find. H. sanguineus were not significantly more successful than C. sapidus in feeding when they were not first to encounter the item. C. sapidus, for their part, are active, highly mobile predators capable of pursuing highly mobile prey, and engage in routine agonistic encounters with equally agile, aggressive conspecifics. The shape of C. sapidus chelae suggests tradeoffs in favor of claw speed at the expense of crushing force (Schenk and Wainwright 2001), an advantage in a fast moving fight but less so against a durable opponent. According to Sneddon et al. (2000), C. maenas up to 80 mm in width were capable of generating up to 15.2 kg of force, enough to crush all but the largest juvenile C. sapidus and essentially any H. sanguineus. Further, C. maenas were able to generate enough force to crush gastropod shells from both crusher and cutter chelipeds, giving them extremely formidable weaponry (Preston et al. 1996). Until adult sizes, where C. sapidus grow far larger, C. maenas is likely to maintain this advantage in direct interactions. In the study on defense against predators, our results support the findings of Barshaw et al. (2003) on lobsters: crustaceans are protected better by having thick shells than by having spines or more effective offensive weapons (claws). The relative strength of the shells in conjunction with the strategies employed by each species may explain the outcomes of any agonistic encounters. C. sapidus always attacked its opponents (of either species) claws first, typically attempting to pinch or grab opponents. C. maenas

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tended to merely turn its back on its attacker, presenting its strong carapace, which was more difficult for these opponents to injure. Consequently, C. maenas was able to merely wait out opponents when they had food, continuing to eat it while opponents launched unsuccessful attacks on their backs. When a C. maenas attacked another C. maenas, instead of pinching, it tended to clamber upon the first crab, reaching directly for the food, and in most cases was able to steal part of the meal. H. sanguineus used formidable claws, and had the strongest carapace strength for its size of the three species. This disadvantage for C. sapidus relative to these other crabs in terms of carapace strength is not likely to be alleviated until adult status is reached, given steeper slopes of the strength/size regression line for the two invasives compared to the slope for C. sapidus. H. sanguineus at its maximum size, reported at 43.9 mm (McDermott 1998), would have a breaking strength of approximately 14 kg. According to this curve, it would take a C. maenas with approximately a 55 mm carapace to have the same breaking strength. It would take a C. sapidus with a carapace width closer to 85 mm, almost twice as large as the H. sanguineus and almost 35% larger than the C. maenas to achieve the same breaking strength. Only an adult C. sapidus would have a clear advantage in an agonistic encounter with large Hemigrapsus or medium juvenile C. maenas. The finding that the thickness of the carapace did not correlate well with the strength of the carapace, except in C. sapidus, was an unexpected result. Clearly, more is involved in carapace strength than just shell thickness. Properties of the carapace such as elasticity, shape, spikes or other surface projections, etc., may all affect overall strength of the carapace without affecting overall thickness. One of the most common predators of juvenile crustaceans is adult C. sapidus, which consume not only bivalves but juvenile conspecifics, fiddler crabs, and any other prey they can catch (Laughlin 1982). When feeding on motile prey such as crustaceans, C. sapidus tries to grasp crustacean prey and maintain its grip for as long as necessary until the prey can be consumed (Seed and Hughes 1997). Adult C. sapidus have been observed to

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discard bivalve prey that are too strong to quickly break open (Seed and Hughes 1997). In this case, the relatively strong carapace of C. maenas and H. sanguineus may discourage predator persistence and reduce predation risk. It cannot be determined from this experiment if increased carapace strength directly increases resistance to predation; however a stronger carapace may reduce damage during agonistic encounters and provide resistance to smaller predators (large predators can easily crush a carapace). In tethering experiments at a site where all three species are found (unpublished) we found that C. sapidus were far more likely to be taken than either of the other two species. Overall, H. sanguineus and C. maenas are potentially strong juvenile competitors with C. sapidus in the eastern U.S. Of the two, C. maenas is the more obvious and likely more serious competitor, growing to larger sizes and being a stronger competitor for sessile prey. H. sanguineus and C. sapidus of equivalent size are fairly evenly matched, and given the limited overlap between the two species, competition with H. sanguineus is unlikely to have a large impact on C. sapidus. H. sanguineus is, however, a strong competitor with C. maenas, effectively displacing them from rocky areas in some locations probably due to rapid reproduction (Lohrer and Whitlatch 2002b). So, if C. maenas is a competitor with C. sapidus, the introduction of H. sanguineus may actually benefit C. sapidus populations in areas where all three species overlap. However, increased predator density seems to decrease foraging success in C. sapidus (Clark et al. 2000). Since all three species are known to consume bivalves, the mere presence of the exotics, especially if they are in the same feeding patches, may adversely impact C. sapidus. That said, as the range of C. maenas has spread south into the heart of C. sapidus’ native range, its rate of expansion has slowed. Studies across a latitudinal gradient have shown that C. maenas is generally not successful at depths and locations where C. sapidus is most abundant, nor have they spread into the Chesapeake Bay where C. sapidus is especially abundant, suggesting that C. sapidus is able to limit the spread of C. maenas (DeRivera et al. 2005). While juveniles may be behaviorally


disadvantaged compared to C. maenas, adult C. sapidus are formidable enough predators to overcome any juvenile disadvantages. Despite sporadic over-fishing, C. sapidus populations are still robust enough to place severe predation pressure on C. maenas, and maybe H. sanguineus as well. The displacement of C. maenas by H. sanguineus in rocky shores and jetties may also have had the effect of forcing C. maenas into areas where they are more vulnerable to predation by adult C. sapidus, but also more likely to compete with juveniles. In many areas where C. sapidus is less abundant, however, C. maenas (and H. sanguineus) are well established, and can impact C. sapidus populations on the periphery of its range, with the potential for local ecological and economic consequences. In the natural environment, there is more space and alternate food sources available for juvenile C. sapidus, making it easier to avoid conflict. However, if C. maenas retain their superior ability to locate prey in the field, C. sapidus may have to expend more energy looking for an unoccupied prey item or risk conflict. C. maenas have exhibited a preference for smaller mussels during experiments (DeGraaf and Tyrrell 2004), as has C. sapidus (Micheli 1995), suggesting that both species may selectively seek out similar prey. This preference is likely to be even more prevalent among smaller individuals such as those tested in this study, which will be forced by anatomical constraints to seek out smaller prey. C. sapidus has, however, exhibited the ability to switch to a different size class of bivalve prey (Micheli 1995) suggesting that in the event of conflict with C. maenas they can avail themselves of less desired alternatives. In extreme cases, displaced individuals may be forced to forage for entirely different prey items, e.g. plant material or detritus, potentially stressing the animal. H. sanguineus demonstrated an ability to eat all size classes, making that species a factor but still less likely to be a competitor with C. sapidus (DeGraaf and Tyrrell 2004). C. maenas and, to a lesser extent, H. sanguineus can not be considered an immediate threat to C. sapidus, primarily because adult C. sapidus hold them in check. A severe drop in C. sapidus populations, however, (e.g., due to disease or over

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fishing), might allow C. maenas to spread into areas where they are currently limited. These juvenile competitors, particularly C. maenas, displayed the ability, at least in the laboratory, to locate a prey item first, successfully defend it once found, and wrest control of all or part of a food item from a C. sapidus, suggesting a real advantage in foraging ability in areas where juveniles of all three species are found. More study will be required in order to determine if these results hold true under field conditions. These results suggest that C. maenas are formidable juvenile competitors with C. sapidus and their presence has the potential to impact C. sapidus populations, at least where adults are scarce. H. sanguineus is comparable in competitive ability to C. sapidus, and would be expected to have lower rates of encounter with C. sapidus; therefore H. sanguineus is unlikely to have much direct impact on C. sapidus under normal conditions. Acknowledgements The authors would like to thank Jessica Reichmuth, Lauren Bergey, Celine Santiago Bass, and Eleni Kotsis for all their help. We also thank Dajun Zhang of Rutgers Engineering School and his lab for assistance with the load cell. We would also like to especially thank Paul Jivoff of Rider University for helpful advice and assistance in procuring crabs, Ken Able and Bobbie Zlotnick at RUMFS for logistical and funding support, and two anonymous reviewers for helpful comments on the manuscript. This work was supported by a grant from RUMFS- Tuckerton, N.J.

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