Some Recently Discovered Underwater Vibration Receptors in Invertebrates

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Some Recently Discovered Underwater Vibration Receptors in Invertebrates Some Contemporary Studiea in Marine Science, pp. 395-405 (1966) Harold Ba.mes, Ed. George Allen and Unwin Ltd., London SOME RECENTLY DISCOVERED UNDERWATER VIBRATION RECEPTORS IN INVERTEBRATES G. A. HORRIDGE Gatty Marine Laboratory and Department of Natural Hi~tory, University of St. Andrewa As every submarine commander knows, the best and almost the only underwater sense organs which are effective at long range utilize the excellent transmission of mechanical waves through water. And yet when the known examples of sense organs which are adapted to the detection of underwater vibrations were recently reviewed by Frings (1964), almost no substantiated examples could be found among marine invertebrates. Even in shallow water, large animals with excellent eyes spend about half of their time in dim moonlight or in the dark, and the range of vision falls off rapidly with depth, so that objects cannot be seen until they are relatively close. However, most invertebrates have eyes which are not well adapted for the detection of the direction and range of a moving prey. On the other hand, vibrations are set up in the water by any animal which propels itself along, as well as by waves at the surface or choppy water at a shore line. Therefore we can expect receptors for vibrations to be distributed ubiquitously through the marine groups, and to be used to detect prey or enemies, or to allow avoidance of environ­ mental sources of vibration. Perhaps one of the reasons why more examples of sense organs of this type are not known is because we ourselves have nothing similar, because the receptors are inconspicuous, and because the responses depending on them are usually not obvious escape reactions. However, in the last two or three years a number of examples have appeared in different phyla so that the general features of invertebrate underwater vibration receptors have now become apparent. Several of these examples have been discovered at St. Andrews. VIBRATION RECEPTORS Fingers of Leucothea (Ctenophora) This is an example of the vibration sense used by a carnivore in locating its prey. Leucothea ( = Eucharis) multicornis is a large fragile carnivorous Mediter­ ranean ctenophore which has numerous finger-like organs about 1 cm long scat- 396 G . .A. HORRIDGE tered over its external surface (Fig. lA). The epithelium of the finger tips is com­ posed of large glandular cells between which are sensory cells (Chun, 1880). Some of the sensory cells bear single straight stiff, non-motile cilia and these are receptors for any small displacement of the surrounding water. When a copepod or similar small planktonic animal swims within range, the finger shoots out with a sudden extension, caused by contraction of circular muscles which run through the mesogloea of the finger. The fingers extend to about 1 cm from a resting length of about half this value. The bottom of any dish in which the animal is supplied with copepods is soon littered with immobilized copepods. In 1844 Dr. Will, working in Trieste, claimed that the copepods were caught on small hooks on the ends of the fingers, but I have not yet seen this, and have not yet discovered how the Leucothe,a makes use of its victims. There are neither nematocysts nor similar organs on the fingers and the poison which kills the copepods presumably originates in the gland cells. A C B 2cm L---.J Fig. 1.-Leucothea ( = Etwharis) multicornis. A, the apical part of the ctenophore showing the finger organs scattered over the general surface. B, two fingers, one in the relaxed, and the other in the extended, position. C, the terminal epithelium of a finger showing the gland cells, thick pogs (function unknown) and a long non-motile cilium of the vibration sensory neurone. D, the base of a non-motile cilium with concentric lamellae which are surrounded by a mass of tubules (after Horridge, 1965a). The sense organs have been directly demonstrated to be the non-motile cilia in the following way. When an isolated finger is observed on a slide with a high power objective of long working distance, the cilia are found to be extremely sensitive mechanically. They cannot be touched without exciting the response. A glass needle mounted on the diaphragm of a loudspeaker, vibrated at a fre­ quency of 10 cycles/sec with a tip excursion of a few microns, can be manoeuvred into position near the cilium with a micromanipulator, but cannot be brought closer than about 100 µ, before the extension response of the whole finger is evoked. The structure of the sensory cilium itself is not peculiar, but the basal body and root is modified into a solid banded core which fits inside a spherical shell. The latter fits concentrically inside another spherical shell which is attached to a mass UNDERWATER VIBRATION RECEPTORS 397 of tubules filling the cytoplasm of the distal end of the cell (Fig. ID). It is clear that the non-motile cilium is mechanically coupled with the water so that any lateral movement of the water will be conveyed into a rocking movement of the basal body inside its spherical cup. This assumes that there is a plane of shearing between the concentric shells. A tentative theory of the mechanism is that shearing between the spherical shells causes current to flow through the mass of tubules which in turn depolarize the distal end of the cell membrane. The proximal end of the sensory neurone bears an axon which connects with other axons of the nerve net, which in turn are inferred to connect specifically with the circular muscle fibres causing extension. For further details, with electron micrographs, see Horridge (1965a). Tentacles of Pleurobrachia This is an example of a vibration receptor used as a detector of adverse environ­ mental conditions. The common St. Andrews ctenophore Pleurobrachia pileus, after being caught in a plankton net, usually swims downwards when brought into the laboratory. However, when the animals are carefully dipped out of the sea, and are handled . r ! ~ Fig. 2.-A, Pleurobrachia pilet,s turning over when vibration receptors of the tentacles and elsewhere are stimulated. B, Eutonina indicans turning to swim downwards and away from a source of low frequency vibration or ripples. Approximately natural size. gently without being lifted from the water, they commonly swim upwards. Speci­ mens which are swimming up respond by turning over and swimming downwards when one runs one's fingers to and fro over them in the tank, so causing ripples on the water surface. This stimulus causes a strong vibration which shakes the whole animal. The first sign of the responsei s a contraction of the two long tenta- 398 G. A. HORRIDGE cles, which normally trail in a relaxed fashion behind the animal. A vibrating needle, attached to a loud-speaker diaphragm, can stimulate a single tentacle when brought close to it. The response then starts as a contraction of the tentacle and spreads to the body of the Pleurobrachia, which changes the rate of its comb­ plates on one side relative to the other and turns over to swim downward (Fig. 2A). Isolated tentacles will respond by contracting and animals without tentacles will still invert when stimulated with the vibrating probe. The sense organ has not been identified. However, Hertwig, R. (1880, p. 326) mentioned that "Sinnesborsten" , similar to those of Leucothea, occur on the tenta­ cles of ctenophores. These are non-motile cilia which have not yet been found with the electron microscope on tentacles, but they may well turn out to be similar to the vibration receptors of Eucharis. The statolith in the ctenophore apical organ functions as a receptor of the direction of gravity because the weight of the statolith bears on the four groups of balancer cilia. These are strong groups of cilia which stand at the head of the ciliated grooves which in turn lead down to the comb-plates. Each beat of the balancer cilia sets off a wave of beats along the pair of ciliated grooves, which run from that balancer tuft and this wave travels along the comb-plates. In this way the balancer cilia are in control of the geotactic response (Horridge, 1965b). When a ctenophore turns over and swims downward in response to disturbance of the water, the sign of the response of the balancer cilia is reversed by excitation in the general nerve net. As a vibration receptor the statolith is not very effective. A large vibration in the water will jerk the statolith and then the balancer cilia respond, but usually all four respond together so that the additional waves in the comb-plates are of no consequence. Margin of Eutonina indicans (Hydromedusae) This is another example of the avoidance of surface ripples by a delicate plank­ tonic animal, which at the same time presents its mouth to a source of vibration. Eutonina is a hemispherical medusa about 3 cm. diameter, with a manubrium which reaches as far as the edge of the bell. Although the response is not typical of Hydromedusae the manubrium can be directed to any point on the subumbrellar surface where a stimulus is applied (Romanes, 1877). As was shown by making cuts, the manubrium is controlled by radial pathways which transmit inwards from the edge of the bell, as in Geryonia (Horridge, 1955). When a Eutonina is swimming in an upright position in a dish of sea water, it can be stimulated with a vibrating needle mounted on a loudspeaker diaphragm. The Eutonina turns over in a direction away from the stimulus and it swims downwards for several seconds or minutes (Fig. 2B). Like ctenophores, individuals of Eutonina which are damaged when collected from the sea usually swim down­ wards when brought into the laboratory, and upwardly swimming specimens must be dipped, not netted, out of the sea.
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