The impact of limb autotomy on mate competition in blue crabs Callinectes sapidus Rathbun

Summary This study is the first to demonstrate experimentally that autotomy (self-amputation of a body part) adversely affects competition for mates. Experiments were conducted using blue crabs Callinectes sapidus Rathbun to examine the consequences of limb loss and pairing precedence on mate acquisition by males. Two adult males of equivalent size were introduced sequentially into pools containing a sexually-receptive female and observed after 24 h and 48 h. One male in each pair was left intact, while the other experienced: (1) no autotomy, (2) autotomy of one cheliped, or (3) autotomy of both chelipeds, one walking leg, and one swimming leg. In the absence of a competitor (first 24 h), both intact and injured males established precopulatory embraces with females. Intact males were highly successful (84–95%) in defending females from intact or injured intruders in the second 24 h period. Both autotomy treatments, however, significantly reduced the ability of males to defend females from intact intruders. Females in experiments suffered greater frequency of limb loss than did males. In the field, paired blue crabs showed significantly higher incidence of limb loss than unpaired crabs. Limb loss frequency increases with body size, and field observations indicated that larger males may be more successful than smaller males in obtaining females. Both experimental manipulations and field studies provide strong evidence for mate competition in this ecologically and commercially important portunid species.     

Limb autotomy patterns in Paralithodes camtschaticus (Tilesius, 1815), an invasive crab, in the coastal Barents Sea

We examined levels of limb injury in the red king crab Paralithodes camtschaticus at 3 sites in the coastal waters of the Barents Sea. High incidences of autotomy were registered at all sites examined averaging 46.6% in Dolgaya Bay (DLB), 42.6% in Yarnyshnaya Bay (YRB) and 45.6% in Dalnezelenetskaya Bay (DZB). These levels were greater than in deep waters of the Barents Sea. Significant inter-annual increases in limb loss rates were observed in DZB. The positive correlation of autotomy frequency with the body size was observed for the females in YRB and DZB. The frequency of autotomy was independent of sex for all sites and size groups except for the crabs with CL > 135 mm in DZB where the females had autotomized limbs more often than the males. The chance of injury was higher for posterior legs. Right-side limbs (especially, claws) were lost more often than left-side limbs. The observed frequency of crabs within limb loss patterns did not differ significantly from the expected levels in P. camtschaticus collected in DLB and in YRB but was significantly different than a frequency expected if limb losses were independent in DZB. Our results suggest that crabs in DZB are more affected by limb-inducing factors than individuals from DLB or YRB. The main factors affecting limb injuries in P. camtschaticus in the coastal Barents Sea are predator pressure (mainly for immature crabs), and illegal fishing and recreational diving (for mature crabs).     

Interruption of proecdysis by autotomy of partially regenerated limbs in the land crab, Gecarcinus lateralis

In the land crab, Gecarcinus lateralis, autotomy of partially regenerated limbs before a critical stage in the premolt period results in (1) a very rapid decrease in the serum ecdysone titer, (2) a delay in the growth of partial regenerates remaining on the animal, (3) a delay in the deposition of gastroliths, and (4) a delay in cytological changes in the epidermis. Serum ecdysone titers remain low while new limb regenerates form at the sites of those removed. Ecdysone titers rise when these secondary regenerates complete basal regeneration. Premolt events, which had ceased at the time of autotomy of the partial regenerates, resume their normal patterns of development when ecdysone titers reach the level present in the serum at the time of this interruption. We propose that the effect of autotomy before a critical period is to reinitiate a normal proecdysis. The same pattern of events occurs following autotomy of partial regenerates of crabs without eyestalks, suggesting that the decrease of serum ecdysones is brought about by some mechanism other than changes in the titer of the molt inhibitory hormone.     

Limb Loss and Regeneration in Two Grabs: The King Crab Paralithodes camtschatica and the Tanner Crab Chionoecetes bairdi

The incidence of limb loss and regeneration in two species of benthic Crustacea, the king crab Paralithodes camtschatica, an anomuran, and the tanner crab Chionoecoetes bairdi, a brachyuran, is surveyed in populations from the Bering Sea. 29.4 % of young juvenile P. camtschatica and 14.8 % of adults had lost at least one limb. The overall incidence of limb loss in C. bairdi was 38.8 %, with female adults less prone to damage than males and juveniles. Limb loss increases in frequency in more posterior limbs. Right hand limbs are lost more often than left in both species. This “right handedness” appears to be widespread in crabs and may be due to the greater vulnerability of leading limbs. The frequency distribution of limb regenerate lengths in a population of young juveniles suggests that at least four instars must be passed before limb symmetry is restored.     

Hair-trigger autotomy in porcelain crabs is a highly effective escape strategy

The benefits of autotomy, the voluntary shedding of limbs, havebeen adequately demonstrated in vertebrates but are poorlystudied in invertebrates. We provide strong experimental evidencefor an antipredatory benefit to autotomy in two porcelain crabs(Petrolisthes cinctipes and P. manimaculis). Since the outcomeof autotomy depends critically on the species of predator andprey involved, we first surveyed field populations of porcelaincrabs to identify ecologically relevant predators to use insubsequent experiments. We then examined the escape tacticsof the porcelain crabs in response to the four potential predatorswe identified, all larger predatory crabs. Cheliped autotomywas induced by three of the predator species (Cancer antennarius,Hemigrapsus nudus, Pachygrapsus crassipes); the fourth didnot attack porcelain crabs. Autotomy occurred in response to34% of all attacks, and in 67% of attacks in which the preywas held at some point by only the cheliped. Autotomy was ahighly effective escape mechanism against these predators;58 of 59 crabs that autotomized escaped, usually while thepredator stopped pursuit to eat the shed cheliped. Relianceon autotomy as a primary mechanism for escaping predators maybe particularly common in small crabs that cannot adequatelydefend themselves by other means and in suspension-feedingcrabs that do not need their chelipeds for feeding.     

Characterization of limb autotomy factor-proecdysis (LAF(pro)), isolated from limb regenerates,that suspends molting in the land crab Gecarcinus lateralis

Molting and limb regeneration are tightly coupled processes, both of which are regulated by ecdysteroid hormone synthesized and secreted by the Y-organs. Regeneration of lost appendages can affect the timing and duration of the proecdysial, or premolt, stage of the molt cycle. Autotomy of all eight walking legs induces precocious molts in various decapod crustacean species. In the land crab Gecarcinus lateralis, autotomy of a partially regenerated limb bud before a critical period during proecdysis (regeneration index <17) delays molting so that a secondary limb bud (2 degrees LB) forms and the animal molts with a complete set of walking legs. It is hypothesized that 2 degrees LBs secrete a factor, termed limb autotomy factor-proecdysis (LAF(pro)), that inhibits molting by suppressing the Y-organs from secreting ecdysone. Molting was induced by autotomy of eight walking legs; autotomy of primary (1 degrees ) LBs reduced the level of ecdysteroid hormone in the hemolymph 73% by one week after limb bud autotomy (LBA). Injection of extracts from 2 degrees LBs, but not 1 degrees LBs, inhibited 1 degrees LB growth in proecdysial animals, thus having the same effect on molting as LBA. The inhibitory activity in 2 degrees LB extracts was stable after boiling in water for 15 min, but was destroyed by boiling 15 min in 0.1 N acetic acid or incubation with proteinase K. These results support the hypothesis that LAF(pro) is a peptide that resembles a molt-inhibiting hormone.     

Limb Autotomy as an Investigatory Tool: Host Molt-Stage Affects the Success Rate of Infective Larvae of a Rhizocephalan Barnacle

D. M. Skinner was the first biologist to systematically investigatethe effect of multiple limb autotomy on ecdysis in decapod crustaceans.She proposed the existence of (1) limb autotomy factor anecdysis(LAF_an) which initiates precocious molting, and (2) limb autotomyfactor proecdysis (LAF^pro) which postpones proecdysis. Meantime to ecdysis did not differ significantly among groups ofsmall juvenile Callinectes sapidus with zero, two, four, andsix limbs removed. Variance was significantly less for the groupmissing six limbs; i.e., autotomy of six limbs synchronizedthe molt-cycle. These patterns were consistent with the hypothesesthat LAF^an exerts an additive effect, i.e., more anecdysialcrabs enter proecdysis as more limbs are autotomized and thata delay of proecdysis occurs above a threshold (>4) of autotomizedlimbs. Multiple limb autotomy provides investigators with easyaccess to crabs in metecdysial molt-stages which is useful instudying interactions between rhizocephalan barnacles and theirhosts. While 71% of metecdysial C. sapidus exposed to infectivelarvae of the sacculinid rhizocephalan, Loxothylacus texanus,developed the external stage of the parasite, no similarlysizedanecdysial crab was parasitized, suggesting that these crabsare not susceptible to infection during anecdysis. Size of C.sapidus at infection was inversely proportional to the numberof ecdyses between infection and emergence of the parasite,but not correlated to final host size. These data suggest thatthere is a minimum threshold for host size; smaller hosts undergomore ecdyses before attaining the threshold. Rhizocephalansare being considered as biological control agents and thereis a need to understand how they find and infect hosts. Becauselimb autotomy is such a useful research tool, D. M. Skinner'scontributions to our understanding of how limb autotomy influencesthe crustacean molt cycle will continue to pay significant dividendsin crustacean biology.     

Alternative tactics and responses to conflicting inputs in the porcellanid crab Petrolisthes elongates

When animals receive stimuli associated with incompatible responses, they either show behaviour patterns relevant to just one input (hierarchical model) or show levels of responses intermediate in intensity (summation model). When animals have alternative responses to one category of input, the summation model can be followed.

Individuals of the porcellanid crab Petrolisthes elongates were exposed to food odours and then to alarm odours and the intensity of feeding behaviours recorded. With their chelipeds intact, crabs exposed to food and alarm odours showed intermediate levels of feeding. Following the induction of cheliped autotomy (thereby eliminating autotomy as an alternative response to predation risk), the crabs exposed to food and alarm odours showed a complete cessation of feeding responses. Thus elimination of an alternative response to elevated predation risk led to a switch from the summation model to the hierarchical model, as predicted.     

The mechanics of predation by the shore crab,Carcinus maenas (L.), on the edible mussel,Mytilus edulis L.

Summary Mechanical aspects of predation by the shore crab, Carcinus maenas, on the edible mussel, Mytilus edulis, were examined. The shore crabs from the population studied utilized five distinct, largely size-related, mussel-opening techniques. Crushing the mussel umbone appeared the most successful opening method for medium-sized prey. Small mussels were crushed outright and large mussels could be opened by a slow, uneconomical, boring technique. The strengths of mussels, from an exposed shore, were tested under compression in four separate planes to determine the loads a crab would need to apply to crush the shells outright and the mechanical properties of mussels. Little inter-plane variability in compressive strength was observed, although intra-plane variability appeared high. The compressive strengths of mussels from a sheltered shore were found to be significantly higher than those from the exposed shore in the plane tested. A strain gauge was embedded in a mussel shell enabling the pattern and magnitude of forces produced by crab chelae in opening a mussel to be studied. The crab's chelae did not appear overwhelmingly strong when compared directly to the compressive strength of the crab's preferred mussel sizes. It is, therefore, postulated that crabs usually seek out and exploit weak spots in the umbone of mussels by trial and error, eventually breaking through the shell by a cumulative process of extending minute fractures in the shell substructure.     

Ecology and behavior of Gecarcoidea natalis, the Christmas Island red crab, during the annual breeding migration.

The terrestrial crab Gecarcoidea natalis is endemic to the forests of Christmas Island but must migrate each year to the coast to breed. During 1993 and 1995, radio-tracking, mark and recapture, and counting methods were used to establish the routes, walking speeds, direction of travel, and destinations of migrating crabs, as well as crab numbers and distribution. The density of crabs ranged from 0.09 to 0.57 crabs per square meter, which gave a population estimate of 43.7 million adult crabs on the island. During the dry season the crabs were relatively inactive but on arrival of the wet season immediately began their migration. The crabs generally walked in straight lines, and most crabs from around the Island traveled toward the northwest shore instead of simply walking toward the nearest shore. The maximum recorded distance walked by a red crab in one day was 1460 m, but the mean was 680 m per day in 1993 and 330 m in 1995. Comparing the 1993 and 1995 study seasons, there was a 3-week difference in the timing of the start of the migration, but the spawning date was fixed by the lunar phase and took place 17 to 18 days after mating. In 1993, late rain prompted a "rushed" migration and crabs walked directly to their shore destinations; in contrast, in 1995 most crabs made stops of 1 to 7 days during the downward migration. By giving the crabs a chance to feed along the way and minimizing the time that the population was concentrated near the shore, these stops may be important in ensuring that the animals have enough food after the long dry season. Furthermore, this behavior implies that the crabs are able to judge how far away they are from the shore during the migration.     

Patterns of autotomy and regeneration in Hemigrapsus nudus

Leg autotomy and regeneration can have severe impacts on survival and reproduction, and these impacts may be even more pronounced in animals with multifarious legs, such as decapods. Thus, determining the patterns and frequency of autotomy and regeneration could reveal the effects of these processes on the individual and population level. We investigated whether some legs are lost more often than others and if all legs are equally likely to be regenerated. We sampled nearly 500 purple shore crabs (Hemigrapsus nudus) and showed that (1) most animals are found with at least one injured leg, (2) the patterns of autotomy differ between males and females, and (3) successful claw regeneration is unlikely in both males and females. Future work with H. nudus and other grapsid crabs will elucidate how patterns seen here relate to other developmental and ecological factors.     

Regeneration of Walking Legs in the Fiddler Crab Uca pugilator

SYNOPSIS. Regeneration of walking legs in the fiddler crab Ucapugilator is most efficient when it follows autotomy (the reflexiveloss of a limb). Closure of the wound and would healing occurimmediately following autotomy and visible regeneration beginswithin a few days. Regeneration of the walking leg occurs intwo distinct stages: The first stage, called Basal Growth, involvesmitosis and differentiation. The second stage involves primarilyprotein synthesis and water uptake and is called ProecdysialGrowth. Proecdysial Growth is, in part, under direct hormonalstimulation.     

Sexual selection and the physiological consequences of habitat choice by a fiddler crab

In mid-Atlantic salt marshes, reproductively active male sand fiddler crabs, Uca pugilator, use a single greatly enlarged major claw as both a weapon to defend specialized breeding burrows from other males and an ornament to attract females for mating. During the summer breeding season, females strongly prefer to mate with males controlling burrows in open areas high on the shore. Food availability decreases while temperature and desiccation stress increase with increasing shore height, suggesting that the timing and location of fiddler crab mating activity may result in a potential trade-off between reproductive success and physiological condition for male crabs. We compared thermal preferences in laboratory choice experiments to body temperatures of models and living crabs in the field and found that from the perspective of a fiddler crab, the thermal environment of the mating area is quite harsh relative to other marsh microhabitats. High temperatures significantly constrained fiddler crab activity on the marsh surface, a disadvantage heightened by strongly reduced food availability in the breeding area. Nevertheless, when the chance of successfully acquiring a mate was high, males accepted a higher body temperature (and concomitantly higher metabolic and water loss rates) than when the chances of mating were low. Likewise, experimentally lowering costs by adding food and reducing thermal stress in situ increased fiddler crab waving display levels significantly. Our data suggest that fiddler crabs can mitigate potential life history trade-offs by tuning their behavior in response to the magnitude of both energetic and non-energetic costs and benefits.     

The effects of exposure and predation on the shell of two British winkles

Changes in shell size and shell shape of the two British winkles Littorina nigrolineata and L. rudis were studied in relation to exposure and to crab-size. In both species, shells from exposed shores are smaller and more globose than those from sheltered shores. Also, in rudis of exposed shores the mouth is relatively wider. In shores of equally sheltered conditions, shells are bigger at those localities where crabs are large than at those localities where they are small. The largest shells are found in those localities where it is extremely sheltered, and the crabs are very large.
It is argued that on exposed shores, small shells are favoured because they have more possibilities than large ones to shelter in crevices and in barnacle interspaces, from the impact of winds and waves. A globose shell could accommodate more foot muscle and thus enable a stronger adherence to the rock; and an increased mouth diameter would increase the area of foot adherence to the rock. On sheltered shores, on the other hand, large, narrow-mouthed shells are favoured because they discourage crab predation, large crabs being abundant mainly on sheltered shores.
The possible significance of shell size and shape in relation to zonation is discussed, in view of the different predatory and physical conditions which prevail in different zones of the shore, and the different shell specializations which these conditions would require.     

Regeneration and molting effects on a proprioceptor organ in the dungeness crab,Cancer magister

Decapoda Crustacea molt in order to grow; some species, such as the Dungeness crab Cancer magister, achieve a very large size. Does sendory neuron hyperplasia in internal proprioceptors accompany this growth? To determine this, neurons in propodite-dactylopodite (PD) chordotonal organs were counted in first walking legs of juvenile (5th through 9th instar) and adult (10th through 13th instar) C. magister. We found that the PD organs of J5 crabs have about 56 neurons; the number increases to about 61 neurons in J6 crabs. Significant hyperplasia now occurs because an average of 79 neurons are found in the PD organs of J7 crabs. Little to no hyperplasia accompanies the several succeeding juvenile and adult molts (ca. 82–86 neurons are present). Because autotomized limbs are regenerated upon molting, we also examined how the number of PD organ neurons in regenerated legs compare with those of pristine legs. Newly regenerated legs (termed 1st stage regenerates) have fewer sensory neurons than do their contralateral pristine partners (65 vs 81); larger regenerated legs which have attained nearly normal size as a result of additional molts (2nd stage regenerates) still have fewer neurons than their pristine partners (69 vs 81). Additionally, in contrast to those of pristine walking legs, the elastic strand of PD organs from 1st stage regenerates is a misshapen sheet containing a cluster of small neurons with no obvious functional organization. Nonetheless, neurophysiological recordings indicate that all the receptor types typical for pristine legs (movement and position cells) are represented. The PD organs of 2nd stage regenerates differentiate to the shape and neuronal organization of pristine legs. © 1994 John Wiley & Sons, Inc.     

Experimental infections of Orchitophrya stellarum (Scuticociliata) in American blue crabs (Callinectes sapidus) and fiddler crabs (Uca minax)

Outbreaks of an unidentified ciliate have occurred on several occasions in blue crabs from Chesapeake Bay held during winter months in flow-through systems. The parasite was initially thought to be Mesanophrys chesapeakensis, but molecular analysis identified it as Orchitophyra stellarum, a facultative parasite of sea stars (Asteroidea). We investigated the host-parasite association of O. stellarum in the blue crab host. Crabs were inoculated with the ciliate, or they were held in bath exposures after experimentally induced autotomy of limbs in order to determine potential mechanisms for infection. Crabs inoculated with the ciliate, or exposed to it after experimental autotomy, rapidly developed fatal infections. Crabs that were not experimentally injured, but were exposed to the ciliate, rarely developed infections; thus, indicating that the parasite requires a wound or break in the cuticle as a portal of entry. For comparative purposes, fiddler crabs, Uca minax, were inoculated with the ciliate in a dose-titration experiment. Low doses of the ciliate (10 per crab) were sometimes able to establish infections, but high intensity infections developed quickly at doses over 500 ciliates per crab. Chemotaxis studies were initiated to determine if the ciliate preferentially selected blue crab serum (BCS) over other nutrient sources. Cultures grown on medium with BCS or fetal bovine serum showed some conditioning in their selection for different media, but the outcome in choice experiments indicated that the ciliate was attracted to BCS and not seawater. Our findings indicate that O. stellarum is a facultative parasite of blue crabs. It can cause infections in exposed crabs at 10–15 °C, but it requires a portal of entry for successful host invasion, and it may find injured hosts using chemotaxis.     

The influence of temperature,sex and chela size in the foraging strategy of the shore crab,Carcinus maenas (L.)

Foraging rate was highly variable among shore crabs of the same size category and for individual crabs from day to day. Possible physiological reasons for this variability are discussed. Shore crab foraging rate, both in terms of mussels eaten per day and energy intake per day, was estimated to be higher at 17°C than at 10°C. The shape of diet curves and their mode for male shore crabs at 17°C closely resembled those for 10°C, indicating that the temperature increase had no effect on their previously demonstrated optimal foraging strategy.

Female and certain male shore crabs showed a preference for prey smaller than for other equivalent sized males. These suboptimally feeding male and female crabs attained a relatively higher prédation rate (mussels day^‐1), although their energy intake (KJ day^‐1) remained lower than that of optimally feeding males. Preferred mussel size, number of mussels eaten per day and energy intake were strongly related to master chela height. The diet curves for female and suboptimally feeding male shore crabs could be explained by these crabs’ proportionately smaller master chelae.     

Flight or fight: flexible antipredatory strategies in porcelain crabs

Autotomy, the voluntary shedding of limbs or other body partsin the face of predation, is a highly effective escape mechanismthat has evolved independently in a variety of taxa. Crabs areunusual in that the limb that is typically sacrificed duringautotomy, the anterior clawed cheliped, can also be used toward off attack. During an encounter with a predator, an individualmust thus decide between two mutually exclusive strategies:flight or fight. We used experimental predation encounters withtwo species of porcelain crabs (genus Petrolisthes) to examinethe factors that influence the decision to flee versus fightand to determine the degree to which this decision is context-dependent.We found that autotomy was highly conditional. The characteristicsthat best predicted autotomy—smaller body size or femalegender—also correlated with a lower escape rate by thealternative escape tactic, struggling and pinching the predator.Variation among individuals in the benefit of autotomy (relativeto alternative tactics) appears to drive variation in propensityto autotomize. Porcelain crabs thus demonstrate adaptive flexibility,employing the costly strategy of autotomizing a limb as a lastresort, only when their chance at success by struggling is low.     

A developmental model for predicting handedness frequencies in crabs

Brachyuran crabs develop handedness in at least two different ways. Some crabs, such as Cancer productus, become heterochelous through use-induced differences in claw growth. Other crab species, for instance Carcinus maenas, appear to have a genetic predisposition towards right handedness. In this latter case, however, handedness reversal may take place following autotomy of the major claw. Thus, in C. maenas, and other species with this developmental strategy, younger cohorts are strongly biased towards right-handed individuals and the frequency of left-handedness increases with each subsequent moult. In the absence of differential mortality the ratio of left-handed to right-handed crabs in a given population should be predictable if the frequencies of right and left claw loss are known for different stages in the life history. Here, we develop a simple mathematical model for predicting handedness in crabs under the Carcinus-model of claw ontogeny and apply it to two species with very different ecologies and life histories; the green crab (Carcinus maenas (L.)) and the Trinidadian mountain crab (Eudaniela garmani (Rathburn)). The predicted and observed handedness frequencies were in complete concordance for the early intermoults of both species but significantly deviated in mature C. maenas where left-handed individuals were under-represented in the population. These results are discussed in the context of the evolution and functional significance of claw autotomy and handedness in crabs.     

Simultaneous induction of ectopic pelvic zone and duplication of regenerated limbs in tadpoles of Polypedates maculatus by vitamin A

With a view to determine ectopic limb developing capacity along with normal hind limb regeneration in response to vitamin A palmitate in well-differentiated hind limb stage tadpoles of P. maculatus, higher doses of vitamin A (30 IU/ml and 20 IU/ml) were administered for a longer period (120 hr) to the tadpoles following tail amputation through middle and hind limb amputation through middle of thigh. Simultaneous development of ectopic pelvic zone was observed along with hind limbs from the cut end of tail and duplication of regenerated hind limbs in the same tadpole for the first time. Besides, development of double ectopic pelvic girdle was also reported in one case. Results also indicate that induction of pelvic zone and duplication of regenerated limbs are concentration dependent.