Pincer Claw Research Articles

Plasticity of external setae during claw transformation in the snapping shrimp, Alpheus angulosus McClure, 2002 (Decapoda, Caridea)

The snapping shrimp,Alpheus angulosusMcClure, 2002, is a small crustacean with bilaterally asymmetric claws that serve distinct behavioural and sensory functions. If the large claw is lost, the organism switches handedness, transforming its small pincer claw into a large snapping claw while simultaneously developing a small claw on the contralateral side. To better understand the mechanisms required to adapt to this radical change in body composition, we examined developmental plasticity by tracing changes in sensory setae distribution on the claws throughout transformation. We observed only two broad types of setae, simple and plumose. Quantitative analysis across molt stages revealed significant alterations in setae composition and numbers that occurred primarily on the edge of the propodus, where the most drastic morphological changes also occur. These results suggest that previous developmental mechanisms are re-engaged to support the proliferation and differentiation of new setae during transformation.

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.

Claw Transformation and Regeneration in Adult Snapping Shrimp: Test of the Inhibition Hypothesis for Maintaining Bilateral Asymmetry.

In the paired asymmetric claws of adult snapping shrimp, Alpheus heterochelis, the minor, or pincer, claw may transform into a major, or snapper, claw if the existing snapper claw is damaged or lost, implying that an intact snapper claw normally inhibits the contralateral pincer claw from advancing to a snapper. We find that the pincer-to-snapper advancement in external form occurs almost immediately after the snapper is lost even as late as the premolt stage. The transforming claw in turn inhibits the newly regenerating pincer claw from becoming a snapper, but if the dactyl of the transforming claw is cut, then snapper-based inhibition is removed and the contralateral claw may regenerate as a snapper, resulting in shrimp with paired snapper claws. However, damaging an established snapper claw will not allow another snapper claw to regenerate at the pincer site, implying that less inhibition is required to restrict a newly regenerating claw to a pincer than to arrest an existing pincer claw. Inhibition may be manifested largely in terms of quantity of innervation. Hence the greater innervation of the snapper side over the pincer side would inhibit the pincer side, accounting for the regeneration of paired claws in their previous configuration following loss of both claws. Loss of the paired claws in two consecutive molts retards their development so that both claws often appear as pincers, but in succeeding molts one usually differentiates into a snapper and bilateral asymmetry is restored. In contrast, shrimp with paired snapper claws retain this configuration over several molts unless one or both of the claws are lost; in that case, regeneration restores bilateral asymmetry. Thus, bilateral asymmetry of the paired claws of adult shrimp is governed by a strong intrinsic lateralizing mechanism in which the snapper claw inhibits the pincer from advancing to another snapper.

Regeneration and sex-biased transformation of the sexually dimorphic pincer claw in adult snapping shrimps

Adult snapping shrimps Alpheus heterochelis have paired asymmetric claws, a large snapper which is similar in the sexes, and a much smaller pincer which is sexually dimorphic. The male pincer is slightly more hypertrophied compared to the female and therefore intermediate in size between the female pincer and the snapper. This has led to the suggestion that female pincer, male pincer and snapper represent a continuum in claw development. To test this possibility we examined regenerating snappers and found them to pass through a pincer-like stage in both sexes. In males they transiently possess the pincer-characteristic setose fringe. As well, the regenerating closer muscle shows a band of fast fibers reminiscent of the pincer closer muscle in both sexes. Since the male pincer more closely resembles the snapper in external and internal morphology than the female pincer, its transformation to a snapper may be more easily precipitated. To test this possibility we cut the snapper dactyl and this triggered transformation of the pincer to a snapper in 84% of male shrimps but only in 28% of female shrimps. During the intermolt in which the snapper dactyl is cut, axon numbers on the pincer side exceeded those on the snapper side in males but not in females. Since this shift in axon numbers favoring the pincer side occurs well before the pincer transforms to a snapper at the next molt it may signal transformation. J. Exp. Zool. 279:356–366, 1997. © 1997 Wiley-Liss, Inc.

Regeneration and sex‐biased transformation of the sexually dimorphic pincer claw in adult snapping shrimps

Regeneration and sex‐biased transformation of the sexually dimorphic pincer claw in adult snapping shrimps

Neural factors influence the degeneration of muscle fibers in the chelae of snapping shrimps.

The asymmetric pincer and snapper claws in the snapping shrimp differ in external morphology and musculature. The snapper is a massive claw used for displays and defense; the pincer is small and slender, used for feeding and burrowing. The snapper has only slow muscle fibers; the pincer has both slow and fast. Removal or denervation of the snapper claw induces transformation of the contralateral pincer to a snapper type of claw at the subsequent molt. A removed claw regenerates as a pincer type, as long as the innervation of the remaining claw is intact. Fast muscle fibers, found exclusively in the pincer claw, normally degenerate completely within 10 d after the moult, which transforms the pincer to a snapper. Morphological transformation of the pincer following removal of the snapper claw can occur even if the pincer claw is denervated. Denervation of the pincer, however, delays degeneration of the fast fibers, increasing the estimated half-time of muscle degeneration, for 4.4 +/- 0.2 to 19.5 +/- 0.8. d after the transforming moult. Neural influences therefore are involved both in the determination of the morphology of the claw and in the induction of degenerative changes during the remodeling of an existing claw.

Establishment and maintenance of claw bilateral asymmetry in snapping shrimps

AbstractThe paired asymmetric chelae, or claws, in snapping shrimps, Alpheus heterochelis, differ in form and function; the major, or snapper, claw is grossly enlarged, has a hammer and socket, and functions in agonistic displays, while the minor, or pincer, claw is small and slender and functions in burrowing and feeding. The paired claws are symmetrical and undifferentiated in the larval and early juvenile stages but differentiate on a random basis into a snapper and a pincer claw by the sixth juvenile stage. Removal of one of the paired claws in the third or fourth juvenile stage results in the intact claw developing into a snapper, suggesting that differential use initially determines claw type. However, claw bilateral asymmetry may be altered in adults as removal of the snapper claw causes transformation of the existing pincer into a snapper while a new pincer regenerates at the old snapper site. To test the hypothesis that inhibitory influences from the transforming pincer‐to‐snapper claw may limit the newly regenerating claw to a pincer type, we observed the effects of closer muscle tenotomy and nerve lesions in the intact transforming claw on the type of claw regenerated at the old snapper site. With mild tenotomy in which the tendon is cut at its attachment to the moveable dactyl but the closer muscle and its innervation is otherwise intact, a pincer claw regenerates similar to the control animals. However, with radical tenotomy in which the tendon is removed from the claw and the closer muscle and its innervation is severely disrupted, either a pincer or snapper claw regenerates. Lesioning of the large nerve 2 by itself or together with the small nerve 1 (but not nerve 1 by itself) in the intact transforming claw also permits regeneration of either a pincer or snapper claw at the old snapper site. Thus, neural influences from the transforming pincer‐to‐snapper claw restrict regeneration of the contralateral claw to a pincer type thereby ensuring bilateral asymmetry in adult shrimps. © 1994 Wiley‐Liss, Inc.

Muscle remodeling in adult snapping shrimps via fast-fiber degeneration and slow-fiber genesis and transformation

Bilateral asymmetry of the paired snapper/pincer claws may be reversed in adult snapping shrimps (Alpheus heterochelis). Removal of the snapper claw triggers transformation of the contralateral pincer claw into a snapper and the regeneration of a new pincer claw at the old snapper site. During this process the pincer closer muscle is remodeled to a snapper-type, and these alterations have been examined with the electron microscope. There is selective death of the central band of fast fibers, accompanied by an accumulation of electron-dense crysttaline bodies in the degenerating fibers. Two principal types of hemocytes (amebocytes and coagulocytes) invade the area and the degenerating muscle fibers. New myotubes also appear in this central site. The myotubes are characterized by a prolific network of presumptive sarcoplasmic reticulum and transverse tubules, nascent myofibrils, and crystalline bodies. The myotubes are innervated by many motor nerve terminals, and they subsequently differentiate into long-sarcomere (8–12 μm), slow muscle fibers. Remodeling of the central band, therefore, occurs by degeneration of the fast fibers and their replacement by new slow fibers. Remnants of the degenerating fast fibers act as scaffolding for the myotubes which originate from adjacent satellite cells. The crystalline bodies may represent protein stores from the degeneration of the fast fibers, recycled for use in the genesis of new fibers. The invading hemocytes appear to play several roles, initially phagocytosing the fast muscle fibers, transporting the crystalline bodies into the new myotubes, and acting as stem cells for the new muscle fibers. Apart from the central band of fibers, the remaining pincer-type slow fibers with sarcomere lengths of 5–7 μm are transformed via sarcomere lengthening into snapper-type slow fibers with sarcomere lengths of 7–12 μm. Thus, during claw transformation in adult snapping shrimps, the pincer closer muscle is remodeled into a snapper closer muscle by selective death of the fast-fiber band, replacement of the fast-fiber band by new slow fibers, and transformation of the existing slow fibers to an even-slower variety.

Regenerate Limb Bud Sufficient for Claw Reversal in Adult Snapping Shrimps.

The paired, bilaterally asymmetric snapper and pincer claws in the adult snapping shrimp Alpheus heterochelis were simultaneously autotomized at the beginning of an intermolt, and the resulting growth of the limb buds was characterized into several stages. At the next molt the limb buds emerged as newly regenerated claws of the same morphotype as their predecessors. Next, the paired claws were autotomized sequentially, with the second autotomy timed to different stages of limb bud growth at the first autotomy site. When the snapper is autotomized and a limb bud varying from stages 1 to 5 is allowed to develop at this site before the pincer is removed, the paired claws regenerate in their previous configuration. Similarly, claw asymmetry is retained when the pincer claw is removed first and an early limb bud (stage 1-2) is allowed to form at this site before the snapper is autotomized. However, claw asymmetry is reversed if an advanced limb bud (stage 3-5) is allowed to form at the pincer site before the snapper claw is removed. Under these conditions a snapper regenerates at the pincer site and a pincer at the snapper site. Because the limb bud at this pincer site regenerates as a snapper rather than a pincer, claw transformation has occurred, with the stage 3-5 limb bud substituting for an intact pincer. Therefore, the minimal requirement for pincer-to-snapper transformation is a stage 3-5 limb bud. We postulate that the newly transforming snapper claw restricts regeneration at the contralateral old snapper site to a pincer, thereby ensuring that claw bilateral asymmetry is present, albeit reversed.

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.

Muscle and Muscle Fiber Type Transformation In Clawed Crustaceans

SYNOPSIS. The first pair of thoracic limbs in many crustaceans is elaborated into claws in which the principal muscle is the closer. Changes in the fiber composition of the closer muscle during claw development, regeneration and reversal are reviewed here and the hypothesis is advanced that such changes are nerve-dependent. In adult lobsters, Homarus amencanus , the paired claws and closer muscles are bilaterally asymmetric, consisting of a minor or cutter claw with predominantly fast fibers and a small ventral band of slow and a major or crusher claw with 100% slow fibers. Yet in the larval and early juvenile stages the paired claws and closer muscles are symmetric consisting of a central band of fast fibers sandwiched by slow. Differentiation into a cutter or crusher muscle during subsequent juvenile development is by appropriate fiber type transformation. Experimental manipulation of the claws or the environment in early juvenile stages when the claws are equipotent revealed that the determination of claw and closer muscle asymmetry is dependent on the convergence of neural input from the paired claws: the point of convergence most likely being the CNS. Bilaterally symmetrical input results in the development of paired cutter claws while bilaterally asymmetric input gives rise to dimorphic, cutter and crusher claws. In the northern crayfish, Orconectes rusticus , where the paired claws are bilaterally similar, the closer muscle transforms its central band of fast fibers to slow, both during primary development and regeneration. Whether these fiber type transformations are nerve-dependent is unknown. In adult snapping shrimps, Alpheus sp., the paired claws and closer muscles are asymmetric: the minor or pincer claw has a central band of fast fibers flanked by slow while the major or snapper claw has 100% slow fibers. Claw reversal occurs with removal of the snapper resulting in the transformation of the existing pincer to a snapper and the regeneration of a new pincer at the old snapper site. Transformation of the closer muscle from pincer to snapper type is by degeneration of the fast fiber band and hypertrophy of the slow fibers. Claw transformation can be either prevented if the pincer nerve is sectioned at the time of snapper removal or promoted if the snapper nerve is sectioned: both results implicating a neural basis for muscle transformation.

Spontaneous generation of bilateral symmetry in the paired claws and closer muscles of adult snapping shrimps

Abstract Adult snapping shrimps Alpheus heterochelis (Say) have paired asymmetric claws consisting of a major or snapper claw and a minor or pincer claw. An unusual condition of bilateral symmetry consisting of paired snapper claws arose spontaneously in several snapping shrimps by transformation of the pincer to a snapper in the presence of an existing contralateral snapper claw. Transformation in the external morphology and fibre composition of the closer muscle was completed within two intermoult periods in the majority of cases where true symmetry was achieved and once established became permanent. Thus snapping shrimps, which are by nature solitary, when continually exposed to each other in the laboratory may transform their pincer to a snapper without any trauma to the existing snapper claw.

Selective degeneration of fast muscle during claw transformation in snapping shrimps

The closer muscle in the paired asymmetric claws of adult snapping shrimp Alpheus heterochelis is composed of 100% slow fibers in the major or snapper claw and a central band of fast fibers flanked by slow in the minor or pincer claw. Removal of the snapper claw induces the existing pincer to transform over the next several molts into a snapper. During this process there is a selective degeneration of the central band of fast fibers in the transforming closer muscle.

Neuromuscular relationships during claw regeneration in Californian snapping shrimp.

We have examined the innervation patterns of the two excitor axons to the closer muscle in the dimorphic (snapper and pincer) claws of Californian snapping shrimp (Alpheus californiensis). In both claws the fast-closer excitor (FCE) axon supplies all of the closer muscle fibers. The slow-closer excitor (SCE) axon, however, makes functional connections only with fibers on the dorsal and ventral margins, which are composed of slow-type fibers in the large snapper claw and of intermediate-type fibers in the smaller pincer claw. The central band of fast fibers in the pincer closer muscle is not innervated by the SCE. During claw regeneration, the closer muscle is initially composed of a population of fast fibers in the pincer and intermediate-type fibers in the snapper. The innervation patterns of the two excitatory motor axons in regenerating claws at this stage are the same as in fully developed claws. During the first intermolt period some fast-closer muscle fibers in the pincer claw differentiate into intermediate-type fibers, but the axon innervation patterns do not change. If the correlation between SCE axon innervation pattern and the regional distribution of different muscle fiber types is indicative of nerve-muscle interactions, the present data suggest that the trophic influence must proceed from nerve to muscle.

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

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 (R0) to fiber diameter (d) is predicted by the proportionality,R0∝d−3/2. Muscle fiber membrane resistance,Rm, is independent of fiber diameter, but membrane capacitance,Cm, 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.

Neuromuscular relationships in the asymmetric claws of Californian snapping shrimp

AbstractThe asymmetric claws of Californian snapping shrimp (Alpheus californiensis) are comprised of a smaller pincer claw and a larger snapper claw. The present paper describes the morphology of the single closer muscle and the facilitation properties of an excitatory motor axon for both claws. In the snapper claw the closer muscle fibers are composed of uniformly long sarcomeres, measuring 10–15 μm in length. In the pincer the closer muscle fibers are of a smaller diameter and can be divided into two groups on the basis of sarcomere length. One group has short (2 and 3 μm) sarcomeres, while the other has intermediate (7 and 8 μm) sarcomeres. Microelectrode recordings from single closer muscle fibers showed that all fibers are supplied by the fast excitatory motor axon. The slow excitatory motor axon innervates only fibers on the dorsal and ventral surfaces of the closer muscle. Facilitation of excitatory junctional potentials (ejps), produced by stimulation of the fast axon with pairs of brief electrical shocks, revealed that at intervals above 100 ms no facilitation was recorded from either claw. At intervals below 100 ms, however, facilitation was recorded from pincer closer muscle fibers, but defacilitation or depression was recorded from the snapper. This was confirmed by making extracellular recordings of synaptic potentials from snapper closer muscle fibers.

Actomyosin components of the asymmetric claw closer muscles of californian snapping shrimp

AbstractThe dimorphic claws of the Californian snapping shrimp, Alpheus californiensis, contain an opener and a closer muscle. The closer muscle in the smaller pincer claw is composed of fibers with short and intermediate sarcomere lengths, whereas the closer muscle in the larger snapper claw is composed of fibers with long sarcomeres. Electrophoretic analysis of actomyosin extracts from the closer muscle in each claw revealed some common components. However, the snapper contains two additional components with molecular weights of 25 and 100 daltons.

REGIONAL DISTRIBUTION OF MUSCLE FIBER TYPES IN THE ASYMMETRIC CLAWS OF CALIFORNIAN SNAPPING SHRIMP

The properties of the opener and closer muscles in the asymmetric claws of Alpheus californiensis have been investigated using sarcomere length measurements and histochemical techniques. In the smaller pincer claw two types of muscle fibers are regionally distributed within the single closer muscle. A central band of fibers have short (2.5 µm) sarcomeres and high myofibrillar ATPase activity. Intermediate-type fibers have smaller diameters, sarcomeres 8.5 to 9 µm in length and low myofibrillar ATPase activity. The snapper closer muscle, by contrast, is composed of fibers with long (11-14 µm) sarcomeres and low myofibrillar ATPase activity. Opener muscle fibers in the pincer claw have shorter sarcomere lengths than their counterparts in the snapper claw.

Modification of motor neuron size and position in the central nervous system of adult snapping shrimps

Cell bodies of claw closer motor neurons in snapping shrimp are dimorphic. Snapper claw motor neurons are larger than corresponding pincer claw motor neurons, but the relative sizes of these cells are reversed during claw transformation. An additional neuronal modification occurs early within this period, in that the pincer claw dorsal inhibitor cell body migrates within the nervous system, from a dorsal to a ventral position. These findings are evidence of rapid, reversible changes in the nervous system following the trigger for the transformation process.

The motor organization of claw closer muscles in snapping shrimp

1. The motor supply to the closer muscles of the snapper and pincer claws in alpheid shrimp was examined using electrical stimulation and recording techniques. Closer muscles of both claws are innervated by two excitatory and two inhibitory axons. Details of the relative distribution of the two excitatory axons to both sets of closer muscle fibers in each claw are similar. 3. Properties of synaptic transmission at the neuromuscular junction in the pincer claw resemble those in developing or regenerating muscle, with frequent failures and fluctuating ejp amplitudes. 4. We conclude that gross reorganization of claw motor innervation does not occur during the phenomenon of pincer-snapper transformation. Moreover the developmentally primitive state of neuromuscular transmission in the pincer provides a clue to possible control mechanisms in the transformation of the closer muscle.