Flow visualisation and high speed video analysis of water jets in the snapping shrimp (Alpheus heterochaelis)

Snapping shrimp (Alpheus heterochaelis) produce a fast, well-focused water jet by rapid closure of their specialised snapper claw. As shown previously, water jets may injure the opponent in interspecific encounters (e.g. with small crabs) although no damage was observed in intraspecific encounters. For conspecific receivers the jet represents a potential hydrodynamic signal and can be analysed with the help of mechanosensory hairs. To gain more insight in the biophysical characteristics of the water jet we visualised and analysed jets of tethered snapping shrimp using standard and high speed video recordings. Water jet width increases with increasing distance from the snapper claw tip, and both width and distance increase with increasing snapper claw size. Water jet distances do not increase with increasing claw cocking duration (building up muscle tension) but medium cocking durations of about 550 ms result in longest distances. Mean water jet velocity is 6.5 m s⁻¹ shortly after claw closure but rapidly decreases subsequently. At the mean distance between snapping conspecifics (9 mm) water jet velocities produced by snapping shrimp with larger snapper claws are significantly higher than those of animals with smaller claws. Interestingly, males with equal snapper claw size as females produce significantly faster water jets. Accepted: 31 March 1999     

Snapping behaviour in intraspecific agonistic encounters in the snapping shrimp (Alpheus heterochaelis)

During intraspecific agonistic encounters in snapping shrimp (Alpheus heterochaelis) the behaviour of the snapper, emitting a fast water jet by very rapid closure of the large modified snapper claw, and the receiver was analysed by single frame video analysis before, during, and after the snap. During snapping the opponents usually face each other. Snapping is most frequently preceded by touch of frontal appendages. The snapping animal keeps its snapper claw slightly across the midline, shielding frontal body parts, and its tailfan bent downwards. The mean claw cocking duration (generating muscle tension) before snapping amounts to about 500 ms. In 58% of the snaps, the snapper claw pointed at the opponent, its claws, densely covered with sensory hairs, representing the main target of the water jet. The mean distance for these directed snaps was 0.9 cm, while undirected snaps were emitted from larger distances of on average 3.4 cm. The snapper usually withdraws immediately after snapping, the receiver approaches. Initial snaps are often answered by return snaps and both are emitted from smaller distances and hit more often than subsequent snaps.     

Post-autotomy claw regrowth and functional recovery in the snapping shrimp Alpheus angulosus

The ability to regenerate lost tissues, organs or whole body parts is widespread across animal taxa; in some animals, regeneration includes transforming a remaining structure to replace the one that was lost. The transformation of one limb into another involves considerable plasticity in morphology, physiology and behavior, and snapping shrimp offer excellent opportunities for studying this process. We examined the changes required for the transformation of the small pincer to a mature snapping claw in Alpheus angulosus. First molt claws differ from mature claws in overall shape as well as in morphology related to snapping function; nonetheless, shrimp with first molt claws do produce snaps. While most shape variables of second molt claws do not differ significantly from mature claws, the plunger (structure required for snap production) does not reach mature size until the third molt for females, or later for males. Thus, the pincer claw can be transformed into a functional snapping claw in one molt, although both the underlying morphology and superficial shape are not fully regenerated at this stage. The rapid production of a functional snapping claw that we observe in this study suggests that this particular function is of significant importance to snapping shrimp behavior and survival.     

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 comparative study by serial electron microscopy of neuromuscular junctions in the dimorphic claws of the snapping shrimp, Alpheus heterochelis

We compared the neuromuscular junctions on the main closer muscle in the first pair of chelipeds in the snapping shrimp Alpheus heterochelis by serial section electron microscopy. We sought an ultrastructural basis for the different behavioral and physiological functions of these dimorphic claws and for the role of the nervous system in claw transformation. We were unable to detect any statistically significant morphological differences between the junctions. Further, we found the muscle fiber populations and filament arrangements, as well as the electrical properties of the fibers, to be more homogeneous and similar to each other in A. heterochelis than those reported for another species, A. armillatus. We consider our results in light of recent data on the anatomy and electrical properties of the motor neurons within the CNS and conclude that the neural trigger for claw transformation involves factors not revealed by conventional electron microscopy.     

Reproductive strategy of the snapping shrimp Alpheus armillatus H. Milne-Edwards, 1837 in the South Atlantic: fecundity,egg features,and reproductive output

Summary

The family Alpheidae, composed by shrimps of relatively small size, popularly known as snapping shrimps, is the one of the most diverse decapod groups. These shrimps are found worldwide and occur in tropical and subtropical waters, from the intertidal zone to great depths. We investigated reproductive aspects of Alpheus armillatus, in order to gather information on egg production, aiming to enhance knowledge of its reproductive strategies in a population in an intertidal area of the South Atlantic. Ovigerous females were collected under rocks, in May and July 2006 (dry season) and in November 2006 and March 2007 (rainy season). Egg production and reproductive output were analyzed and compared seasonally and during the period of embryonic development. Females measured on average 11.28 mm CL, with a mean of 763 eggs and 0.10 mm3 egg volume. The egg volume of this population was smaller than previous estimates for other species of snapping shrimps, but the mean egg number was higher. The volume of eggs doubled during the incubation period, but despite this increase, no significant loss of eggs was observed. Alpheus armillatus invests on average about 12% of body weight in reproduction. The proportional investment in egg production is significantly higher in the rainy season when compared with the dry season (17.9% vs 4.8%), correlated with higher temperatures and increased food availability at this time. Our results corroborated the hypothesis of a pattern of egg production influenced by environmental conditions and intraspecific variability among the family Alpheidae, as a function of the biogeographic region.     

Evidence for three major clades within the snapping shrimp genus Alpheus inferred from nuclear and mitochondrial gene sequence data

The snapping shrimp genus Alpheus is among the most diverse of caridean shrimps, and analyses of taxa separated by the Isthmus of Panama have been used to estimate rates of molecular evolution. Although seven morphological groups have been informally suggested, no formal phylogenetic analysis of the genus has been previously attempted. Here we infer the phylogenetic relationships within Alpheus using sequence data from two nuclear genes, glucose-6-phosphate isomerase and elongation factor-1alpha, and from the mitochondrial gene cytochrome oxidase I. Three major clades corresponding to previously noted morphological features were identified. Discrepancies between earlier informal morphological groupings and molecular analyses largely consisted of species whose morphologies were not entirely typical of the group to which they had been assigned. The traditional placements of shrimp with highly sessile lifestyles and consequently simplified morphologies were also not supported by molecular analyses. Phylogenies for Alpheus suggest that specialized ecological requirements (e.g., symbiotic associations and estuarine habitats) and modified claw morphologies have evolved independently several times. These new analyses also support the sister species status of transisthmian pairs analyzed previously, although very similar pairs were not always resolved with the more slowly evolving nuclear loci. In addition, six new cryptic species were identified in the course of these studies plus a seventh whose status remains to be determined.     

Comparative Ecology of the Gobies <Emphasis Type="Italic">Nes longus</Emphasis> and <Emphasis Type="Italic">Ctenogobius saepepallens</Emphasis>, Both Symbiotic with the Snapping Shrimp <Emphasis Type="Italic">Alpheus floridanus</Emphasis>

Synopsis We re-examined the symbiotic association of the western Atlantic gobiid fishes Nes longus and Ctenogobius saepepallens with the snapping shrimp Alpheus floridanus on the basis of a critical literature review and new data. Our research confirms that N. longus interacts closely with the shrimp and is dependent on it for the cover provided by the burrow that the shrimp constructs; the goby serves as the sentinel at the burrow entrance. Ctenogobius saepepallens is often seen occupying a burrow of the alpheid, and the shrimp will leave the burrow to deposit sediment with the goby at the entrance, even pushing the goby aside at times. However, the shrimp does not make contact with the goby with its antennae, nor does the goby communicate with caudal fin fluttering at the approach of danger. We suggest that their relationship is a first step in an evolutionary process that may lead to the very close mutualistic association exhibited by N. longus and the alpheid, as well as Indo-Pacific shrimp gobies of 13 different genera and their alpheid partners. Nes longus remains close to the burrow entrance; it feeds mainly on small gastropods, decapod crustaceans, ostracods, and isopods. By contrast, C. saepepallens makes longer excusions from the shelter of the burrow; its diet is dominated by benthic copepods, followed by ostracods and lesser amounts of foraminiferans, isopods, and decapod crustaceans. By virture of its greater mobility, it can be more selective in its prey.     

Composition of external setae during regeneration and transformation of the bilaterally asymmetric claws of the snapping shrimp,Alpheus heterochelis

The paired thoracic chelipeds or claws of adult snapping shrimp, Alpheus heterochelis, are bilaterally asymmetric, consisting of an enlarged and elaborate, sound-producing major (snapper) claw and a much smaller minor (pincer) claw. These paired claws vary in the composition of their external sensilla. Both possess long serrulate and simple short setae but the snapper also have plumose setae and long serrulate setae on the plunger. The pincers differ in having short serrulate setae and, in males alone, a prominent fringe of plumoserrate setae. During regeneration of each claw type, these setal structures are gradually added over three molts to reach the pristine condition. The long serrulate and simple short setae appear first, being seen in intermolt limb buds and commonly in both claws. Setae exclusive to each claw, i.e., plumoserrate and short serrulate in the pincer and plumose and long serrulate on the plunger in the snapper, appear sparsely in either the regenerated 1st or 2nd postmolt claw, they proliferate in the subsequent 2nd or 3rd postmolt claw. Transformation of the pincer claw to the snapper type begins in the 1st postmolt stage with the loss of pincer setae and addition of snapper setae and is completed by the 3rd postmolt stage. Since changes in composition of the external sensilla are restricted to postmolt stages, the underlying hypodermis is presumably being remodeled during proecdysis.     

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.     

Morphological Variation of the Forelimb and Claw in Neotropical Sigmodontine Rodents (Rodentia: Cricetidae)

The limbs of mammals exhibit a variety of morphologies that reflect the diversity of their habitats and their functional needs, including subtle structural differences in their distal limb integumentary appendages (hooks, claws, adhesive pads). Little is known about structure and function of claws of sigmodontine rodents. Here, we analyze claw shape and forelimb skeleton morphology of 25 species of sigmodontine rodents with different locomotory types (ambulatory, fossorial, natatorial, quadrupedal saltatorial, and scansorial), taking into account their phylogenetic affinities. Qualitative differences in claw shape were examined using digital photographs, and quantitative measurements were made for length, height, and curvature of the claws of all digits, and dimensions of other forelimb skeletal elements. Our results show that both phylogeny and ecological categories explain substantial components of the morphological variation in sigmodontine rodents. Qualitative analysis reveals that non-specialized forms (ambulatory, quadrupedal saltatorial, and scansorial) tend to have high and strongly curved claws, whereas highly specialized forms (fossorial and natatorial) tend to have elongate and smoothly curved claws. However, the quantitative analysis differentiated the fossorial and scansorial by variables related to claw, and natatorial by variables related to bones of the forelimb. No variables that could differentiate ambulatory or quadrupedal saltatorial forms were found, demonstrating that these forms show a generalized morphological pattern. This study indicates that both historical and ecological factors contribute to the evolution of claw length in these groups.     

Specialized shell-breaking crab claws in Cretaceous seas

Here we report on a large brachyuran crab species from the Late Cretaceous of Mexico that has claws indicative of highly specialized shell-breaking behaviour. This crab possessed dimorphic claws (the right larger than the left), armed with several broad teeth, including a curved tooth structure found at the base of the movable finger of the right claw. The curved tooth is similar to the one observed on claws of many living durophagous crabs that use it as a weapon to peel, crush or chip the edges of hard-shelled prey, particularly molluscs. These morphological traits suggest that specialized shell-breaking crab predators had evolved during the Cretaceous, which contradicts previous findings supporting an Early Cenozoic origin for specialized shell crushers within the brachyuran clade.     

Muscle Restructuring in Crustaceans: Myofiber Death, Transfiguration and Rebirth

Research on the dimorphic claws of the snapping shrimp Alpheushas revealed moult-associated changes in structure and biochemicalcomposition—including atrophy and biochemical modification—ofclaw muscle fibers during morphological transformation of aclaw from a pincer to a snapper. Electrophysiology, SDS-PAGEgel electrophoresis, and immunocytochemistry were used to analyzechanges in claw closer muscle function and composition duringthe transformation process. Remodification of closer muscleduring claw transformation, involving the complete loss of acentral section of fast-contracting fibers and their replacementthrough enlargement of existing slowly-contracting segmentsof the muscle, may mimic similar muscle modifications duringinitial claw development. Exposure of intact animals to environmentalecdysteroid hormones accelerated the rate of these changes.These processes appear to be a product of a remarkable trophicplasticity of crustacean skeletal muscle first discovered bySkinner.     

Characterization and comparison of the mitochondrial genomes from two Alpheidae species and insights into the phylogeny of Caridea

The mitochondrial genome (mitogenome) has been widely used in phylogenetics and molecular evolution as a parameter, due to its simple genetic structure, high evolutionary rate, and compositional heterogeneity properties. Alpheidae is a large and highly diverse family of the Caridea infraorder, currently containing about 600 species dispersed all over the world. However, only a few shrimps in Alpheidae have their complete mitogenome annotated in GenBank. In our study, the entire mitogenomes of two shrimps from Alpheidae were determined, Alpheus randalli and Alpheus bellulus. The mitogenomes of both shrimps share the complete set of 37 mitochondrial genes found in other Alpheidae species. In A. randalli the AT-skew is slightly positive and GC-skew is negative, whereas in A. bellulus the AT-skew is negative and GC-skew is slightly positive. Furthermore, the secondary structures of trnS1 in the two shrimps are partially missing, and another three tRNAs formed the typical cloverleaf shaped secondary structures. Also, the trnS1 of A. randalli has an unusual anticodon stem with some unpaired nucleotides. Comparative genomic analysis suggests that the mitochondrial gene order of Alpheus genus exhibits a different gene rearrangement compared with that of Caridea. Most species in Alpheus share the same gene order, except for A. lobidens, which has an additional pseudogenomic trnQ (trnQ*). Compared with the mitochondrial gene order of Caridea the Alpheus trnE underwent both translocation and inversion, which were caused by a recombination event. Bayesian inferences (BI) and Maximum Likelihood (ML) phylogenetic analyses of 105 species amino acid datasets resulted in a well-supported topology, whereas four families in Caridea are monophyletic and can be divided into two major clades. Moreover, we demonstrated the phylogenetic relationships of six infraorders in Decapoda (Dendrobranchiata, (Caridea, (Stenopodidea, (Achelata, (Polychelida, Astacidea))))). This study used the large taxon sampling available to date for phylomitogenomic analysis. The results provide a theoretical basis for further research on the evolution of the Decapoda order, specifically Caridea infraorder.     

Evolution of the morphological innovations of feathers

Feathers are complex assemblages of multiple morphological innovations. Recent research on the development and evolution of feathers has produced new insights into the origin and diversification of the morphological innovations in feathers. In this article, I review and discuss the contribution of three different factors to the evolution of morphological innovations in feathers: feather tubularity, hierarchical morphological modularity, and the co-option molecular signaling modules. The developing feather germ is a tube of epidermis with a central dermal pulp. The tubular organization of the feather germ and follicle produces multiple axes over which morphological differentiation can be organized. Feather complexity is organized into a hierarchy of morphological modules. These morphological modules evolved through the innovative differentiation along multiple different morphological axes created by the tubular feather germ. Concurrently, many of the morphological innovations of feathers evolved through the evolutionary co-option of plesiomorphic molecular signaling modules. Gene co-option also reveals a role for contingency in the evolution of hierarchical morphological innovations.     

Evolutionary Trends of External Morphology in the Marine Mite Genus Rhombognathides (Acari: Halacaridae: Rhombognathinae)

A morphology-based phylogenetic analysis of the eight species of Rhombognathides (Acari: Halacaridae) demonstrated some evolutionary tendencies of character transformation. In the course of the evolution of Rhombognathides, idiosomal plates increased in size or fused. Simple filiform setae transformed into spiniform or bipectinate setae. The number of tarsal claws, the length of median claw and leg chaetotaxy of telofemora and tibiae were reduced. The fusion or expansion of dorsal plates, transformation from filiform to other setal forms, and reduction of leg setae would have recurrently occurred in halacarid evolution. The claw structure most likely reflects adaptation to specific habitat.     

Locomotion and adhesion: dynamic control of adhesive surface contact in ants

Tarsal adhesive pads of insects are highly dynamic organs that play an important role in locomotion. Many insects combine fast running performance with strong resistance to detachment forces. This capacity requires an effective control of attachment forces at the tarsus and pretarsus. Here we investigate mechanisms of attachment control in Asian weaver ants (Oecophylla smaragdina) by measuring the dynamics of the adhesive contact area and the claws during locomotion. O. smaragdina ants walking upside down on a smooth substrate used only a fraction (approx. 14%) of their maximum possible contact area. When these ants were loaded with 30 mg weights (corresponding to approx. 6 times their own body weight), however, they employed much larger (but still submaximal; approx. 60%) contact areas. The increase of contact area was accompanied by a stronger flexion of the claws, which demonstrates the participation of the claw flexor muscle in the control of adhesive contact. However, only part of the contact area dynamics could be explained by the action of the claw flexor. During the stance phase, adhesive contact area changed while the claws remained motionless. Even when corrected for the effects of claw flexion, adhesive contact areas differed by a factor of 2.1 between loaded and unloaded ants. Our findings give evidence that running ants control their adhesive contact area by a combination of active movements of the claw flexor muscle and passive reactions of the mechanical system.     

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.     

Arboreallty and morphological evolution in ground beetles (Carabidae: Harpalinae): testing the taxon pulse model

Abstract.— One-third to two-thirds of all tropical carabids, or ground beetles, are arboreal, and evolution of arboreality has been proposed to be a dead end in this group. Many arboreal carabids have unusual morphological features that have been proposed to be adaptations for life on vegetation, including large, hemispheric eyes; an elongated prothorax; long elytra; long legs; bilobed fourth tarsomeres; adhesive setae on tarsi; and pectinate claws. However, correlations between these features and arboreality have not been rigorously tested previously. I examined the evolution of arboreality and morphological features often associated with this habitat in a phylogenetic context. The number and rates of origins and losses of arboreality in carabids in the subfamily Harpalinae were inferred with parsimony and maximum-likelihood on a variety of phylogenetic hypotheses. Correlated evolution in arboreality and morphological characters was tested with concentrated changes tests, maximum-likelihood, and independent contrasts on optimal phylogenies. There is strong evidence that both arboreality and the morphological features examined originated multiple times and can be reversed, and in no case could the hypothesis of equal rates of gains and losses be rejected. Several features are associated with arboreality: adhesive setae on the tarsi, bilobed tarsomeres, and possibly pectinate claws and an elongated prothorax. Bulgy eyes, long legs, and long elytra were not correlated with arboreality and are probably not arboreal adaptations. The evolution of arboreal carabids has not been unidirectional. These beetles have experienced multiple gains and losses of arboreality and the morphological characters commonly associated with the arboreal habitat. The evolutionary process of unidirectional character change may not be as widespread as previously thought and reversal from specialized lifestyles or habitats may be common.