The evolution of armament strength: evidence for a constraint on the biting performance of claws of durophagous decapods

Performance data for the claws of six sympatric species of Cancer crabs confirmed a puzzling pattern reported previously for two other decapod crustaceans (stone crabs, Menippe mercenaria, and lobsters, Homarus americanus): Although biting forces increased, maximum muscle stresses (force per unit area) declined with increasing claw size. The negative allometry of muscle stress and the stress at a given claw size were fairly consistent within and among Cancer species despite significant differences in adult body size and relative claw size, but were not consistent among decapod genera. Therefore, claw height can be used as a reliable predictor of maximum biting force for the genus Cancer, but must be used with caution as a predictor of maximum biting force in wider evolutionary and biogeographical comparisons of decapods. The decline in maximum muscle stress with increasing claw size in Cancer crabs contrasts with the pattern in several other claw traits. Significantly, three traits that affect maximal biting force increased intraspecifically with increasing claw size: relative claw size, mechanical advantage, and sarcomere length of the closer muscle. Closer apodeme area and angle of pinnation of the closer muscle fibers varied isometrically with claw size. The concordant behavior of these traits suggests selection for higher biting forces in larger crabs. The contrast between the size dependence of muscle stress (negative allometry) and the remaining claw traits (isometry or positive allometry) strongly suggests that an as yet unidentified constraint impairs muscle performance in larger claws. The negative allometry of muscle stress in two distantly related taxa (stone crabs and lobsters) further suggests this constraint may be widespread in decapod crustaceans. The implications of this performance constraint for the evolution of claw size and the "arms-race" between decapod predators and their hard-shelled prey is discussed.     

Size,shape, and sex‐dependent variation in force production by crayfish chelae

The ability to generate large closing forces is important for many animals. Several studies have demonstrated that bite or pinching force capacity is usually related to the linear dimensions of the closing apparatus. However, relatively few studies have applied geometric morphometrics to examine the effects of size‐independent shape on force production, particularly in studies of crustacean pinching force. In this study, we utilized traditional and geometric morphometric techniques to compare the pinching force of Procambarus clarkii crayfish to their chela morphology. We found that males possessed larger chelae and pinched harder than females, but that their chela shape and size were weak predictors of strength. Female pinching force was significantly affected by both chela size and shape, with shape variation along the short axis of the claw contributing most to pinching force. We discuss our results in the context of reliable signaling of strength by males and females, and the different selective forces acting on chela shape in the two sexes.     

Variation in safety factors of claws within and among six species of Cancer crabs (Decapoda: Brachyura)

To better understand how safety factors of biological structures evolve, we examined the frequency of claw failure, and the intra‐ and interspecific patterns of variation in maximum biting force and breaking strength in the claws of six species of Cancer (Linnaeus) crabs that live in sympatrv along the coast of the northeastern Pacific: C. antennarius, C. branneri, C. gracilis, C. maguter, C. oregonensis and C. productus. Although the breakage frequencies in natural populations were similar among species (6%), they were higher than predicted based on failure probabilities calculated from laboratory measurements of biting force and breaking strength for healthy pristine claws. The incidence of claw damage was correlated with the degree of wear, suggesting that claws later in the intermolt interval were more likely to fail. Within species, safety factors increased from 3.1 to 4.6 with increasing instar number due primarily to a decline in muscle stress (force per unit area of apodeme). Surprisingly, the lower maximum muscle stress generated by later instars appeared to be due to behavioral restraint, since it was not accompanied by relatively lower muscle mass. In addition, among individuals of the same claw size, lower breaking forces were correlated with lower maximum biting force, and both were correlated with lighter cuticle and closer muscle mass, suggesting a coupling that maintains a more stable safety factor over the moult cycle. In some species, size‐adjusted maximum biting forces were higher for males than females, but this paralleled differences in breaking strength, so safety factors did not differ between the sexes. Among the six Cancer species, one exhibited an unusually high safety factor (C. oregonensis, 7.4) and another an unusually low one (C. maguter, 2.6). The remaining four species were similar to each other and exhibited an intermediate safety factor (3.6). From a phylogenetic perspective, the species with more extreme safety factors appeared to be derived from a common ancestor with an intermediate safety factor. From an ecological perspective, species more closely associated with rocky substrata, and presumably a higher incidence of hard‐shelled prey, exhibited higher safety factors. But safety factors were also correlated with relative claw size, and sexual dimorphism in claw size. Although we cannot say whether habitat, diet or sexual selection are primarily responsible for the differences in safety factors observed among species, the cost of producing a relatively larger claw seems an unlikely explanation because safety‐factors did not differ between males and females in any of the sexually dimorphic species.     

The effects of biting and pulling on the forces generated during feeding in the Komodo dragon (Varanus komodoensis)

In addition to biting, it has been speculated that the forces resulting from pulling on food items may also contribute to feeding success in carnivorous vertebrates. We present an in vivo analysis of both bite and pulling forces in Varanus komodoensis, the Komodo dragon, to determine how they contribute to feeding behavior. Observations of cranial modeling and behavior suggest that V. komodoensis feeds using bite force supplemented by pulling in the caudal/ventrocaudal direction. We tested these observations using force gauges/transducers to measure biting and pulling forces. Maximum bite force correlates with both body mass and total body length, likely due to increased muscle mass. Individuals showed consistent behaviors when biting, including the typical medial-caudal head rotation. Pull force correlates best with total body length, longer limbs and larger postcranial motions. None of these forces correlated well with head dimensions. When pulling, V. komodoensis use neck and limb movements that are associated with increased caudal and ventral oriented force. Measured bite force in Varanus komodoensis is similar to several previous estimations based on 3D models, but is low for its body mass relative to other vertebrates. Pull force, especially in the ventrocaudal direction, would allow individuals to hunt and deflesh with high success without the need of strong jaw adductors. In future studies, pull forces need to be considered for a complete understanding of vertebrate carnivore feeding dynamics.     

Differential distribution of β-pigment-dispersing hormone (β-PDH)-like immunoreactivity in the stomatogastric nervous system of five species of decapod crustaceans

Summary Pigment-dispersing hormone (PDH) acts to disperse pigments within the chromatophores of crustaceans. Using an antibody raised against -PDH from the fiddler crab Uca pugilator, we characterized the distribution of -PDH-like immunoreactivity in the stomatogastric nervous system of five decapod crustaceans: the crabs, Cancer borealis and Cancer antennarius, the lobsters, Panulirus interruptus and Homarus americanus, and the crayfish, Procambarus clarkii. No somata were stained in the stomatogastric ganglion (STG) or the esophageal ganglion in any of these species. Intense PDH-like staining was seen in the neuropil of the STG in P. interruptus only. In all 5 species, cell bodies, processes, and neuropil within the paired circumesophageal ganglia (CGs) showed PDH-like staining; the pattern of this staining was unique for each species. In each CG, the -PDH antibody stained: 1 large cell in C. borealis; 3 small to large cells in C. antennarius; 3–8 medium cells in P. clarkii; 1–4 small cells in H. americanus; and 13–17 small cells in P. interruptus. The smallest cell in each CG in C. antennarius sends its axon, via the inferior esophageal nerves, into the opposite CG; this pair of cells, not labeled in the other species studied, may act as bilateral coordinators of sensory or motor function. These diverse staining patterns imply some degree of evolutionary diversity among these crustaceans. A -PDH-like peptide may act as a neuromodulator of the rhythms produced by the stomatogastric nervous system of decapod crustaceans.     

Predation by red-jointed fiddler crabs on congeners: interaction between body size and positive allometry of the sexually selected claw

The enlarged (major) claw of male fiddler crabs is used in contestsover breeding burrows and is waved to attract females. We recentlydiscovered that males of the red-jointed fiddler crab, Uca minax,also use the claw to kill smaller-sized fiddler crabs, U. pugnaxand U. pugilator, with which they co-occur in Atlantic coastsalt marshes. Large U. minax males use walking legs or the enlargedclaw to capture prey feeding on moist sand flats. On sand flats,small U. minax males and females are much less common than largemales, suggesting that large males move onto sand flats to seekprey. Males of prey species use the major claw against attackingpredators and, consequently, are more likely than females toescape. In laboratory experiments, large U. minax males weremore likely to attack and kill small-clawed males and femalesthan large-clawed males, consistent with a preference for morevulnerable, less threatening prey. The size of the major clawis a positive allometric function of body size. The allometricfunction varies little among species. Also, the mechanical advantageand indices of closing speed and closing force of the majorclaw, when corrected for body size, are not consistently greaterin U. minax relative to prey species. Thus, predation by U.minax males may reflect the opportunity afforded by larger bodysize and positive allometric growth, which result in a majorclaw that is more massive than the prey it is directed against.     

Shaking a leg and hot to trot: the effects of body size and temperature on running speed in ants

Abstract.  1. Data were compiled from the literature and our own studies on 24 ant species to characterise the effects of body size and temperature on forager running speed.
2. Running speed increases with temperature in a manner consistent with the effects of temperature on metabolic rate and the kinetic properties of muscles.
3. The exponent of the body mass-running speed allometry ranged from 0.14 to 0.34 with a central tendency of approximately 0.25. This body mass scaling is consistent with both the model of elastic similarity, and a model combining dynamic similarity with available metabolic power.
4. Even after controlling for body size or temperature, a substantial amount of inter-specific variation in running speed remains. Species with certain lifestyles [e.g. nomadic group predators, species which forage at extreme (>60 °C) temperatures] may have been selected for faster running speeds.
5. Although ants have a similar scaling exponent to mammals for the running speed allometry, they run slower than predicted compared with a hypothetical mammal of similar size. This may in part reflect physiological differences between invertebrates and vertebrates.     

Intraspecific temperature dependence of the scaling of metabolic rate with body mass in fishes and its ecological implications

Metabolism constitutes a fundamental property of all organisms. Metabolic rate is commonly described to scale as a power function of body size and exponentially with temperature, thereby treating the effects of body size and temperature independently. Mounting evidence shows that the scaling of metabolic rate with body mass itself depends on temperature. Across‐species analyses in fishes suggest that the mass‐scaling exponent decreases with increasing temperature. However, whether this relationship holds at the within‐species level has rarely been tested. Here, we re‐analyse data on the metabolic rates of four freshwater fish species, two coregonids and two cyprinids, that cover wide ranges of body masses and their naturally experienced temperatures. We show that the standard metabolic rate of the coregonids is best fit when accounting for a linear temperature dependence of the scaling of metabolic rate with body mass, whereas a constant mass‐scaling exponent is supported in case of the cyprinids. Our study shows that phenotypic responses to temperature can result in temperature‐dependent scaling relationships at the species level and that these responses differ between taxa. Together with previous findings, these results indicate that evolutionarily adaptive and phenotypically plastic responses to temperature affect the scaling of metabolic rate with body mass in fishes.     

Intraspecific mass scaling of metabolic rates in grass carp (Ctenopharyngodon idellus)

We assessed the intraspecific mass scaling of standard metabolic rate (SMR), maximum metabolic rate (MMR), excess post-exercise oxygen consumption (EPOC), and erythrocyte size in grass carp (Ctenopharyngodon idellus), with body masses ranging from 4.0 to 459 g. SMR and MMR scaled with body mass with similar exponents, but neither exponent matched the expected value of 0.75 or 1, respectively. Erythrocyte size scaled with body mass with a very low exponent (0.090), suggests that while both cell number and cell size contribute to the increase in body mass, cell size plays a smaller role. The similar slopes of MMR and SMR in grass carp suggest a constant factorial aerobic scope (FAS) as the body grows. SMR was negatively correlated with FAS, indicating a tradeoff between SMR and FAS. Smaller fish recovered faster from the exhaustive exercises, and the scaling exponent of EPOC was 1.075, suggesting a nearly isometric increase in anaerobic capacity. Our results provide support for the cell size model and suggest that variations of erythrocyte size may partly contribute to the intraspecific scaling of SMR. The scaling exponent of MMR was 0.863, suggesting that the metabolism of non-athletic fish species is less reliant on muscular energy expenditure, even during strenuous exercise.     

Food availability in beach and marsh habitats and the size of the fiddler crab claw,a sexually selected weapon and signal

Males of the sand fiddler crab Uca pugilator possess a greatly enlarged claw that is used as a weapon in ritualized contests for control of breeding burrows and is waved to attract females to breeding burrows. Approximately 5400 crabs were collected along the Atlantic coast of North America at 14 localities, all of which had both beach and salt marsh habitats. Five measurements were made on each claw. Principal components analysis was used to generate a single measure of claw size from the seven correlated measures and scores of the claw. Carapace width was measured to index body size. Claw size was greater in beach than marsh habitats, controlling for body size. However, body size did not differ by habitat type. Claw size was also greater in laboratory‐reared males receiving more food, suggesting that differential access to food could influence habitat‐associated differences in claw size. Chlorophyll a concentration and total organic content, reflecting, respectively, the abundance of benthic algae and other food, were greater in beach than marsh habitats. Moreover, feeding opportunities were greater in the wetter beach habitat because crabs there, but not in marsh habitat, can feed at breeding burrows. Adult fiddler crabs continue to molt and grow in both body and claw size as they age. Energetic investment in the claw relative to the body is plastic. It appears that the availability of food can affect the amount of energy invested in the claw.     

Idiosyncratic species effects confound size-based predictions of responses to climate change

Understanding and predicting the consequences of warming for complex ecosystems and indeed individual species remains a major ecological challenge. Here, we investigated the effect of increased seawater temperatures on the metabolic and consumption rates of five distinct marine species. The experimental species reflected different trophic positions within a typical benthic East Atlantic food web, and included a herbivorous gastropod, a scavenging decapod, a predatory echinoderm, a decapod and a benthic-feeding fish. We examined the metabolism–body mass and consumption–body mass scaling for each species, and assessed changes in their consumption efficiencies. Our results indicate that body mass and temperature effects on metabolism were inconsistent across species and that some species were unable to meet metabolic demand at higher temperatures, thus highlighting the vulnerability of individual species to warming. While body size explains a large proportion of the variation in species'' physiological responses to warming, it is clear that idiosyncratic species responses, irrespective of body size, complicate predictions of population and ecosystem level response to future scenarios of climate change.     

Size,but not sex,predicts pinch force and exoskeleton mechanical properties in crayfish of the genus Faxonius

Studies of animal weaponry and defensive structures rarely take into consideration their underlying mechanical properties. We measured the compressive strength and thickness of the exoskeleton of the claw (chela) in two North American crayfish species, Faxonius virilis and F. limosus. We performed similar measures on the carapace, a body region not directly involved in agonistic contests. Males of both species generated significantly stronger maximum pinch forces than females. However, these differences can be attributed to differences in claw size between the sexes. The thickness (ultrastructure) of the claw exoskeleton was a significant predictor of its compressive strength and likely explained the difference in compressive strength we observed between the two species. Neither claw thickness nor claw compressive strength was correlated with maximum pinch force. Additionally, we found that crayfish body size was a strong predictor of carapace compressive strength and thickness, whereas sex was not. The claw had greater compressive strength and thickness than the corresponding values for the carapace. Our study shows that the mechanical properties of the crayfish exoskeleton are largely a function of size and highlights the need to integrate mechanical properties into studies of animal morphology and performance.     

Exotic species of freshwater decapod crustaceans in the state of São Paulo,Brazil: records and possible causes of their introduction

Based on recent surveys of the freshwater decapod fauna, distributional data of five exotic species of freshwater decapod crustaceans for the hydrographic basins of the state of São Paulo are presented, as part of a large initiative for a comprehensive survey of the state’s biodiversity (BIOTA-FAPESP Program). These species are the North American crayfish Procambarus clarkii (Girard) (Cambaridae), the crab Dilocarcinus pagei Stimpson (Trichodactylidae) from the Amazon and Paraguay/lower Paraná River Basins, and the palaemonid shrimps Macrobrachium rosenbergii (De Man), from the Indo-Pacific region, Macrobrachium amazonicum (Heller) and Macrobrachium jelskii (Miers), both from the Orinoco, Amazon and the Paraguay/lower Paraná River Basins. Possible modes by which their introduction might have occurred are commented upon and potential consequences are discussed.     

A new use for synchrotron X‐ray microtomography: three‐dimensional biomechanical modeling of chelicerate mouthparts and calculation of theoretical bite forces

Abstract. We present the first report on the use of the non‐invasive method of synchrotron X‐ray microtomography to model the dynamics and theoretical bite forces of arthropod mouthparts. The nature of the data allowed us to include precise measurements of muscle areas and the spatial geometry of muscle origins and insertions into a biomechanical model of a morphological microstructure. We investigated the functional morphology of the chelicera in the oribatid mite Archegozetes longisetosus (Acari, Oribatida), a model organism for Chelicerata. The chelicera represents a first‐class lever; the intrinsic muscular system consists of a feather‐shaped depressor with six muscle bundles and a bouquet‐shaped levator with 16 bundles. The relative bite forces, as compared with body mass (force/mass^2/3), are 390 N kg^?1 and lie within those known for vertebrates (≤260 N kg^?1) and decapod chelae (≤915 N kg^?1). The dynamics of force transmission and bite forces during the movement of the apotele are calculated. The conserved organization of cheliceral musculature allows broad adaptation of the model to other chelicerate taxa.     

Sample size and mass range effects on the allometric exponent of basal metabolic rate

The controversial relationship between body mass and basal metabolic rate in animals revolves around two questions: what is the allometric scaling exponent and what is the functional basis for it? For mammals, the first question could be resolved if measurements from all 4600 extant species were available, but this study shows that data for only 150 species, spanning three to four orders of magnitude variation in body mass, are sufficient to accurately determine the exponent. Because the currently available data set includes about 600 species that vary over five orders of magnitude in body size, further increases in sample size are unlikely to change the estimate of the scaling exponent.     

Adult neurogenesis: examples from the decapod crustaceans and comparisons with mammals

Defining evolutionary origins is a means of understanding an organism's position within the integrated web of living beings, and not only to trace characteristics back in time, but also to project forward in an attempt to reveal relationships with more recently evolved forms. Both the vertebrates and arthropods possess condensed nervous systems, but this is dorsal in the vertebrates and ventral in the arthropods. Also, whereas the nervous system in the vertebrates develops from a neural tube in the embryo, that of the arthropods comes from an ectodermal plate. Despite these apparently fundamental differences, it is now generally accepted that life-long neurogenesis, the generation of functionally integrated neurons from progenitor cells, is a common feature of the adult brains of a variety of organisms, ranging from insects and crustaceans to birds and mammals. Among decapod crustaceans, there is evidence for adult neurogenesis in basal species of the Dendrobranchiata, as well as in more recent terrestrial, marine and fresh-water species. The widespread nature of this phenomenon in decapod species may relate to the importance of the adult-born neurons, although their functional contribution is not yet known. The many similarities between the systems generating neurons in the adult brains of decapod crustaceans and mammals, reviewed in this paper, suggest that adult neurogenesis is governed by common ancestral mechanisms that have been retained in a phylogenetically broad group of species.     

Maximum force production: why are crabs so strong?

Durophagous crabs successfully hunt hard-shelled prey by subjecting them to extremely strong biting forces using their claws. Here I show that, for a given body mass, six species of Cancer crabs (Cancer antennarius, Cancer branneri, Cancer gracilis, Cancer magister, Cancer oregonensis and Cancer productus) were able to exert mean maximum biting forces greater than the forces exerted in any other activity by most other animals. These strong biting forces were in part a result of the high stresses (740-1350 kN m(-2)) generated by the claw closer muscle. Furthermore, the maximum muscle stress increased with increasing mean resting sarcomere length (10-18 microm) for the closer muscle of the claws of these six Cancer species. A more extensive analysis incorporating published data on muscle stresses in other animal groups revealed that stress scales isometrically with the resting sarcomere length among species, as predicted by the sliding filament model of muscle contraction. Therefore, muscle or filament traits other than a very long mean sarcomere length need not be invoked in explaining the high stresses generated by crustacean claws.     

Approach of females to magnified reflections indicates that claw size of waving fiddler crabs correlates with signaling effectiveness

Male sand fiddler crabs, Uca pugilator, wave a claw to attract females to a breeding burrow. The effect of claw size on the likelihood of attracting mate-seeking females is little studied although in some other species females preferentially approach larger males. We used paired mirrors to reflect different sized images of the same male in a South Carolina (USA) back-beach habitat. Use of mirrors controlled for waving rate (but not velocity), waving motion, claw color, and claw shape. Female choice was attributed to instances in which a female contacted one of two mirrors. Paired mirrors were inclined toward one another in an arena defined by blinds and containing a single male. Two reflections of the male were visible to females moving approximately 50 cm toward the mirrors. The male was behind a small internal blind and not directly visible. In one-half of the trials, a non-magnifying mirror was placed at the bottom of mirrors so that only the elevated claw was magnified. Thus, body and burrow size and apparent distance were controlled. Receptive females preferred the larger reflection whether or not the body of the male was magnified, suggesting the importance of claw size. Non-receptive females did not exercise a choice. Control arenas, without a male, rarely attracted females. The results suggest that females choose on the basis of claw size. Selection on females may favor response to larger-clawed males because use of the claw in contests between males over burrows maintains the honesty of claw size as a signal of burrow quality.     

Acoustic detection and communication by decapod crustaceans

This paper reviews behavioral, physiological, anatomical, and ecological aspects of sound and vibration detection by decapod crustaceans. Our intent is to demonstrate that despite very limited work in this area in the past 20 years, evidence suggests that at least some decapod crustaceans are able to detect and use sounds in ways that parallel detection and processing mechanisms in aquatic and terrestrial vertebrates. Some aquatic decapod crustaceans produce sounds, and many are able to detect substrate vibration at sensitivities sufficient to tell of the proximity of mates, competitors, or predators. Some semi-terrestrial crabs produce and use sounds for communication. These species detect acoustic stimuli as either air- or substrate-borne energies, socially interact in acoustic "choruses," and probably use "calls" to attract mates.     

The geography of crushing: Variation in claw performance of the invasive crab Carcinus maenas

The major claws of predatory, durophagous decapods are specialized structures that are routinely used to crush the armor of their prey. This task requires the generation of extremely strong forces, among the strongest forces measured for any animal in any activity. Laboratory studies have shown that claw strength in crabs can respond plastically to, and thereby potentially match, the strength of their prey's defensive armor. These results suggest that claw strength may be variable among natural populations of crabs. However, very few studies have investigated spatial variation in claw strength and related morphometric traits in crabs. Using three geographically separate populations of the invasive green crab in the Gulf of Maine, we demonstrate, for the first time, geographic variation in directly measured claw crushing forces in a brachyuran. Despite variation in mean claw strength however, the scaling of claw crushing force with claw size was consistent among populations. We found that measurements of crushing force were obtained with low error and were highly repeatable for individual crabs. We also show that claw mass, independent of a linear measure of claw size, and carapace color, which is an indicator of time spent in the intermoult, were important predictors of claw crushing force.