The Mechanism of Rapid Running in the Ghost Crab, Ocypode Ceratophthalma
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J. Exp. Biol. (1973), 58, 327-349 327 With 1 plate and 19 text-figures Printed m Great Britain THE MECHANISM OF RAPID RUNNING IN THE GHOST CRAB, OCYPODE CERATOPHTHALMA BY MALCOLM BURROWS* AND GRAHAM HOYLE Department of Biology, University of Oregon, Eugene, Oregon, U.S.A., and Hawaiian Institute of Marine Biology, Coconut Island, Hawaii {Received 19 July 1972) INTRODUCTION Of all crustaceans which move on land, crabs of the genus Ocypode living on tropical sandy beaches achieve the highest speeds. Their rapid, sideways running represents an escape response terminating in the surf or a burrow previously built at or above high-tide mark. When retreat into either of these safe havens is prevented the crab flees at great speed for a short distance but then either prostrates itself in any available depression on the beach or begins to dig itself a new burrow (Cott, 1929). It has been stated that they run sideways using three pairs of walking legs (Koepcke & Koepcke, 1953) or sometimes only two pairs (Gravier, 1922). The impression of high speed is enhanced by supreme agility; they can accelerate rapidly from a standing start, reverse direction abruptly without great loss of speed and rotate their body through 1800 while continuing to run in the same direction (Koepcke & Koepcke, 1953). Estimates of the speed of running have been made many times. Cott (1929) estimated that the O. ceratophtkalma which he observed ' could hardly have been travelling at less than iom.p.h.' (4-4m/sec), while Koepcke & Koepcke (1953) estimated the O.gaudichaudU ran at i-6 m/sec. Hafemann & Hubbard (1969) deter- mined the speed of O. ceratophihalma over unspecified distances on sandy beaches and found an average speed of i-8 m/sec. On the harder surface of a wooden ship's deck the same authors found the average speed increased to 2-3 m/sec, with one individual recorded at 4 m/sec. They found that speed is correlated with body size, measured as width of the carapace, up to a particular size beyond which all the larger crabs ran at approximately the same speed. Hafemann and Hubbard attempted to explain the high speed of running in terms of three specializations of the body. First, the length of the legs for a given body size is greater than for other species of crab from the same habitat; for example Sesarma (Cott, 1929) or Pachygrapsus (Hafemann & Hubbard, 1969). This would allow the length of a step and hence the 'gearing' of the movement to be increased. Secondly, the extensor muscle in the meropodite is always larger than its antagonist, while the reverse is true in other crabs such as Pachygrapsus. This leads to the main power for running being developed about the mero-carpopodite joint in the form of a pushing thrust. Thirdly, since they found the muscles of the leg to have high tetanus fusion-frequencies, of the order of 90 Hz, this might allow the muscles to produce • Present address: Beit Memorial Fellow, Department of Zoology, University of Oxford. 328 M. BURROWS AND G. HOYLE a high rate of cycling of leg movement. Hafemann & Hubbard (1969) calculated that stepping at 90-100 Hz would be necessary to explain the maximum speeds they observed. We were attracted to the problem principally because we were searching for examples of experimentally analyzable central nervous motor programs. The high predicted stepping rates for Ocypode would require complete stepping cycles of only about 10 msec, leaving insufficient time for peripheral sensory feedback to adjust motor output. In addition, since the length changes are relatively large, whilst force requirements are high, specializations of the muscle fibres, a matter in which we are also interested, might have been expected to have occurred. We first tested the ability of the muscles to produce unfused contractions of sufficient magnitude at the high rates required. Although the tetanus fusion-frequency is high, the muscles give very little tension variation at frequencies above 30 Hz, and we estimated that the maximum usable rate would be 25 Hz. This is well below the rate which Hafemann and Hubbard stated would be required and forced us to examine the various aspects of running. We also decided to study the actual rates of movement by electromyography from the running crab. Our findings were some- what surprising, but they do allow us to offer an explanation of rapid running in terms of rates of stepping compatible with the contractile properties of the muscles. They also show a large disparity between the action of the legs on the leading side of the body compared with the trailing side. A difference, though much less than the differences we shall describe below, has recently been shown for Carcinus (Clarac & Coulmance, 1971). MATERIALS AND METHODS Ocypode ceratophthcdma were collected from beaches on the windward side of the island of Oahu, Hawaii. Crabs above 20 mm in carapace width were obtained in the late evening after sunset for they were not visible during the day. By contrast, smaller crabs were common during the daytime. They were kept in a tank with a sloping floor which allowed access to exposed sand or circulating sea water and thus simulated a sloping beach. Most runs were carried out with crabs which had been held captive for less than 24 h. To examine the neuromuscular physiology of leg muscles a third leg was removed, and the muscles were exposed and bathed either in a Ringer's solution containing, in imi/1: Na+, 466; K+, 8; Ca5*, 20; Mg5*, 2; C\~, 502; HCO3-, 8; buffered to pH 70 or in filtered sea water, both at 24-26 °C. Electrical responses of the muscle fibres were recorded with conventional intra- cellular electrodes, and the nerve fibres were stimulated with electrical shocks of variable duration and intensity through a pair of chlorided silver hook electrodes. Tension of the whole muscle was measured by grasping the muscle apodeme between forceps attached to a Grass FTO 3 mechano-electronic transducer. The speed of running was measured using a race track 3 m long by 0-2 m wide having a base of moist, hard-packed sand 40 mm deep. The middle metre of the track was marked by photocells 10 mm wide on to which were focused beams of light. The resolution of the photocells was such that interception of the light beam by the individual legs of a crab as they passed could be detected. Rapid running in ghost crabs 329 The output of the photocells was displayed on a pen recorder which allowed measurement of the time taken to cover 1 m to be made with an accuracy of ± 4 msec. Speed could thus be determined to within at least + 0-5 % over a range 0-5-2-5 m/sec after a start (to permit acceleration) of at least 1 m. Crabs were induced to run in either direction along the track with either the left or right set of legs leading. Those with carapace widths below 12 mm were run on a second, smaller track 600 mm long and 10 mm wide but with the same base of hard-packed sand. The middle 200 mm of this track was monitored by photocells. The gait of the crabs was investigated by first allowing them to run over smooth, moist but firm sand in which the tips of the dactyls left an impression. A clearer picture was obtained by dipping the tips of selected dactyls into acrylic paint of different colours and allowing the crab to run over white paper placed in the 3 m race track. Electromyograms from freely moving crabs were made by inserting 50 fim silver or copper wire insulated but for the tip into the appropriate muscle. The leads were sealed in place using Eastman 910 adhesive and wax of low melting point. The leads were taken to a central anchoring point on the carapace formed by a bracelet of 200 fim copper wire which passed around the body and between the bases of the first and second pairs of legs. From this point the wires ran to a junction box 1 m above the track and then via shielded cables to a.c.-coupled pre-amplifiers with a band width of 80 Hz to 5 kHz. The output of these amplifiers was recorded on an Ampex d.c. tape-recorder for later display on a pen recorder or oscilloscope. The crabs were allowed to move freely across either a circular tank with a diameter of 1 m or along the 3 m track. All behavioural and electromyographic experiments were conducted at ambient air temperatures of 28-32 °C. RESULTS Neuromuscular physiology We measured twitch time, tetanus fusion-frequency, time to peak tetanic contraction and the relaxation time from this for the opener and closer of the dactylopodite, the extensor and flexor of the carpopodite and the levator and depressor of the basipodite. Only the extensor and flexor of the carpopodite will be described in detail (summarized in Table 1) since the others were closely similar. We did not detect any properties which we consider would radically affect the speed of locomotion. Of the two muscles in the meropodite the extensor is heavier by some 30% (Hafemann & Hubbard, 1969). Its fibres arise from a centrally placed apodeme and insert predominantly on the posterior wall of the meropodite, the majority being towards the proximal end of the segment. The colour of the fibres varies along the length of the muscle, there being a central portion of white, translucent fibres bounded proximally and dorsally by a small group of pinkish-brown fibres and distally by a larger group of pink fibres.