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.     

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.     

Bilateral linkage of monomorphic and dimorphic limb sizes in fiddler crabs

In this study, the subject of whether investment in one bilateral structure was linked to investment in the homologous bilateral opposite structure was investigated. Male fiddler crabs (genus Uca, family Ocypodidae) displayed strong bilateral claw differentiation of function and size, which are used for feeding (minor claw) or display/combat (major claw). Females had similar‐sized feeding claws. Linkage between claw size was investigated by estimating the deviations from an overall fitted regression of claw length to body size. The positive correlations of the deviations of claw size for major and minor claws of males and between right and left claws of females, relative to body size, suggested a linkage in investment between one claw and the corresponding claw on the other side of the body, for both monomorphic females and dimorphic males. A signal to send resources may be effectively gated to the claw complex, suggesting that positively correlated resources are allocated to both claws. Positive correlations were also found at the interspecific level. The fiddler crab model, described here, gives access to study the linkage in symmetric and asymmetric bilateral structures in the same species with a connection to the macroevolutionary level.     

Claw morphometrics in monitor lizards: Variable substrate and habitat use correlate to shape diversity within a predator guild

Numerous studies investigate morphology in the context of habitat, and lizards have received particular attention. Substrate usage is often reflected in the morphology of characters associated with locomotion, and, as a result, claws have become well‐studied ecomorphological traits linking the two. The Kimberley predator guild of Western Australia consists of 10 sympatric varanid species. The purpose of this study was to quantify claw size and shape in the guild using geometric morphometrics, and determine whether these features correlated with substrate use and habitat. Each species was assigned a Habitat/substrate group based on the substrate their claws interact with in their respective habitat. Claw morphometrics were derived for both wild caught and preserved specimens from museum collections, using a 2D semilandmark analysis. Claw shape significantly separated based on Habitat/substrate group. Varanus gouldii and Varanus panoptes claws were associated with sprinting and extensive digging. Varanus mertensi claws were for shallow excavation. The remaining species’ claws reflected specialization for some form of climbing, and differed based on substrate compliance. Varanus glauerti was best adapted for climbing rough sandstone, whereas Varanus scalaris and Varanus tristis had claws ideal for puncturing wood. Phylogenetic signal also significantly influenced claw shape, with Habitat/substrate group limited to certain clades. Positive size allometry allowed for claws to cope with mass increases, and shape allometry reflected a potential size limit on climbing. Claw morphology may facilitate niche separation within this trophic guild, especially when considered with body size. As these varanids are generalist predators, morphological traits associated with locomotion may be more reliable candidates for detecting niche partitioning than those associated directly with diet.     

Curvature facilitates prey fixation in predatory insect claws

Insects show a large variety in prey capture strategies, with a correspondingly large diversity in predatory adaptations. We studied a specific type of predatory claws, these can for example be found in praying mantis species. The claw is closeable over its entire length and the prey is fixed between the femur (upper arm) and the tibia (lower arm) of the insect leg. The morphology of these predatory claws is diverse. Some species have straight claws covered with spines, while other species have smooth, curved claws. We have studied the mechanics of this femur-tibia type of predatory insect claws, by making a physical model, eventually trying to explain why in some insect species the claws are curved instead of straight. The main results are (1) when comparing curved claws to straight claws, curvature leads to a strong reduction of forces driving the prey away from the pivoting point, thereby reducing the need for friction generating structures. (2) In the curved claw model a position exists where the resulting force on the prey is exactly zero. This is because the normal forces on the femur and tibia are opposed, and in line. At this position the prey is perfectly clamped and not driven out of the claw. This feature does not exist in straight claws. (3) In the curved claw, the prey cannot be placed at a position further than a certain maximum distance from the pivoting point. Near this maximum position, the resulting force on the prey reaches high values because moment arms are near zero. (4) Between the zero position and the maximum position the resulting force is directed toward the pivoting point, which stabilizes prey fixation.     

Pinching forces in crayfish and fiddler crabs,and comparisons with the closing forces of other animals

The pinching forces of crustaceans are in many respects analogous to the biting forces of vertebrates. We examined the effects of body size and chelae size and shape, on the closing forces of the fiddler crab, Uca pugilator, and the crayfish, Procambarus clarkii. We hypothesized that the allometric relationships would be similar among species, and comparable to those reported for other decapod crustaceans. We further hypothesized that the scaling of the closing forces of crustaceans, with respect to body size and with the geometry of the pinching or biting structures, would be similar to that of vertebrates. We found that pinching forces increased with body mass, claw dimensions, and claw mass in U. pugilator, but only with claw height and claw mass in P. clarkii. Contraction time increased with body mass for both species combined, whereas contraction speed decreased. Pooled data for these and 17 other species of decapod crustacean revealed a positive correlation between the pinching force and body mass with a scaling exponent of 0.71. These data are remarkably comparable to the values on closing forces of vertebrate jaws, with the pooled data having a scaling exponent of 0.58, slightly below the value of 0.67 predicted for geometric similarity. Maximum closing forces vary tremendously among both crustaceans and animals in general, with body size and food habits being among the most important determining factors.     

Walking on smooth or rough ground: passive control of pretarsal attachment in ants

The hymenopteran tarsus is equipped with claws and a movable adhesive pad (arolium). Even though both organs are specialised for substrates of different roughness, they are moved by the same muscle, the claw flexor. Here we show that despite this seemingly unfavourable design, the use of arolium and claws can be adjusted according to surface roughness by mechanical control. Tendon pull experiments in ants (Oecophylla smaragdina) revealed that the claw flexor elicits rotary movements around several (pre-) tarsal joints. However, maximum angular change of claws, arolium and fifth tarsomere occurred at different pulling amplitudes, with arolium extension always being the last movement. This effect indicates that arolium use is regulated non-neuronally. Arolium unfolding can be suppressed on rough surfaces, when claw tips interlock and inhibit further contraction of the claw flexor or prevent legs from sliding towards the body. To test whether this hypothesised passive control operates in walking ants, we manipulated ants by clipping claw tips. Consistent with the proposed control mechanism, claw pruning resulted in stronger arolium extension on rough but not on smooth substrates. The control of attachment by the insect claw flexor system demonstrates how mechanical systems in the body periphery can simplify centralised, neuro-muscular feedback control.     

Avian claw morphometry and growth determine the temporal pattern of archived stable isotopes

Detailed knowledge about claw formation and growth rate is a prerequisite for the interpretation of avian claw stable isotopes, as is commonly done with feather stable isotopes to e.g. infer habitat use, dietary specialisations, and spatial occurrence. In this study, we provide basic information about claw formation and empirical evidence about the time scale of archiving isotopic information to develop a reliable assessment of archived isotopic pattern in claws of passerines. Avian claws grow conically from the tip of the bone of the phalanx. The length of the tip of an avian claw, suitable for stable isotope analysis, is about 42 ± 6.8% (SD) of total linear claw length and can also be estimated from the body mass of a given species. Claw growth rate in adult songbirds typically ranged between 0.03 and 0.05 mm d^?1, but differed between front and back toes, and varied seasonally. From the claw growth rate, the archiving period of a given claw length can be estimated. In long‐distance migrant species, δ¹³C of claws matched δ¹³C of feathers grown during the same period (wintering or breeding period). In Palaearctic‐African migrants sampled in the breeding season, δ¹³C of the distal half of the claw tip reflected the African wintering site, while the proximal half reflected a blend of African and European δ¹³C signatures, as expected. Hence there is empirical evidence that entire claw tips mirror the isotopic environments over longer periods (up to months), and over weeks when parts can be analysed. However any part of a claw contains a blend of material formed at different times due to the claw's conical (i.e. longitudinal and lateral) growth. Avian claws provide a complementary isotope archive for investigations, but its applicability may vary according to the ecology of the study species.     

THE DESIGN OF A BEAUTIFUL WEAPON: COMPENSATION FOR OPPOSING SEXUAL SELECTION ON A TRAIT WITH TWO FUNCTIONS

Male fiddler crabs, genus Uca, have one greatly enlarged claw with which they court females and threaten and fight other males. Longer claws are more effective signals but are thought to be less effective weapons because the relative closing force at the tip of the claw decreases with claw length. We studied claw morphology and fighting in Uca terpsichores and Uca beebei and found a mechanism that may resolve opposing selection for signaling and fighting ability. When males fought they delivered gripping forces not at the tips but at the tubercles on the inner margins of their claws’ fingers. As claws grow, these tubercles remain relatively close to the apex of the gape. Consequently, the mechanical advantage that governs the forces that can be delivered at these tubercles decreases only slightly with increasing claw length allowing the claw to be an effective signal and a powerful weapon. Animal weapons are exceptionally diverse in form and detail of armature and the causes of this diversity are poorly understood. We suggest that the designs of weapons may often reflect compensatory patterns of growth and placement of armature that enhances the weapon's overall utility for multiple uses in competition for mates.     

Crushing behavior of tropical and temperate crabs

The Guamunian xanthids Carpilius maculatus (L.), C. convexus (Forskal), and Eriphia sebana (Shaw & Nodder), and the parthenopid Daldorfia horrida (L.), possess large master claws with molariform teeth than are used to crush the shells of hermit crabs and snails. These crabs typically sever the spire of their prey, or make a gash in the body whorl. They tend to employ sustained pressure on the prey shell, and, except for Eriphia, rarely attack the outer lip, so that the outer lip of the shell typically remains undamaged, except in shells near the critical size, i.e., the maximum size of vulnerability to predation. Temperate species of Cancer (C. productus Randall and C. oregonensi Rathbun) may also crush shelled prey in the larger of their two claws, but more commonly they use both claws together in breaking open their victims. Sustained pressure is applied for only short periods by these crabs.Gastropod adaptations conferring resistance to crushing by crabs include a thick shell, narrow or otherwise small aperture, thickened outer lip, strong sculpture, and a low spire. Emphasis on these traits lowers the critical size of the prey, i.e., permits escape from cushing at a smaller size. An equatorward increase in the expression of the characteristics of crushing-resistance parallels an increase in crushing power of the crabs.     

Pincer-like claws in centipedes (Chilopoda): multiple evolutionary origin of similar form and serial pattern

In most Chilopoda, the walking legs end in a single-tip claw usually accompanied by short accessory spines. Instead, in all species of three small and only distantly related geophilomorph taxa (Diphyonyx, Neogeophilidae, Eucratonyx), the claws of an anterior set of leg pairs are unusually pincer-like. By integrating different microscopic techniques, including confocal laser scanning microscopy, we found that these modified claws are very similar in form, internal structure, and pattern of variation in shape along the trunk in all three taxa: the claws are distinctly swollen and bent, provided with peculiar bulges, and flanked by a conspicuous additional branch, either cylindrical or flattened, which overreaches the tip of the claw; instead, the internal cuticular features are not modified with respect to the condition in the other centipedes, claiming against the possibility of controlled abduction/adduction between claw and branch. Irrespective of the total number of leg pairs (63–129), the claws change gradually from pincer-like to usual shape invariantly in the range spanning between the 34 and the 45% of the total number of leg pairs. Despite these similarities, pincer-like claws originated independently in the three taxa, and by way of fundamentally different changes, either by the dramatic modification of the already existent anterior accessory spine (Diphyonyx, Neogeophilidae) or by the production of a novel cuticular projection (Eucratonyx). Moreover, their shared pattern of variation along the body was most probably constrained by already operating developmental processes controlling the longitudinal patterning of the trunk.     

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.     

Muscle and Muscle Fiber Type Transformation In Clawed Crustaceans

SYNOPSIS. The first pair of thoracic limbs in many crustaceansis elaborated into claws in which the principal muscle is thecloser. Changes in the fiber composition of the closer muscleduring claw development, regeneration and reversal are reviewedhere and the hypothesis is advanced that such changes are nerve-dependent.In adult lobsters, Homarus amencanus, the paired claws and closermuscles are bilaterally asymmetric, consisting of a minor orcutter claw with predominantly fast fibers and a small ventralband of slow and a major or crusher claw with 100% slow fibers.Yet in the larval and early juvenile stages the paired clawsand closer muscles are symmetric consisting of a central bandof fast fibers sandwiched by slow. Differentiation into a cutteror crusher muscle during subsequent juvenile development isby appropriate fiber type transformation. Experimental manipulationof the claws or the environment in early juvenile stages whenthe claws are equipotent revealed that the determination ofclaw and closer muscle asymmetry is dependent on the convergenceof neural input from the paired claws: the point of convergencemost likely being the CNS. Bilaterally symmetrical input resultsin the development of paired cutter claws while bilaterallyasymmetric input gives rise to dimorphic, cutter and crusherclaws. In the northern crayfish, Orconectes rusticus, wherethe paired claws are bilaterally similar, the closer muscletransforms its central band of fast fibers to slow, both duringprimary development and regeneration. Whether these fiber typetransformations are nerve-dependent is unknown. In adult snappingshrimps, Alpheus sp., the paired claws and closer muscles areasymmetric: the minor or pincer claw has a central band of fastfibers flanked by slow while the major or snapper claw has 100%slow fibers. Claw reversal occurs with removal of the snapperresulting in the transformation of the existing pincer to asnapper and the regeneration of a new pincer at the old snappersite. Transformation of the closer muscle from pincer to snappertype is by degeneration of the fast fiber band and hypertrophyof the slow fibers. Claw transformation can be either preventedif the pincer nerve is sectioned at the time of snapper removalor promoted if the snapper nerve is sectioned: both resultsimplicating a neural basis for muscle transformation.     

Using morphological characters of subfossil daphniid postabdominal claws to improve taxonomic resolution within species complexes

Daphnia subfossils from lake sediments are useful for exploring the impacts of environmental stressors on aquatic ecosystems. Unfortunately, taxonomic resolution of Daphnia remains is coarse, as only a small portion of the animal is preserved, and so the identification of daphniid subfossils typically relies upon postabdominal claws. Daphniid claws can be assigned to one of two species complexes: D. longispina or D. pulex. Both complexes contain species with differing environmental optima, and therefore improved taxonomic resolution of subfossil daphniid claws would aid paleolimnological analyses. To identify morphological features that may be used to help differentiate between species within complexes, we used species presence/absence data from net tows to select lakes in central Ontario (Canada) containing only a single species from a particular complex, then used remains preserved in surface sediments of these lakes to isolate four Daphnia species: D. ambigua and D. mendotae from the D. longispina complex, and D. pulicaria and D. catawba from the D. pulex complex. Our analyses demonstrate that, within the D. longispina complex, postabdominal claw length (PCL) and spinule length can be used to distinguish D. mendotae from D. ambigua. In addition, within the D. pulex complex, there are differences between D. pulicaria and D. catawba in the relative lengths of the proximal and middle combs on the postabdominal claw. However, the number of stout spines on the middle comb is an unreliable character for differentiating species. Overall, our data demonstrate that greater resolution within Daphnia species complexes is possible using postabdominal claws; however, the process is arduous, and applicability will likely decrease with the number of taxa present.     

Linking Laboratory and Field Approaches in Studying the Evolutionary Physiology of Biting in Bamboo Lemurs

A realistic understanding of primate morphological adaptations requires a multidisciplinary approach including experimental studies of physiological performance and field studies documenting natural behaviors and reproductive success. For primate feeding, integrative efforts combining experimental and ecological approaches are rare. We discuss methods for collecting maximum bite forces in the field as part of an integrated ecomorphological research design. Specifically, we compare maximum biting ability in 3 sympatric bamboo lemurs (Hapalemur simus, H. aureus, and H. griseus) at Ranomafana National Park, Madagascar to determine if biting performance contributes to the observed partitioning of a shared bamboo diet. We assessed performance by recording maximum bite forces via jaw-muscle stimulations in anesthetized subjects from each species. Behavioral observations and food properties testing show that the largest species, Hapalemur simus, consumes the largest and most mechanically challenging foods. Our results suggest that Hapalemur simus can generate larger bite forces on average than those of the 2 smaller species. However, the overlap in maximum biting ability between Hapalemur simus and H. aureus indicates that biting performance cannot be the sole factor driving dietary segregation. Though maximum bite force does not fully explain dietary segregation, we hypothesize that size-related increases in both maximum bite force and jaw robusticity provide Hapalemur simus with an improved ability to process routinely its more obdurate diet. We demonstrate the feasibility of collecting physiological, ecological, and morphological data on the same free-ranging primates in their natural habitats. Integrating traditionally laboratory-based approaches with field studies broadens the range of potential primate species for physiological research and fosters improved tests of hypothesized feeding adaptations.     

It takes two: Seasonal variation in sexually dimorphic weaponry results from divergent changes in males and females

Sexually dimorphic weaponry often results from intrasexual selection, and weapon size can vary seasonally when costs of bearing the weapon exceed the benefits outside of the reproductive season. Weapons can also be favored in competition over nonreproductive resources such as food or shelter, and if such nonreproductive competition occurs year‐round, weapons may be less likely to vary seasonally. In snapping shrimp (Alpheus angulosus), both sexes have an enlarged snapping claw (a potentially deadly weapon), and males of many species have larger claws than females, although females are more aggressive. This contrasting sexual dimorphism (larger weaponry in males, higher aggression in females) raises the question of whether weaponry and aggression are favored by the same mechanisms in males and females. We used field data to determine whether either sex shows seasonal variation in claw size such as described above. We found sexual dimorphism increased during the reproductive season due to opposing changes in both male and female claw size. Males had larger claws during the reproductive season than during the nonreproductive season, a pattern consistent with sexual selection. Females, however, had larger claws during the nonreproductive season than during the reproductive season—a previously unknown pattern of variation in weapon size. The observed changes in female weapon size suggest a trade‐off between claw growth and reproduction in the reproductive season, with investment in claw growth primarily in the nonreproductive season. Sexually dimorphic weaponry in snapping shrimp, then, varies seasonally due to sex differences in seasonal patterns of investment in claw growth, suggesting claws may be advantageous for both sexes but in different contexts. Thus, understanding sexual dimorphisms through the lens of one sex yields an incomplete understanding of the factors favoring their evolution.     

A new species of Tardigrada (Eutardigrada: Milnesiidae): Milnesium krzysztofi from Costa Rica (Central America)

Abstract

A new eutardigrade species Milnesium krzysztofi sp. nov. is described from Costa Rica. M. krzysztofi sp. nov. differs from the most similar Milnesium katarzynae Kaczmarek et al., 2004 mainly by the presence of spurs on internal claws I–III and on external claw IV.     

Gape and bite force in the rodents Onychomys leucogaster and Peromyscus maniculatus: Does jaw‐muscle anatomy predict performance?

Compared with the deer mouse, Peromyscus maniculatus, the grasshopper mouse, Onychomys leucogaster, exhibits modifications in its jaw‐muscle architecture that promote wide gapes and large bite forces at wide gapes to prey upon large vertebrate prey. In this study, we determine whether jaw‐muscle anatomy predicts gape and biting performance in O. leucogaster, and we also assess the influence of gape on bite force in the two species. Although O. leucogaster has an absolutely longer jaw, which facilitates larger gapes, maximum passive gape is similar in both species, averaging ～12.5 mm. Thus, when scaled to jaw length, O. leucogaster has a smaller maximum passive gape. These results suggest that predatory behaviors of O. leucogaster may not require remarkably large gapes. On the other hand, both absolute and relative bite forces exerted by O. leucogaster are significantly larger than those of P. maniculatus. The largest bite forces in both species occur at 5.0 mm of gape at the incisors, or 40% of maximum gape. Although bite force in both species decreases at larger gapes, O. leucogaster does maintain a larger percentage of maximum bite force at gapes larger than 40% of maximum passive gape. Therefore, although structural modifications in the masticatory apparatus of O. leucogaster may constrain gape, they may help to maintain bite force at large gapes. These results suggest that increases in gape differentially influence the length‐tension properties of the jaw muscles in the two species. Finally, these results highlight the importance of considering the effect of muscle stretch on force production in comparative studies of bite force. As a first approximation, it appears that gapes of 40–50% of maximum gape in rodents optimizes bite force production at the incisors. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Electrical properties and transmitter output associated with growth and transformation in shrimp muscle fibers

Summary Comparisons were made of the passive electrical properties of closer muscle fibers in the dimorphic claws of snapping shrimp,Alpheus armillatus. During claw transformation the small fibers of pincer claws grow to become much larger snapper claw fibers. As muscle fibers grow, the relationship of fiber input resistance (R ₀) to fiber diameter (d) is predicted by the proportionality,R ₀d ^–3/2. Muscle fiber membrane resistance,R _m, is independent of fiber diameter, but membrane capacitance,C _m, grows with diameter. This results in a 40 to 50 fold reduction in fiber input impedance as fiber diameter enlarges during transformation. Reductions of muscle fiber impedance are partially compensated by 2–5 fold increases in quantal content at excitatory synapses on snapper muscle fibers. However, changes in quantal content during transformation apparently are independent of fiber diameter per se. Excitatory junction potentials in both pincer and snapper muscle fibers have equal amplitude. Because fiber input impedance decreases precipitously during transformation, and in view of the relatively small compensatory changes in quantal content at excitatory synapses, additional pre- or post-synaptic modifications must supplement increased quantal content to maintain synaptic efficacy in transformed muscle fibers.Abbreviations ejp excitatory junctional potential - epp endplate potential - mepp miniature endplate potential