Neurobehavioral Mechanisms and Biomechanics are Inseparable

Tailfan skeleton musculature, tailflip behaviors, and MG and LG neurons are interrelated. Before plunging into the analysis of any central nervous system, the machinery that the particular nervous system operates must be considered. For example, cephalo-pod mollusks have excellent visual capabilities and manipulative skills, as do humans, but our brain in an octopus would be as helpless in controlling

Hippid

Hippid

Albuneid

Leg 2

Leg 3

Backward walking

Backward walking

Leg 4

Uropod beating

Uropod beating

Nongiant swimming

Forward walking

Nongiant swimming

Leg 2

Leg 3

Leg 2

Leg 3

Backward walking

Leg 4

Backward walking

Forward walking

Figure 4 The mosaic ancestry of sand crab digging behaviors. Limb movements of hippids (a, c) and albuneids (d). The movements and motor patterns of the second and third digging legs resemble those used by other decapods to walk backward, while those of the fourth legs resemble patterns for forward walking in other species. a, Hippid uropods cycle in the same, bilaterally synchronous pattern during swimming and digging, but during digging the three pairs of digging legs also move rhythmically. The fourth legs cycle in the same direction as the uropods, whereas the second and third pairs cycle in the opposite direction (curved arrows). b, The coordination between the cycling of left (solid box) and right (open triangle) fourth legs with respect to the uropod period changes during the course of a dig according to the frequency of uropod beating (data are onset of electromyograms bursts recorded from unrestrained animals). The fourth legs move in unison and in antiphase to the uropodsatthe beginning of a dig (time 1), and drift apart when overall frequency drops until they are cycling about one-third of a cycle out of phase with each other and the uropods (time 2). Inset: position at start of dig, above (1) and when submerged below (2) surface of sand (horizontal line). c and d, Summary diagram of the neural organization of digging in hippid (c) and albuneid (d) sand crabs. The evolutionary change in coordination between limb CPGs (central pattern generators) was greater than in the CPGs themselves (see character 12 in Figure 2). Adapted from Faulkes and Paul (1997a, 1997b, 1998); see also Paul etal. (2002).

tentacle movements as octopus motor circuitry would be in controlling our hands and feet. What skeletal-muscular requirements must be met for a decapod crustacean to be able to swim with the uropods?

1.07.3.1 Hinged versus Single-Pivot Joints

Two basic requirements for generating propulsive force with any limb that functions as a lever are a basal joint that allows limb movement through a sufficiently large arc and musculature capable of generating powerful movement of the limb through its full trajectory while providing stabilization against counter forces. Arthropod joints are typically double hinged, with movement restricted to one plane. The uropod has just one articular point with abdominal segment 6, but in most decapods this joint is so deeply recessed between the telson and the sixth segment that elevation of the propo-dite (the basal segment of the uropod) above the horizontal plane is impossible and protraction and retraction in the horizontal plane are severely restricted. The joint does, however, allow uropod depression, which results in cupping of the tailfan (Figure 1b2). Hippids, by contrast, have evolved a 'socket-and-ball' uropod joint with the sixth segment that is biomechanically analogous to a vertebrate ball-and-socket joint (Figure 5d; Paul et al., 1985). This allows the uropod propodite to be swung through large arcs nearly comparable to the range of motion of the human shoulder joint. Hippids swim exclusively with the equivalent of a human swimmer's backstroke.

Figure 5 The divergence of telson musculature in Hippidae from that typical of the decapod telson is so extreme that no specific homologies can be suggested by visual inspection alone; analysis of the innervation is required. a, Ventral views of the tailfans of E. analoga (left) and crayfish (right) show the most ventral muscles in place on the left and removed on the right. Note that all of the telson muscles in E. analoga arise from broad areas of the inner dorsal telson and insert directly on the uropod propodite via discrete tendons. This is in marked contrast to crayfish, where nearly all of the muscles in the telson are the terminal elements of the series of abdominal fast flexor muscles, and all insert on or are linked to the flexor tendon in the posterior-lateral abdominal segment 6, which, in turn, is linked to the ventral side of the uropod. The fibers of the trio of relatively small telson-uropod muscles in crayfish (only PTU labeled) insert directly, without tendons, over the proximal ventral surface of the propodite, but are attached to the dorsal-anterior telson via a slender tendon, which is bound to the flexor tendon by connective tissue. b and c, The modifications of conserved telson muscles (blue), loss of an ancestral muscle (orange), and appearance of a new muscle (green) in the anomalen species were discovered by inspection of the tailfans of two anomalen species that continue to tailflip, B. occidentalis and M. quadrispina (Paul etal., 1985; Paul, 1991; Wilson and Paul, 1987). The ventral (blue) muscles are removed from one side to expose the deeper/more dorsal muscles. b, E. analoga (Hippidae, left) compared with crayfish (right; the inset shows a more dissected view to reveal the three telson-uropod muscles attached to the dorsal telson by a single tendon, left side; the area of attachment of AT muscle fibers (orange oval), right side. c, B. occidentalis (Albuneidae, left), M. quadrispina (Galatheidae, middle). Muscle homologies were surmised by examination of their positions relative to each other and skeletal landmarks and confirmed by the similarities in central positions and morphologies of the motoneurons innervating them (see Figure 7). d, Detail of the dorsal insertion on the uropod of the uropod RS muscle in the albuneid B. occidentalis (left) and hippid E. analoga (right); note that it is adjacent to the tendon of the uropod remoter muscle, which arises in the sixth segment, and is similarly positioned in crayfish (shown in a). AT, anterior telson muscle; En, uropod endopodite; Ex, uropod exopodite; Pro, uropod propodite; PTF, posterior telson flexor muscle; PTU, posterior telson-uropod muscle; Re-l, lateral uropod remoter muscle; Re-m, medial uropod remoter muscle; STF, slow telson flexor muscle (present in all species, function unclear); VTF, ventral telson flexor muscle. a (right), Adapted from Schmidt, W. 1915. Die Musculatur von Astacus fluviatilis: Ein Beitrag zur Morphologie der Decapoden. Z. Wiss. Zool. 113, 165-251. b-d, Adapted from Paul, D. H. 1981b. Homologies between neuromuscular systems serving different functions in two decapods of different families. J. Exp. Biol. 94,169-187; Paul, D. H., Then, A. M., and Magnuson, D. S. 1985. Evolution of the telson neuromusculature in decapod Crustacea. Biol. Bull. 168, 106-124.

1.07.3.2 Neuromuscular Repercussions of Increasing a Joint's Freedom of Movement

The evolution of musculature capable of generating controlled, forceful movements around such a flexible joint, while simultaneously stabilizing it against counter forces as the uropod is swept through its full trajectory, is no mean feat. The divergence of proximal tailfan musculature in hippids from that of typical decapod tailfans is so extreme that visual inspection alone gives no clues about muscle homo-logies. In fact, the one apparent exception turned out to be a false lead: the strikingly similar muscles in the anterior telson of crayfish and hippids, which also have approximately equivalent actions on the uropod, are not homologues, as was made evident by analysis of their innervations (Figures 5-7; Paul et al., 1985). Comparison of the motoneurons showed that the muscle in crayfish (the anterior telson (AT) muscle) had been lost in the sand crab lineage long before the advent of Hippidae, and was accompanied (or followed) by expansion of a smaller muscle (the anterior telson-uropod (ATU) muscle) into the vacated space in the anterior telson.

The modifications of conserved telson muscles (e.g., the ATU muscle), the loss of an ancestral muscle (the AT muscle), and the appearance of a new muscle (below) in the hippid lineage are illustrated in Figure 5 and summarized in Figure 6. Two obvious differences distinguish the tailfan muscles of hippid sand crabs and prototypical tailflipping species, such as crayfish. One is the massive uropod return-stroke muscle (RS muscle, Figures 5 and 6), which is absent from crayfish and allies. This muscle is responsible for swinging the uropod rearward preceding each power stroke, which corresponds to the extension phase in swimming by repetitive tailflipping and is equivalent to the upstroke of a wing beat in flying species. Without this muscle, swimming by uropod beating could not have evolved, for no conceivable morphological changes could have produced its biomechanical equivalent from ancestral telson muscles. The second obvious difference is the pair of ventral muscles that insert on the ventral side of the uropod propodite and are responsible for the uropod power stroke. The large uropod power-stroke muscle (PS = homologue of crayfish's ATU

Behavior Genus

Telson Flexors

Telson-uropod muscles

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