The Function of the Lyriform Organs of Arachnids

The term ‘lyriform organs’ was first used by Gaubert (1890) to describe the groups of peculiar sense organs found on the legs and elsewhere in arachnids. The individual sensilla in these organs are similar in structure to isolated sensilla which occur widely on the cephalothorax and abdomen of many spiders and other arachnids and which were first described by Bertkau (1878). They are often referred to as ‘slit sense organs ‘(Spaltsinnesorgane), since their appearance in surface view suggests a slit in the cuticle. Recent investigators (Vogel, 1923 ; Kaston, 1935) are, however, agreed that there is no actual canal leading from within to the exterior, but merely a pronounced thinning of the ‘chitin’ along a narrow groove with a continuous epicuticular membrane. The term ‘lyriform organ’ describes the characteristic appearance of the compound organs where a number of slits of varying length are arranged in a parallel or near-parallel orientation in the same manner as the strings of the musical instrument (Fig. 1).

Single or compound sense organs of this type occur in nearly all arachnids, and their distribution over the body is remarkably constant within each order (Gaubert, 1892 ; Hansen, 1893 ; McIndoo, 1911). They are found near the joints of the legs and other appendages, on the sterna of the cephalothorax and abdomen and on the sting of scorpions, and, as Vogel (1923) has pointed out, are constant not only in position but also in the orientation of the slits. The leg organs are usually compound and are often situated where the cuticle is curved near the articular surfaces.

The internal histological structure of the sensilla has been described fully by Vogel (1923) and Kaston (1935). In external view the slits (10–50µ long) have a slight widening at one point and to the centre of this widened region inserts the distal process of a sense cell. The cells of the hypodermal layer under the sensilla are modified in appearance and are probably responsible for the modified cuticular structure of the region.

The most recent view of the function of the slit sense organs (Millot, 1949) is that they are chemoreceptors, an opinion supported by McIndoo (1911) and Kaston (1935). Apart from earlier implausible hypotheses the only other function attributed to them is that of proprioception (Vogel, 1923). McIndoo and Kaston supported their hypothesis by experiments on the contact chemical sense of spiders, and claimed that the distribution of the slit sense organs on the body was consistent with their being the structures concerned; Vogel had no experimental evidence to connect them with a kinaesthetic sense, but was impressed by the constancy of orientation and the continuity of the epicuticular membrane, features which he could not correlate with a chemoreceptive function.

None of the workers who have studied these organs appear to have noted the similarity between their structure and distribution (at any rate on the appendages) in arachnids and the structure and distribution of the campaniform sensilla of insects. In both cases modified regions of the cuticle near the joints have sense-cell processes attached to the centre of a thin membrane, and both types of sensillum have a constant orientation in different individuals and in related species. The campaniform sensilla of insects were at one time thought to be chemoreceptors (McIndoo, 1914), but Pringle (1938), by recording impulses in their sensory nerves, established that they are mechanoreceptors sensitive to strains in the cuticle, and that the orientation of the more advanced type of sensillum found in adult insects is significant in relation to the quality of stimulus to which they respond. Similar investigation of the range of sensitivity of the lyriform organs is made difficult by the small size of the arachnids available in temperate countries and by the poor survival of spiders as experimental animals for neurophysiological work. The tropics are better provided in this respect, and it has now been possible to settle the function of the lyriform organs in an unequivocal manner.

Two large arachnids have been used in this investigation; a scorpion Heterometrus (Palamnaeus) swammerdami Simon, and an amblypygid Phrynichus lunatus (Pallas) (Fig. 2). The animals were collected in the field in Ceylon and kept in cages in the laboratory. The scorpions varied in body length from 7 to 15 cm. Three specimens only of P. lunatus were obtained ; these had a body length of about 3 cm.

Impulses were recorded in various sensory nerves by means of platinum wire electrodes, a Grass Type P.4 pre-amplifier and a Cossor Type 1049 oscilloscope. Alternatively, the output from the pre-amplifier was fed to an M.S.S. Type PMR/1 magnetic tape recorder and the results re-photographed on oscilloscope film after return to England. This method distorts the waveform of nerve impulses but is satisfactory when only the frequency and relative amplitude of impulses is of interest. Since the motor speed of the tape recorder varies slightly with the voltage of the electric supply, time measurements from oscilloscope records made in this way have an accuracy of about ± 10%.

No form of Ringer’s solution was necessary. The temperature of the laboratory was 28−32°C.

If electrodes are placed on the nerve trunk near the base of the amputated leg of a scorpion impulses are readily recorded in the sensory fibres. The long setae which occur on each of the leg segments give rapidly adapting impulse discharges of large amplitude when they are moved, and a confused pattern of small impulses results from touch stimuli to the distal tarsal segments.

Forced movement at the coxo-trochanteral, trochan tero-femoral, femoro-tibial or tibio-tarsal joints gives a different result, the discharge then consisting of impulses in a small number (1−6) of fibres, with slow adaptation (Fig. 3A–C). The fibres concerned appear to be of various sizes and different fibres are active when the movement is one of extension from those reacting to flexion. Slow forced movements bring in only the smaller fibres, while fast movements usually excite also a single large fibre, also different for the two directions of movement. At the coxo-trochanteral and trochantero-femoral joints the fibres reacting to joint movement run centrad up the leg for a short distance as a separate trunk before joining the main nerve, and clearer records are obtained when the electrodes are placed on these small trunks.

Similar results are obtained from the femoro-tibial joint of the claw (pedipalp) and legs of the amblypygid Phrynichus lunatus (Fig. 4). Here again slow forced movement of the joint excites only one or two small fibres and fast movements bring in also a larger fibre, both discharges occurring in different fibres for the two directions of movement.

In one experiment on the coxo-trochanteral joint of the scorpion leg the motor nerve supply to the flexor trochanteris muscle was left intact and periodic flexor movements occurred spontaneously. Small diameter nerve fibres from endings at the joint were excited by these movements but the discharge was considerably less than that produced by forced movement of the same amplitude. No impulses in large sensory fibres occurred during spontaneous flexion.

Attempts were made to locate the endings responsible for the sensory discharge accompanying joint movement. With the parallel in mind of the campaniform sensilla of insects, which are strongly excited by strains induced by any form of distortion of the cuticle near the joints (Pringle, 1938), pressure was applied with the blunt point of a needle to the end of the femur near the femoro-tibial joint of the scorpion leg. Fig. 3 D shows that a considerable discharge from slowly adapting endings can be obtained in this way, the size of the fibres so excited being comparable to that of the smaller fibres which are excited by forced joint movement. It is noteworthy that discharges in different fibres were obtained by pressure with the needle at slightly different locations on the femur. This sensitivity to distortion of the cuticle of the next proximal segment was confirmed for each of the four basal joints of the scorpion leg and in the claw and legs of Phrynichus. A similar result was also obtained from the abdominal nerves of the scorpion in response to pressure anywhere on the terminal segment of the sting (Fig. 3E).

These results point clearly to the lyriform organs as the structures concerned in the discharge of the smaller impulses during forced joint movements and show (as postulated by Vogel, 1923) that the slit sense organs are mechanoreceptors, sensitive to strains in the cuticle. Groups of sensilla, sometimes lyriform in appearance, are present on the scorpion leg near the joints close to the positions of maximum sensitivity to pressure with a needle (Fig. 5). The experiment on spontaneous flexion suggests that, as with the campaniform sensilla of insects, the endings are more strongly excited by forced movements of the joints (or presumably by resisted active movement) than by spontaneous movement when the leg is out of contact with the ground. Vogel’s suggestion that the slit sense organs confer a kinaesthetic sense analogous to the muscle and tendon senses of vertebrates is therefore confirmed.

The possible chemoreceptive sensitivity of the slit sensilla was tested briefly in scorpions by the application of liquid xylol to the region of the femoro-tibial joint; no sensory discharge resulted from this treatment.

Two unresolved points may be mentioned. The sensory discharge in large fibres which occurred, both at the three basal joints of the scorpion leg and at the femoro-tibial joint of Phrynichus claw, on rapid forced movement of the joint shows several features which appear to distinguish it from the discharge in smaller fibres which has been identified with the slit sensilla of the lyriform organs. These large impulses adapt more rapidly than those in smaller fibres and occur only with rapid forced movement. Fig. 4 also shows that the discharge of large impulses regularly starts after the maximum frequency in the smaller fibres when some movement of the joint has taken place. If the ending responsible for the large fibre discharge is also a slit sensillum it would be expected that it would be excited at the moment of maximum strain in the cuticle when the frequency of small impulses is also maximal. It is also noteworthy that the large impulses could never be obtained by pressure with a needle on the cuticle near the joint, although impulse frequencies in small fibres were often higher with this form of stimulation than with very rapid movement. On the other hand, the large fibre discharge could usually be obtained without simultaneous excitation of the smaller fibres by probing with the needle into the soft flexible regions of the intersegmental membranes. It was also found that the large fibre discharge on rapid movement of the femoro-tibial joint (scorpion) was selectively abolished by section of the tibia half-way along its length, while the small fibre discharge remained unaltered. The conclusion from these experiments was that this large fibre discharge originates from an ending, of a different type from the slit sensillum, situated internally in the leg near the joint; a structure which may be responsible was discovered by dissection and will be described in a subsequent paper (Parry & Pringle, in preparation).

The other point concerns the direction of strain to which the lyriform organs respond. Pringle (1938) concluded that the campaniform sensilla of insects were excited by a compression strain parallel to the long axis of the sensillum (which is elliptical but rarely has a major/minor axis ratio of more than 3:1). This conclusion was reached partly on microanatomical grounds, the structure being such that this stimulus would be expected to stretch the nerve ending (Fig. 6), and partly from the positioning and orientation of the sensilla on the legs, a compression strain parallel to the long axis being present when the leg is in contact with the ground. Similar reasoning is difficult to apply to the slit sensilla of arachnids owing to the fact that they are usually situated in strongly curved regions of the cuticle. It is, however, highly probable that a greatly elongated structure of this sort is selectively sensitive to one direction of strain, and the differences in orientation of neighbouring lyriform groups, when two organs occur in close proximity (Fig. 1), suggests that such a qualitative discrimination is a property of the sensilla. The fact that different endings are excited when pressure is applied with the needle at slightly different places on the cuticle has already been noted. If it is assumed, as for the campaniform sensilla, that stretch of the distal process of the sense cell is the adequate stimulus for excitation, then Fig. 6 shows that the sensilla should respond when the tension component of shear is at right angles to the orientation of the slits. In a plane surface of uniform thickness this implies a compression component parallel to the slits and a similarity in sensibility to the insect campaniform sensillum; but it is probably unwise to apply reasoning derived from the properties of uniform plane surfaces to the irregular and highly dissected surface of the arachnid cuticle at the lyriform organ. No certain conclusion can be reached on this point without accurate model-building, an undertaking which would be rendered extremely difficult by the differences not only in thickness but also in elastic rigidity of different parts of the cuticle near the articular surfaces of the joints.

I am grateful to Prof. Koch, Department of Physiology, Colombo, and to the Director of Agriculture, Peradiniya, for giving me facilities to carry out this work in Ceylon; and to the Director of the National Museum, Colombo, for allowing his assistant to collect material for my experiments. The visit was made possible by the award of a Leverhulme Research Fellowship, and I also received financial assistance from the H. E. Durham Fund of King’s College, Cambridge, and from the British Council. Part of the apparatus used was purchased with the aid of the Grants Committee of the Royal Society.