[ 270 ]

THE FUNCTION OF THE LYRIFORM ORGANSOF ARACHNIDS

BY J. W. S. PRINGLE

Department of Zoology, University of Cambridge*

(Received 13 August 1954)

INTRODUCTIONThe term ' lyriform organs' was first used by Gaubert (1890) to describe the groupsof peculiar sense organs found on the legs and elsewhere in arachnids. The indivi-dual sensilla in these organs are similar in structure to isolated sensilla which occurwidely on the cephalothorax and abdomen of many spiders and other arachnids andwhich were first described by Bertkau (1878). They are often referred to as 'slitsense organs' (Spaltsinnesorgane), since their appearance in surface view suggestsa 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 merelya pronounced thinning of the 'chitin' along a narrow groove with a continuousepicuticular membrane. The term 'lyriform organ' describes the characteristicappearance of the compound organs where a number of slits of varying length arearranged in a parallel or near-parallel orientation in the same manner as the stringsof the musical instrument (Fig. 1).

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

The internal histological structure of the sensilla has been described fully byVogel (1923) and Kaston (1935). In external view the slits (10-50/i long) havea slight widening at one point and to the centre of this widened region inserts thedistal process of a sense cell. The cells of the hypodermal layer under the sensillaare modified in appearance and are probably responsible for the modified cuticularstructure of the region.

The most recent view of the function of the slit sense organs (Millot, 1949) is thatthey are chemoreceptors, an opinion supported by Mclndoo (1911) and Kaston(1935). Apart from earlier implausible hypotheses the only other function attributedto them is that of proprioception (Vogel, 1923). Mclndoo and Kaston supported

• The experimental work reported here was carried out during 1953 in the Department ofPhysiology, University of Ceylon, Colombo, and in the laboratory of the Division of Entomology,Department of Agriculture, Peradiniya, Ceylon.

The function of the lyriform organs of arachnids 271

their hypothesis by experiments on the contact chemical sense of spiders, andclaimed that the distribution of the slit sense organs on the body was consistent withtheir being the structures concerned; Vogel had no experimental evidence toconnect them with a kinaesthetic sense, but was impressed by the constancy oforientation and the continuity of the epicuticular membrane, features which hecould not correlate with a chemoreceptive function.

None of the workers who have studied these organs appear to have noted thesimilarity between their structure and distribution (at any rate on the appendages)in arachnids and the structure and distribution of the campaniform sensilla ofinsects. In both cases modified regions of the cuticle near the joints have sense-cellprocesses attached to the centre of a thin membrane, and both types of sensillumhave a constant orientation in different individuals and in related species. The

Fig. 1. Lyriform organs on the chelicera of a spider, to show the different orientationof the slit sensilla of the two groups (from Vogel, 1923).

campaniform sensilla of insects were at one time thought to be chemoreceptors(Mclndoo, 1914), but Pringle (1938), by recording impulses in their sensory nerves,established that they are mechanoreceptors sensitive to strains in the cuticle, andthat the orientation of the more advanced type of sensillum found in adult insectsis significant in relation to the quality of stimulus to which they respond. Similarinvestigation of the range of sensitivity of the lyriform organs is made difficult bythe small size of the arachnids available in temperate countries and by the poorsurvival of spiders as experimental animals for neurophysiological work. Thetropics are better provided in this respect, and it has now been possible to settle thefunction of the lyriform organs in an unequivocal manner.

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

272 J. W. S. PRINGLE

Impulses were recorded in various sensory nerves by means of platinum wireelectrodes, 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/imagnetic tape recorder and the results re-photographed on oscilloscope film afterreturn to England. This method distorts the waveform of nerve impulses but issatisfactory when only the frequency and relative amplitude of impulses is ofinterest. Since the motor speed of the tape recorder varies slightly with the voltageof the electric supply, time measurements from oscilloscope records made in thisway have an accuracy of about ± 10%.

No form of Ringer's solution was necessary. The temperature of the laboratorywas 28-320 C.

Fig. a. Pkrynickus lunatus (Pallas). (Two-thirds natural size.)

RESULTSIf electrodes are placed on the nerve trunk near the base of the amputated leg ofa scorpion impulses are readily recorded in the sensory fibres. The long setae whichoccur on each of the leg segments give rapidly adapting impulse discharges of largeamplitude when they are moved, and a confused pattern of small impulses resultsfrom touch stimuli to the distal tarsal segments.

Forced movement at the coxo-trochanteral, trochantero-femoral, femoro-tibialor tibio-tarsal joints gives a different result, the discharge then consisting of impulsesin a small number (1-6) of fibres, with slow adaptation (Fig. 3A-C). The fibresconcerned appear to be of various sizes and different fibres are active when themovement is one of extension from those reacting to flexion. Slow forced move-ments bring in only the smaller fibres, while fast movements usually excite also asingle large fibre, also different for the two directions of movement. At the coxo-trochanteral and trochantero-femoral joints the fibres reacting to joint movementrun centrad up the leg for a short distance as a separate trunk before joining themain nerve, and clearer records are obtained when the electrodes are placed onthese small trunks.

The function of the lyriform organs of arachnids 273

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 forcedmovement of the joint excites only one or two small fibres and fast movementsbring in also a larger fibre, both discharges occurring in different fibres for the twodirections of movement.

A

IAAWVWWVW\AAWWWWVWWYVWWWWWWWUW^

i I I ! i l l i 1 ! M l Mi ! " M ^ ^ i l ' i l i i i l i J l l l J l i i J i i i ! 1 ! 1

•yiiiiiuui i i IMiJI

HUM

i l l I L-L L-i ,i.U.L 1r i

llUilliiJl.Lll.

111 li l l i lUi I ill I I 1 I I

TTT Trim rrAA/VVV\AAAAAAAAAAAA^AAA/VVV\/Vy^/VW\AAAAAAAAAAA/V\AAAA/VVyVVW^l^

Fig. 3. Oscilloscope records from scorpion sensory nerves, re-printed from magnetic tape recordings.A: leg nerve at base of femur; forced extension of femoro-tibial joint; B: small nerve trunk introchanter, maintained forced flexion of trochantero-femoral joint; C: small nerve trunk incoxa, increase from partial to complete extension of coxo-trochanteral joint; D: leg nerve atbase of femur, pressure with needle at two different places on distal end of femur, portions ofa continuous record under conditions comparable to A; E: abdominal nerve, pressure withneedle on terminal segment of sting. Time marker 50 cyc./sec. (trace) and 0-5 sec. (dots).

iff J. W. S. PRINGLE

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

Attempts were made to locate the endings responsible for the sensory dischargeaccompanying joint movement. With the parallel in mind of the campaniform

vmmmmmmmmmmmmmmm

Extension Flexion

Extension Flexion

Fig. 4. Oscilloscope records from Phrymchus claw nerve; forced movement of femoro-tibial jointat various speeds. A, fast extension with slow flexion; B, very fast flexion with slow extension.Time 50 eye./sec.

sensilla of insects, which are strongly excited by strains induced by any form ofdistortion of the cuticle near the joints (Pringle, 1938), pressure was applied with theblunt point of a needle to the end of the femur near the femoro-tibial joint of thescorpion leg. Fig. 3 D shows that a considerable discharge from slowly adaptingendings can be obtained in this way, the size of the fibres so excited being comparableto that of the smaller fibres which are excited by forced joint movement. It isnoteworthy that discharges in different fibres were obtained by pressure with theneedle at slightly different locations on the femur. This sensitivity to distortion ofthe cuticle of the next proximal segment was confirmed for each of the four basaljoints of the scorpion leg and in the claw and legs of Phrymchus. A similar resultwas also obtained from the abdominal nerves of the scorpion in response to pressureanywhere on the terminal segment of the sting (Fig. 3 E).

These results point clearly to the lyriform organs as the structures concerned inthe discharge of the smaller impulses during forced joint movements and show (aspostulated by Vogel, 1923) that the slit sense organs are mechanoreceptors, sensi-tive to strains in the cuticle. Groups of sensilla, sometimes lyriform in appearance,

The function of the lyriform organs of arachnids 275are present on the scorpion leg near the joints close to the positions of maximumsensitivity to pressure with a needle (Fig. 5). The experiment on spontaneousflexion suggests that, as with the campaniform sensilla of insects, the endings aremore strongly excited by forced movements of the joints (or presumably by resistedactive movement) than by spontaneous movement when the leg is out of contactwith the ground. Vogel's suggestion that the slit sense organs confer a kinaestheticsense analogous to the muscle and tendon senses of vertebrates is therefore confirmed.

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

Fig. 5. Outside (A) and inside (B) view of the right fourth leg of a scorpion,showing the position of the slit sensilla (groups numbered 1-6).

DISCUSSIONTwo unresolved points may be mentioned. The sensory discharge in large fibreswhich 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

276 J. W. S. PRINGLE

features which appear to distinguish it from the discharge in smaller fibres whichhas been identified with the slit sensilla of the lyriform organs. These large im-pulses adapt more rapidly than those in smaller fibres and occur only with rapidforced movement. Fig. 4 also shows that the discharge of large impulses regularlystarts after the maximum frequency in the smaller fibres when some movement of thejoint has taken place. If the ending responsible for the large fibre discharge is also a slitsensillum it would be expected that it would be excited at the moment of maximumstrain in the cuticle when the frequency of small impulses is also maximal. It is alsonoteworthy that the large impulses could never be obtained by pressure witha needle on the cuticle near the joint, although impulse frequencies in small fibreswere often higher with this form of stimulation than with very rapid movement.On the other hand, the large fibre discharge could usually be obtained withoutsimultaneous excitation of the smaller fibres by probing with the needle into thesoft flexible regions of the intersegmental membranes. It was also found that thelarge fibre discharge on rapid movement of the femoro-tibial joint (scorpion) wasselectively abolished by section of the tibia half-way along its length, while the smallfibre discharge remained unaltered. The conclusion from these experiments wasthat this large fibre discharge originates from an ending, of a different type from theslit sensillum, situated internally in the leg near the joint; a structure which may beresponsible was discovered by dissection and will be described in a subsequentpaper (Parry & Pringle, in preparation).

The other point concerns the direction of strain to which the lyriform organsrespond. Pringle (1938) concluded that the campaniform sensilla of insects wereexcited by a compression strain parallel to the long axis of the sensillum (which iselliptical but rarely has a major/minor axis ratio of more than 3:1). This conclusionwas reached partly on microanatomical grounds, the structure being such that thisstimulus would be expected to stretch the nerve ending (Fig. 6), and partly fromthe positioning and orientation of the sensilla on the legs, a compression strainparallel 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 thefact 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 selectivelysensitive to one direction of strain, and the differences in orientation of neighbouringlyriform groups, when two organs occur in close proximity (Fig. 1), suggests thatsuch a qualitative discrimination is a property of the sensilla. The fact that differentendings are excited when pressure is applied with the needle at slightly differentplaces on the cuticle has already been noted. If it is assumed, as for the campani-form sensilla, that stretch of the distal process of the sense cell is the adequatestimulus for excitation, then Fig. 6 shows that the sensilla should respond when thetension component of shear is at right angles to the orientation of the slits. Ina plane surface of uniform thickness this implies a compression component parallelto the slits and a similarity in sensibility to the insect campaniform sensillum; butit is probably unwise to apply reasoning derived from the properties of uniformplane surfaces to the irregular and highly dissected surface of the arachnid cuticle

The function of the lyriform organs of arachnids 277

at the lyriform organ. No certain conclusion can be reached on this point withoutaccurate model-building, an undertaking which would be rendered extremelydifficult by the differences not only in thickness but also in elastic rigidity ofdifferent parts of the cuticle near the articular surfaces of the joints.

Fig. 6. Diagrammatic drawings of the structure of an insect campaniform sensillum (A) and anarachnid slit sensillum (B). The arrows show the probable direction of strain which excites thesensilla. (A: based on drawings of the basal plate sensilla on the haltere of Calliphora (Pflug-staedt, 1912); B: based on a drawing of the lyriform organ on the patella of a spider (Vogel,1923)0

SUMMARY

Experiments involving the recording of impulses in sensory nerves in the appendagesof a scorpion and an amblypygid show that the slit sensilla (lyriform organs) ofthese arachnids are mechanoreceptors, sensitive to strains in the cuticle and analo-gous to the campaniform sensilla of insects.

I am grateful to Prof. Koch, Department of Physiology, Colombo, and to theDirector of Agriculture, Peradiniya, for giving me facilities to carry out this workin Ceylon; and to the Director of the National Museum, Colombo, for allowing hisassistant to collect material for my experiments. The visit was made possible bythe award of a Leverhulme Research Fellowship, and I also received financialassistance from the H. E. Durham Fund of King's College, Cambridge, and fromthe British Council. Part of the apparatus used was purchased with the aid of theGrants Committee of the Royal Society.

REFERENCESBERTKAU, P. (1878). Versuch einer naturlichen Anordnung der Spinnen nebst Bemerkungen zu

einzelnen Gattungen. Arch. Natwrgach. 44, 354.GAUBERT, P. (1890). Note sur les organes lyriformes des Arachnides. Bull. Soc. philom. Paris,

sir. 8, 3, 47.GAUBERT, P. (1892). Recherchea sur les organes de sens et sur les systemes integumentaires,

glandulaires et musculaires des appendices des Arachnides. Ann. Sci. nat. s6r. 7, 13, 57.

278 J. W. S. PRINGLE

HANSEN, H. J. (1893). Organs and characters in different orders of Arachnids. Ent. Medd. 4, 137.KASTON, B. J. (1035). The slit sense organs of spiders. J. Morph. 58, 189.MCINDOO, N. E. (1911). The ryriform organs and tactile hairs of Araneids. Proc. Acad. Nat. Sci.

Philad. 63, 375.MCINDOO, N. E. (1914). The olfactory sense of the honey-bee. J. Exp. Zool. 16, 265.MILLOT, J. (1949). Classe de Arachnides. In GRASS*!, P-P., Traiti de Zoologie, 6. Paris: Masson

et Cie.PFLUGSTAEDT, H. (1912). Die Halteren der Dipteren. Z. wist. Zool. 100, 1.PRINGLE, J. W. S. (1938). Proprioception in insects. I. A new type of mechanical receptor from

the palps of the cockroach. II. The action of the campaniform scnsilla on the legs. J. Exp.Biol. 15, 101, 114.

VOGKL, H. (1923). Ueber die Spaltsinnesorgane der Radnetzspinnen. Jena. Z. Naturw. 59, 171.