MARINE ECOLOGY PROGRESS SERIES Published January 12 Mar. Ecol. Prog. Ser.

Effects of limb autotomy and tethering on juvenile blue crab survival from cannibalism

L. David Smith

Smithsonian Environmental Research Center, PO Box 28, Edgewater, Maryland 21037, USA and Department of Zoology, University of Maryland, College Park, Maryland 20742, USA

ABSTRACT: High frequencies of limb loss (18 to 39 %) in blue crab Callinectes sapidus Rathbun popu- lations over broad temporal and spatial scales suggest that the autotomy response is an important escape mechanism. Limb loss, however, may increase vulnerability of prey in future encounters with predators If individual survival is reduced significantly and injury frequency in the population is density-dependent, such nonlethal injury could affect population size. Annual frequencies of limb loss were positively correlated to blue crab abundances in the Rhode River, Maryland, USA, between 1986 and 1989, but results of open-field tethering experiments indicated that, overall, missing limbs did not increase juvenile vulnerability to predators. Limitations imposed by the tether on normal escape behavior, however, may have masked real survival differences among limb-loss treatments To test for interactive effects of limb loss and tethering on survival from predation, I conducted a set of field experiments in 10 m2 enclosures, using adult blue crabs as predators and intact and injured (missing 1 or 4 limbs), tethered and untethered juvenile conspecifics as prey. A second experiment, conducted in small wading pools, tested the impact of limb loss on escape speed and direction of juvenile blue crabs. Results of enclosure experiments demonstrated that: (1) under typical field conditions and crab densities, larger c~nspec~csdo inflict lethal and nonlethal injury on juveniles; and (2) in encounters with predators, prior limb loss does not handicap crabs if escape is possible (untethered treatments), but does impose a defensive cost if escape is restricted (tethered treatments). In addition, survivorship patterns suggest that prey missing multiple limbs altered their activity patterns to decrease vulnera- bility In wading pools, limb loss altered escape speed and direction, although effects varied depending on the type and number of missing limbs. Together, these experiments indicate that prior limb loss can have complex effects on escape effectiveness, defensive ability, and anti-predator behavior. They also suggest that, despite density-dependence, prior limb loss does not reduce blue crab fitness sufficiently to regulate population size.

KEY WORDS: Autotomy - Nonlethal injury . Blue crab . CaJlinectes sapidus. Predation . Cannibalism Density-dependence . Escape response . Tethering Enclosures

INTRODUCTION Cooper 1986, Smith 1990a), hinder foraging ability (Smith & Hines 1991a), decrease reproductive output Autotomy, the self-amputation of a body part at a (Smyth 1974, Maiorana 1977, Dial & Fitzpatrick 1981, breakage plane (Wood & Wood 1932, McVean 1982), Smith 1992), and lower social status (Fox & Rotsker is thought to function principally as a mechanism for 1982). Furthermore, autotomy can leave an animal escape from predators (Vermeij 1982, 1987). Experi- more vulnerable in later encounters with predators mental work on lizards and salamanders has shown by impairing defensive capacity (Bildstein et al. 1989, that tail autotomy effectively distracts predators and Davenport et al. 1992), reducing escape effectiveness prevents subjugation of prey (Congdon et al. 1974, (Congdon et al. 1974, Ducey & Brodie 1983, Dial & Ducey & Brodie 1983, Dial & Fitzpatrick 1983, 1984). Fitzpatrick 1984, Vitt & Cooper 1986, Robinson et al. Nevertheless, for the individual, loss of an appendage 199 la, b), or adversely modifying behavior (Robinson can slow growth rate (Kuris & Mager 1975, Vitt & et al. 1991b).

1Inter-Research 1995 Resale of full article not permitted 66 Mar. Ecol, Prog Ser. 116: 65-74, 1995

Limb autotomy has the potential to affect not only most cases, intact juvenile blue crabs and those miss- individual fitness, but also population dynamics. Theo- ing 1 to 4 limbs had similar mortality rates (Smith retical models suggest that nonlethal injury could 1990b). Tethering, however, may have substantially regulate prey population size if: (1) injury rates were altered normal escape response in this highly mobile density-dependent, and (2) injury significantly reduced species (Zimmer-Faust et al. 1994) and masked real survival or reproduction (Harris 1989). This regulatory survivorship differences among autotomy treatments. effect requires close coupling between predator and By employing large field enclosures, I was able to prey abundances; such coupling is most likely to occur compare survivorship of tethered and untethered, in- if predator and prey are conspecifics. These models jured and intact juvenile blue crabs. These experi- have important implications for animal populations ments are among the first to examine: (1) the role of exhibiting autotomy, because intraspecific predation is cannibalism as an agent of nonlethal injury, and (2) common in many taxa (Fox 1975, Polis 1981, Stevens the effects of prior limb loss and tethering on prey et al. 1982, Kurihara & Okamoto 1987, Reaka 1987, survival using typical crab densities and natural field Kurihara et al. 1988, Spence & Carcam0 1991, Elgar conditions. & Crespi 1992) and injury frequency often correlates A second set of experiments was conducted in small positively with population density (Baker & Dixon wading pools to test the effect of limb loss on escape 1986, Petranka 1989, Robinson et al. 1991b, Smith & behavior. Juvenile blue crabs were subjected to a Hines 1991b, Van Buskirk & Smith 1991). number of limb-loss treatments and their escape speed High frequencies (18 to 39 %) of limb loss have been and direction of movement over a short distance were documented in blue crab Callinectes sapidus Rathbun measured. Results of these enclosure and escape (Portunidae) populations over broad temporal and response experiments, when compared to patterns of spatial scales (Smith & Hines 1991b), suggesting that autotomy observed in natural populations, elucidate the autotomy response is an important survival mecha- the role of autotomy as a survival mechanism and its nism in this species. Blue crabs are dominant predators potential for population regulation. in soft-bottom benthic communities in nearshore waters of the western Atlantic Ocean (Virnstein 1977, Holland et al. 1980, Hines et al. 1990) and are prey for a num- METHODS ber of fish and crustacean species (Millikan & Williams 1984, Shirley et al. 1990).If nonlethal injury regulates Study site and collection methods. I conducted en- population size in C. sapidus, direct and indirect closure experiments in an embayment of the Rhode effects on the community could be far-reaching. The River, Maryland (38' 51' N, 76' 32' W) in 1989 (Fig. 1). potential for density-dependent injury exists, because cannibalism is known to occur in this and in other crab species (Botsford & Wickham 1978, Hankin 1985, Kuri- hara & Okamoto 1987, Peery 1989, Lipcius & Van Engel 1990). Limb-loss patterns observed in juvenile blue crabs tethered in the open field were strikingly similar to those found in natural populations of C. sapidus from 1986 to 1989 (Smith 1990b, Smith & Hines 1991b) indicating that unsuccessful predatory attacks may be the primary cause of autotomy. Although several predatory species could potentially have been respon- sible for these injuries (e.g. Opsanus tau; Hines et d. 1990), larger conspecifics were the only predators I observed attacking and consuming tethered juveniles during these experiments (author's pers. obs.). Based on these findings, I conducted a set of experiments in 10 m2 field enclosures in the Rhode River, Maryland, USA, to test whether larger conspecifics were a source of lethal and nonlethal injury to juvenile blue crabs and whether missing limbs increased prey vulnera- bility to cannibalistic adults. Enclosure experiments were also designed to com- pare prey survival as a function of tethering. Results of Fig. 1. Rhode River subestuary, Maryland, USA, and site of open-field tethering experiments indicated that, in enclosure experiments in Canning House Bay Smith' Autotomy and cannibalism in blue crabs 67

The Rhode River is a shallow (maximum depth 4 m), before placing them in enclosures. Limb-loss treat- mesohaline (4 to 15%0)subestuary located on the west- ments consisted of: (1) intact crabs, (2) crabs missing ern side of central Chesapeake Bay (Hines et al. 1987). 1 cheliped, or (3) crabs missing both chelipeds, 1 walk- Bottom sediments were composed of muddy sand and ing leg, and the opposing ivimming leg. Half of the lacked submerged aquatic vegetation. Coarse woody small crabs were fitted with tethers. Tethering in- debris was the dominant structural component in volved looping monofilament fishing line between the shallow, nearshore waters (Everett & Ruiz 1993).Water crab's lateral spines and cinching the line to form a temperatures ranged from 26 to 32OC. Salinity was halter across the dorsal carapace. The knotted end of a unusually low (2 to 4%o)in 1989. I carried out tests of 1.2 m long nylon-coated, black steel leader was placed escape response in 1989 in small wading pools at the beneath the monofilament and both the steel leader Smithsonian Environmental Research Center, Edge- and monofilament were anchored to the dorsal cara- water, Maryland. pace using cyanoacrylate glue (Krazy GlueTM).I Intermolt blue crabs were collected for experiments attached the free end of the steel leader to a swivel at a fish weir, by seine, and by crab pots in shallow secured to the top of a 10 cm stake, which I later areas near the head of the Rhode River. Crabs were fed embedded into the bottom sediment. 1 or 2 fish (Brevoortia tyrannus) daily and held no I tethered 2 small crabs in each of 6 enclosures and longer than 3 d in floating cages anchored in shallow staked them so that both had access to the enclosure water. Crabs were starved 24 h prior to an experiment. walls, but neither crab could physically contact the Intraspecific predation experiments. Enclosure other. I introduced 2 untethered small crabs into each design: Experiments designed to test the effects of of the 6 remaining enclosures. Within any enclosure, limb loss and tethering on the survival of small blue both crabs had received the same autotomy treatment. crabs from larger conspecifics were conducted in I duplicated each treatment combination so that a enclosures. I constructed 12 adjoining 10 m2 (2.5x 4 m) single experiment consisted of 3 limb-loss treatments enclosures in water approximately 0.5 m deep (mean x 2 tethering conditions x 2 enclosures (= 12 enclo- low tide). The substrate within each enclosure was sures). Treatment combinations were randomized muddy sand lacking structural components. Enclosure among the 12 enclosures. sides were 1.2 m high, made of plastic mesh (1.27 cm Two hours after small crabs had been placed in the mesh VexarTM)held up by wooden poles, and lined enclosures, a single intact, large, intermolt male crab with 18 cm of galvanized wire mesh (1.27 cm mesh (mean CW  1 SD, 141.0  16.0 mm) was placed in each hardware cloth) along the bottom edge. I buried the of the 12 enclosures and left undisturbed for 48 h. hardware cloth 15 cm into the sediment to prevent Based on previous tethering experiments conducted in escape by crabs. I placed a small section (15 cm wide x the open field in the Rhode River and monitored at 1.2m high) of Vexar and hardware cloth in each corner 24 and 48 h, a 48 h period was deemed sufficient time to round the corners off and remove a potential refuge to see an effect from predation (Smith 1990b). At the for smaller crabs. Enclosures were oriented so that the end of 48 h, I removed large crabs and collected small long axis of each unit was parallel to shore. crabs or their remains. I repeated the experiment Preliminary experiments indicated that recovery of 8 times between 13 June and 22 July 1989. A new set untethered live crabs or shell fragments of eaten crabs of 36 crabs was used in each experiment. I checked would be difficult in murky water. To facilitate re- cages before and during each experiment for signs of covery, I attached a 45 cm length of floating fly line to damage (e.g. holes, undercutting of sides by waves) a short (7 cm) steel leader 'antennai rising off the and made necessary repairs. dorsal carapace of all experimental crabs. The part of Escape response experiments. I conducted experi- the floating line at the water surface marked the crab's ments to test for direction and speed of escape response location. The floating line nearest the crab, though, as a function of limb loss in wading pools (1m diameter was painted black so that the line would not be visible x 20 cm depth) filled with water from the Rhode River. to benthic predators. Observations showed that crab Water temperature was 28OC and salinity was 2%o movement and ability to bury were not hindered by during the experiments. To prevent a burial response by the floating line. Mean swimming speeds of intact the crabs, the bottom of the wading pool was kept bare juvenile blue crabs (mean CW  1 SD, 53.9  13.8 mm) of sediment. Juvenile intermolt crabs (mean CW  1 SD, with and without floating lines were not significantly 45.8  12.1 mm) were used. I randomly applied 8 limb- different (t=1.24, df = 18, p = 0.23). loss treatments (Table 1) to crabs and caused limbs to Experimental design: I subjected small, intermolt autotomize 24 h before an experiment. crabs between 41 and 72 mm CW (mean  1 SD, In each experimental trial, I placed a crab under- 54.1  7.2 mm) to 1 of 3 limb-loss treatments and 1 of neath an opaque inverted container in the center of the 2 tethering conditions (tethered or untethered) 24 h pool and allowed it to settle for 30 s. The container top 68 Mar. Ecol. Prog. Ser. 116: 65-74, 1995

Table 1. Callmectes sapidus. Type and number of limbs re- expected 1:1 ratio. I performed all statistical analyses moved in autotomy treatments m escape trials in wading using Statistical Analysis Systems (SAS) software pools. INT. all limbs intact, R: right, L: left, CH* cheliped; (SAS Institute 1985). WL 1st walking leg; SL. swimming leg

Type Number n RESULTS INT 0 15 RCH 1 15 Intraspecific predation experiments LCH 1 15 RSL 1 10 Seventeen of 192 small crabs (9 %) and 6 of 96 (6%) LSL 1 10 large crabs used in the experiments were not re- RCH, RWL 2 10 covered and were excluded from analysis. Frequencies LCH, LWL 2 9 of missing crabs did not differ among experiments (G = RCH, LCH, RWL, LSL 4 11 8.2, df = 7, p > 0.10). Although missing crabs were not RCH, LCH, LWL, RSL 4 4 distributed evenly among enclosures or treatment combinations (G-tests, p < 0.05), sample sizes for all treatment combinations were sufficiently large for was perforated to eliminate suction when raised. After analysis. For combined treatment combinations, pre- 30 s, the container was raised and the crab was dation levels were significantly higher in the final allowed to move to the pool wall. I noted its direction of experiment than in the second or third experiments movement (right or left), and I recorded the time taken (STP tests, p < 0.01). No significant differences in to move 50 cm to the pool wall using a stopwatch. This mortality and injury were found among any other ex- technique measured mean rather than maximum periments. Survivorship was not affected by enclosure escape speed. I then recaptured the crab and repeated location (G= 16.8,df = 22, p = 0.77).Juvemle crabs did the process for a total of 6 trials per crab. If a crab failed not appear to be clustered at any particular location to move or moved only part of the way to the wall inside the enclosures; 1 recovered them in the center as (< 2 % of 588 trials), the trial was discounted. well as along the sides. Mean size of juvenile crabs Statistical analyses. The primary focus of the intra- did not differ among treatment combinations (2-way specific predation experiments was to determme how ANOVA, F = 0.25, df = 5, p = 0.94), experiments (F= limb loss and tethering affected survival and further 0.20, df = 7, p = 0.99), or treatment combinations across injury of juvenile blue crabs in the presence of larger experiments (treatment x experiment interaction, F = conspecifics. Data were treated as categorical, and I 1.16 , df = 35, p = 0.27). For combined treatments over used a logistic analysis (Cox & Snell 1989; PROC all experiments, surviving juveniles were significantly CATMOD with maximum likelihood estimate option, larger than those that were eaten (Wilcoxon 2-sample SAS Institute 1985) to determine whether limb-loss test, p = 0.021). treatment, tethering condition, or their mteraction The effect of limb loss on juvenile blue crab survival affected survival and injury. If a model showed a sig- was dependent on their tethering status (limb-loss nificant association between response and indepen- treatment x tether status interaction, G = 12.9, df = 2, dent variables, I used linear contrasts to make a priori p = 0.002).Among tethered crabs, intact specimens had comparisons (Day & Quinn 1989).Data for each combi- significantly higher survivorship than crabs missing nation of limb-loss treatment and tethering condition 1 cheliped, but did not differ from those missing 4 limbs were pooled for the 8 experiments. (Fig. 2, Table 2). In contrast, survivorship of untethered I used repeated measures procedures to test for auto- crabs did not differ among autotomy treatments (Fig. 2, tomy treatment differences in escape time (ANOVA) Table 2). Untethered crabs that had been subjected and escape direction (logistic regression). If escape to autotomy were twice as likely to survive as therr time differed significantly among treatments, mean tethered counterparts (Fig. 2, Table 2). In contrast, sur- individual escape times were compared using un- vival did not differ between untethered and tethered planned multiple comparisons (Ryan's Q-test; Day & intact crabs. For combined treatments over all experi- Quinn 1989). For these and other comparisons using ments (n = 163 juveniles), survival with additional limb ANOVA, group variances were tested to assure homo- autotomy (4 %) was rare compared to fatality (33%). Ad- geneity (Fmax-test)and residuals were examined for ditional limb loss (1 to 3 limbs) was observed for un- normality. Among-treatment differences in escape tethered individuals that were initially intact (n = 3 direction were compared usmg a simultaneous test crabs) or missing 4 limbs (n = 2 crabs) and for 1 tethered procedure (Sokal & Rohlf 1981). Within-treatment dif- individual missing 4 limbs. Large crabs used as preda- ferences in escape direction were tested against an tors did not lose limbs during the experiment. Smith: Autotomy and cannibalism in blue crabs -

100 -0 limbs those recorded for untethered juvenile blue crabs 0 -1 limbs when approached by larger conspecifics (Zimmer- 90 0 -4 limbs _1 Faust et al. 1994). 2* 80 The number and type of missing limbs had a signifi- > CC 70 cant effect on escape time among experimental crabs 3 (repeated-measures ANOVA for autotomy treatment; 60 I- F = 5.8, df = 8,90, p < 0.001). Individual escape times $ 50 varied significantly (F= 7.4, df = 5,450, p < 0.001) and (J 5 40 increased linearly (polynomial contrast; F = 21.7, df = n. < 30 1,90, p 0.001) over repeated trials. Time differences among individual runs were consistent across all auto- 20 TETHERED UNTETHERED tomy treatments (time x treatment interaction; F = 1.2, CONDITION df = 40,450, p = 0.26). Mean escape times per indi- vidual were used to make comparisons among limb- Fig. 2. Callinectes sapidus Percent survival of blue crabs in loss treatments. Treatments that differed only by side enclosure experiments for 3 autotomy treatments (-0, -1, e.g. right vs left cheliped) did not differ in escape -4 limbs) and 2 tethering conditions (tethered, untethered). Sample sizes for each limb-loss treatment x tethering condi- times (F= 0.43, df = 1,90,p = 0.52); hence, these were tion combination are presented above each bar combined for subsequent comparisons. Escape times did not differ between intact crabs and those missing Nearly equal proportions of male and female juve- either 1 cheliped or 4 limbs (Fig. 3). These 3 treatment nile crabs occurred in all treatment combinations groups showed significantly faster movement than permitting a posteriori testing for sex-related survival crabs missing either a single swimming leg or a differences in encounters with predators. Survival was cheliped and adjacent walking leg. independent of sex for all limb-loss treatments (2-way The direction of movement (right vs left) during an logistic regressions, x2 = 0.47, df = 1, p = 0.49) and escape was not consistent among limb-loss treatments tether conditions (y2= 0.01, df = 1, p = 0.94). (repeated measures logistic analysis: treatment x direc- tion interaction, G = 58.3, df = 35, p = 0.008). Crabs missing both chelipeds, a right first walking and left Escape response experiments swimming leg moved to the left in 70 % of the trials; while their counterparts (i.e. crabs missing both che- Although no natural predators were used to provoke lipeds, a left first walking and right swimming leg) a swimming response in these experiments, my obser- moved to the right in 67 % of the trials (Table 3). vations and comparative data indicate that juvenile Escape direction between other treatment pairs m blue crabs were swimming in escape. Mean swimming speeds (22 cm stfor mtact juveniles) measured over short distances in my experiments were similar to

Table 2. Callmectes sapidus. Linear contrasts comparing sur- vival in enclosure experiments between intact (-0) crabs and treatments missing 1 (-1) or 4 (-4) limbs for tethered and untethered conditions, and intact (-0) or injured (-1 & -4) tethered (T) and untethered (U) crabs. Survival: directionality of survival ns: no difference by sequential Bonferrom test (Rice 1989) where experiment-wise a = 0.05

Contrast df x2 p Survival 1SL CHWL 2CH 1CH INT Tethered WLSL -0 vs -1 1 6.3 0.01 -0 >-1 AUTOTOMY TREATMENT -0 vs -4 1 2.1 0.15 ns Fig. 3. Callmectes sapidus. Mean escape times (Â 1 SE) of blue Untethered crabs subjected to different limb-loss treatments Treatments -0 vs -1 1 2.0 0.16 ns that differed only by side were pooled for presentation. 1SL: -0 vs -4 1 4.1 0.04 ns missing one swimming leg; CHWL: missing cheliped and Tethered vs untethered adjacent 1st walking leg; 2CHWLSL: missing both chelipeds, -0 1 0.8 0.79 ns 1st walking and opposing swimming leg; 1CH. missing one (-1 & -4) 1 12.8 0.001 T < U cheliped; INT: all limbs intact. Means with the same super- script are not significantly different (Ryan's Q-test, p > 0.05) 7 0 Mar. Ecol. Prog. Ser. 116: 65-74, 1995

Table 3. Callmectes sapidus. Frequencies of right and left injury is strongly suggested by the positive correlation escape movements summed for individual trials are com- (r = 0.99, p < 0.05) between annual frequencies of limb pared among and within hmb-autotomy treatments. Among loss and blue crab abundances in the Rhode River from treatments, those with the same superscripted letter do not differ in their direction of movement (STP test, 8 df, p > 0.05). 1986 to 1989 (Smith & Hines 1991b). Within treatments, L:R (%left:% right) is tested against expected pattern of random (50:50) directional movement (G-tests, 1 df). See Table 1 for limb loss codes Autotomy and antipredator responses

Limb loss Escape direction L.R G p The evolution of an autotomy response in diverse Left Right marine taxa (e.g. polychaetes, echinoderms, crusta- INT 41 49 46.54 2.0 > 0 1 ceans) suggests its importance in preventing sub- RCH a 41 49 4654 2.0 > 0.1 jugation by predators (Vermeij 1982, Endler 1986). LCH~~ 54 36 60:40 3.6 > 0.05 Unexpected patterns of blue crab survivorship in RSL-~ 32 28 53-47 0.3 > 0.5 my experiments, however, suggest potentially complex LSLah 35 25 58:42 1.7 > 0 1 RCH, RWL"' 30 30 50:50 0.0 > 0 99 effects of limb loss on future escape effectiveness, LCH, LWLa 25 29 46.54 0.3 > 0.5 defensive ability, and activity levels of decapod crusta- RCH, LCH, RWL, LSLb 46 20 70.30 10 5 < 0 005 cean prey. Following detection and approach by a RCH, LCH, LWL, RSLa 8 16 33:67 2.7 > 0.05 predator, the most effective antipredator mechanism for juvenile crabs is escape or, if captured, autotomy followed by escape (e.g. 5 of 6 instances of autotomy which opposing limb types were removed did not dif- in enclosures occurred among untethered individuals; fer (STP test, df = 8, p > 0.05). Escape direction devi- see also Lawton 1989, Davenport et al. 1992). Tether- ated significantly from an expected random pattern ing limits escape effectiveness (Zimmer-Faust et al. only for crabs missing both chelipeds, a right first 1994) and should force prey either to actively defend walking, and left swimming leg (p < 0.005). A similar themselves or reduce their activity to avoid detection. trend was observed for the matched treatment missing In field enclosures, intact juveniles were able to defend both chelipeds, a left first walking, and right swimming themselves to such a degree that survival rates among leg (0.05 < p < 0.01), but the sample size was too small tethered and untethered intact crabs did not differ to detect a difference. (Fig. 2, Table 2). In contrast, tethered juveniles missing 1 or both chelipeds experienced significantly higher mortality than their untethered counterparts (Table 2). DISCUSSION These results suggest a defensive cost to autotomy if escape is restricted and illustrate the importance of Cannibalism and autotomy escape for injured juvenile blue crabs. Under natural conditions, such restrictions are probably rare; how- Enclosure experiments demonstrated that cannibal- ever, defensive weaknesses will prove detrimental ism is a source of mortality and limb autotomy for whenever escape proves ineffective (e.g. the predator juvenile blue crabs. These results are particularly is adept at pursuit) and injured prey are being sub- meaningful, because experiments were conducted dued. over a relatively large area (10 m2),used realistic den- Prey will modify their activity in proportion to the sities for the Rhode River (0.3 crabs m2;Hines et al. risk of predation (Sih 1980, 1982, Lima & Dill 1990). In 1990), and occurred under ambient field conditions. the presence of cannibalistic adults, smaller, more Together with gut analyses (Laughlin 1982, Hines et vulnerable backswimmers Notonecta hoffmanni re- al. 1990), population dynamics models (Lipcius & Van duced their movements and increased their use of sub- Engel 1990), open-field tethering (Smith 1990b, Ruiz optimal edge space to a greater degree than larger, et al. 1993) and aquarium experiments (Peery 1989), less vulnerable instars (Sih 1982). Similar behavioral these data indicate that cannibalism is common in modifications in blue crabs missing 4 limbs could Callinectes sapidus populations. Larger conspecifics explain: (1) the lack of difference in survival rates are likely the chief agents of death and injury for juve- between multiply injured and intact crabs in tethered nile blue crabs in the Rhode River subestuary, because: treatments (Fig. 2, Table 2), and (2) a tendency towards (1) abundances of other potential predator species in higher survivorship in multiply injured versus intact the Rhode River are low (Hines et al. 1987, 1990, Ruiz crabs in untethered treatments (Fig. 2, Table 2). For et al. 1993); and (2) other sources of injury (e.g. intra- tethered crabs missing 4 limbs, not only was escape specific competitors, fisheries) are unimportant in this hindered by the tether, but the absence of both che- size class (Smith & Hines 1991b). Density-dependent lipeds precluded any defensive posture. While re- Smith: Autotomy and cannibalism in blue crabs 7 1

duced activity could increase the chances of surviving 1990a, Smith & Hines 1991b) did not increase blue until limbs regenerate, such behavior might also de- crab vulnerability to predation in either enclosure crease feeding rates or mating success (Sih 1982, 1992, (untethered treatments) or open-field tethering exper- Dong & Polls 1992). iments (Smith 1990b) and had no observable effect on Any reduction in speed (Punzo 1982, Daniels 1985, escape speed or direction. In addition, single cheliped Robinson et al. 1991a) or evasiveness due to missing loss had no effect on size increase at the molt or inter- limbs could be detrimental for crabs that rely primarily molt duration (Smith 1990a) or on foraging rate on an on escape. In escape response experiments, asym- important bivalve prey species (Smith & Hines 1991a). metrical injuries involving loss of a single swimming In terms of reproductive success, cheliped loss in male leg or a cheliped and walking leg from the same side blue crabs adversely affected competition for mates in slowed swimming speed by ca 36% compared with experimental arenas (Smith 1992),but in natural popu- intact controls (Fig. 3). In contrast, single cheliped lations male body size was a greater determinant of autotomy had no effect on escape time. The latter out- success (Smith unpubl. data). Autotomy of a single come might be expected, because unlike swimming limb is unlikely to affect fecundity in female blue and walking legs, chelipeds provide little, if any, crabs. Energetic tradeoffs between reproductive out- propulsive power (Spirito 1972). Removal of 4 limbs put and regeneration found in chordate taxa (Smyth did not diminish escape speed relative to intact crabs. 1974, Maiorana 1977, Dial & Fitzpatrick 1981) should This surprising result may be due to the symmetry of be absent in blue crabs, because sexually mature the injury (2 limbs per side) and substantial loss of females cannot regenerate limbs (Millikin & Williams mass (ca 20% of total wet weight; Smith 1990a) that 1984). Severe multiple autotomy (-4 limbs) is costly to allowed these individuals to maintain normal swim- individuals in terms of reduced growth (Smith 1990a), ming speed. The direction of escape movement for foraging ability (Smith & Hmes 1991a),and, for certain crabs missing 4 limbs, however, became less random sizes, predator avoidance (Smith 1990b),but injuries of (Table 3). These individuals tended to be propelled by this magnitude are rare (< 1 % of the Rhode River pop- the remaining swimming leg in the direction of the ulation; Smith & Hines 1991b). missing swimming leg. Random directional movement Sacrifice of 1 or 2 limbs appears to be an effective by escaping prey can reduce predator capture effi- survival strategy for highly mobile, non-territorial ciency (Schall & Pianka 1980);conversely, more consis- decapods such as blue crabs. Costs of limb loss to tent movement might expose injured crabs to greater survival and reproduction, however, undoubtedly vary risk of capture. I did not, however, observe increased among species. For species that must defend a burrow, mortality for juveniles missing 4 limbs in enclosure cheliped loss could result in eviction by conspecifics experiments. In the turbid conditions of the Rhode (Conover & Miller 1978, O'Neill & Cobb 1979) or River, visual acuity is sufficiently limited that reduced greater vulnerability to attack by predators (Bildstein escape speed and consistent directional escape re- et al. 1989). Autotomy could reduce reproductive out- sponses by injured crabs may not be extremely costly. put in species that are able to molt and regenerate missing limbs following their molt to maturity (e.g. cancrid crabs). Autotomy as a regulatory mechanism

While density-dependent intraspecific predation can Effects of tethering and enclosures on prey survival potentially regulate population size in many brachyu- rans (e.g. Kurihara & Okamoto 1987, Lipcius & Van Tethering has been employed in marine (e.g.Heck & Engel 1990),the regulatory effect of nonlethal injury is Thoman 1981, Aronson 1987, Wilson et al. 1990, Ruiz uncertain. Using models, Harris (1989) demonstrated et al. 1993) and terrestrial (Belovsky et al. 1990) that nonlethal injury could regulate population size if systems to assess the potential for predation among injury rates were density-dependent, and injury sig- different habitats, latitudes, and species. While tether- nificantly reduced survival or reproduction. The ing is a useful technique for exposing prey to a suite of dynamics of limb loss in Callinectes sapidus popula- predators in a natural environment, few studies have tions meet the first of Harris's model criteria (density- tested for differential effects tethering might have on dependent injury), but not the second. This study and experimental treatments (see review by Peterson & other experiments (Smith 1990a, b, Smith & Hines Black 1994). My enclosure experiments are the first to 1991a, b) indicate that costs of injury to long-term test for such interactions under field conditions, and survival or reproduction are insufficient to regulate results indicate that the technique should be applied population size. The most common form of injury in judiciously. As expected, tethering generally decreased blue crab populations (single cheliped loss; Smith survival of juvenile blue crabs relative to untethered 72 Mar, Ecol. Prog. Ser. 116-65-74, 1995

individuals. Zimmer-Faust et al. (1994) have shown Separation distances of 20 cm are sufficient for juvenile that, while tethers have no significant effect on mean blue crabs to evade larger conspecifics (Zimmer-Faust or maximum escape speeds in juvenile blue crabs, they et aL 1994); thus, my enclosures provided ample room do shorten the distance travelled during each swim- for escape even if encounter rates increased. Signifi- ming burst so that tethered prey are subject to cantly, my results demonstrated that limb loss does not repeated attack. Survivorship patterns in my enclo- dramatically increase mortality from predators if prey sures illuminated injury-dependent behavioral and have an opportunity to escape. Furthermore, low defensive differences in juvenile blue crabs. They incidences of autotomy and high survivorship of illustrate the importance of maintaining uniform untethered crabs (86%) suggest that while con- physical condition of tethered prey lest interpretation specifics do inflict nonlethal injury, the autotomy for other variables be confounded. The degree of response is used infrequently when compared to other handicap tethering imposes on prey also can depend escape mechanisms. on the type of habitat (Barshaw & Abele 1990), preda- tor type (Peterson & Black 1994), and body size (Smith 1990b, Ruiz et al. 1993) and escape mode (Zimmer- Acknowledgements. I extend my sincere appreciation to Dr A. H Hines for his logistical support and advice throughout Faust et al. 1994) of prey. the project I thank M Groom, D. Lello, M. Poteet, T. Steel- As with tethering, enclosures can potentially affect man, A Twitchell, L. Wiechert and other members of the experimental treatments unequally. In all likelihood, crablab' for their assistance in the field The manuscript was enclosure walls provided a structural refuge for juve- greatly unproved by critical comments from Dr D. Allan, Dr nile crabs. Injured free-swimming crabs may have uti- J. Dineen, L Gosselin, Dr M. Raupp, T. Rawlings, Dr M Reaka, Dr E Russek-Cohen, Dr G. Vermeil, Dr C Peterson, lized cage walls to a greater degree than tethered 2 anonymous reviewers, and especially D. Lello This project crabs or untethered intact prey. For tethered prey, has been funded by a Smithsonian Predoctoral Fellowship encounter rates with predators and the chances of and the Department of Zoology's Chesapeake Bay Fund at being captured or killed were likely higher in enclo- the University of Maryland to L.D S. and grants to A. H. Hines from the Smithsonian Environmental Science Program, sures than in the open field. In enclosure experiments, Smithsonian Scholarly Studies Program, and National tethered prey were potentially subject to repeated Science Foundation OCE-8700414 and OCE-9000483. This attacks by the same predator over 48 h. In contrast, in paper was submitted in partial fulfillment of a Doctor of the open field, any one predator is more likely to Philosophy at the University of Maryland. search elsewhere after an unsuccessful attack. Where- as overall mortality for small tethered crabs was similar LITERATURE CITED between enclosure (48%) and open-field experiments (43%; Smith 1990b), the likelihood of death versus Aronson, R. B. (1987). Predation on fossil and Recent ophi- injury was much greater in enclosures (43 : 1) than in uroids. Paleobiology 13: 187-192 the open field (ca 3 : 1). Baker, R. L., Dixon, S. M. (1986). Wounding as an index of Despite the potential for higher-order interactions aggressive interactions in larval Zygoptera (Odonata) Can. J. 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This article waspresented by C. H. Peterson (Senior Editorial Manuscript first received: March 14, 1994 Advisor), Morehead City, N.Carolina, USA Revised version accepted. August 31, 1994