THE EVOLUTIONARY DIFFERENTIATION OF STRIDULATORY SIGNALS IN (Insecta : Coleoptera)

BY RICHARD D . ALEXANDER AND THOMAS E . MOORE Museum of Zoology and Department of Zoology, The University of Michigan, Ann Arbor AND ROBERT E. WOODRUFF Florida Department of Agriculture, Division of Plant Industry, Gainesville

Introduction "Spontaneous" Stridulation in Trogidae Stridulatory noises have been discussed for While collecting at night with headlamps on many different families of beetles, and presumed 16th May, 1959, in Ripley County, Missouri, stridulatory organs have been described for we heard chirping coming from the ground hundreds of species that have not actually been around a dead cat lying in a sparsely vegetated heard stridulating. (cf. Arrow, 1904, and biblio- area along the roadside. Using a portable tape graphy by Frings & Frings 1960). So far, recorder, earphones, and a microphone to neither auditory organs nor acoustical functions amplify and localize the sounds, we found that have been experimentally demonstrated in any chirping came from several burrows, each about . There are a few records of beetles stridu- 8 mm. diameter, which were scattered within a lating upon contact with other individuals of few feet of the carcass . The burrows were about their own species (Liles, 1956 ; Alexander, 1957), 10 centimetres deep and nearly vertical ; each but otherwise, only gross disturbances, e .g. of several excavated contained one adult female handling or restraint, have been observed to of suberosus Fabricius at its lower end . elicit stridulation. One burrow contained a male and a female ; As a more or less incidental adjunct to in- it is not known whether sound was coming from vestigations on the acoustical behaviour of this particular burrow. , Homoptera, and by The sound was a continual irregular, repeating Alexander & Moore, and as a result of the of the phrases shown in Fig. 1 . Each phrase was particular efforts and interest of Woodruff, produced by one stroke of a small ridge (pleg- we have accumulated tape-recordings of about matium) on the dorsal surface of the abdomen 40 beetle species in eight families ; Passalidae, across two tooth-like ridges (files) on the under- Trogidae, , Chrysomelidae, Tene- side of the elytra. The file ,(Figs. 18 and 19) brionidae, Carabidae, Curculionidae, and Cer- covers approximately the posterior one-third of ambycidae . In this paper we compare disturb- the length of the elytra and is composed of over ance stridulation among congeneric, sympatric 150 teeth in a very narrow strip running parallel species in two subsocial families (Trogidae and to the suture on a raised carina . The teeth in the Scarabaeidae) and one non-social family (Cer- middle of the ridge are slightly more widely ambycidae), and discuss two new kinds of beetle separated than those on either end but they are stridulations : a "spontaneous" stridulation in all minute and difficult to detect except under isolated, undisturbed Trogidae and a distinctive high magnification (60X) . Sharp (1897) described aggressive stridulation in the social Passalidae . similar stridulatory apparatus in several Trox All of these sounds taken together appear to species. During stridulation the abdomen is illustrate three stages in the evolutionary elabor- moved up and down and slightly forward and ation of communicative signals : (1) a single backward to engage the plegmatium (Fig. 16) structural kind of signal utilized in a single with the file. This movement is not extensive but functional context (disturbance-actual function is easily observed. Apparently only a portion of not proven) ; (2) a single structural kind of signal the narrow file is struck on each movement, since utilized in two different functional contexts a maximum of twenty tooth strikes is eindicated (disturbance and calling, disturbance and con- on the audiospectrograph. gregation, and possibly disturbance and some The beetles (both sexes) produced essentially sort of "recognition") ; and (3) two structurally the same sound when captured (Fig. 2), different signals utilized in two different func- and when isolated overnight in vials and left tional contexts (disturbance and aggression) . undisturbed . Some individuals produced this

111

112 BEHAVIOUR, XI, 1

sound continually for very long periods of time proprioceptive feedback, or through rhythms while lying otherwise motionless on their backs . inherent in the make-up, of the central nervous Using the amplifier of a tape recorder as a system . Trox suberosus may represent an inter- monitor, we found that some beetles were still mediate stage in the divorcement of a sound stridulating hours after being isolated in padded from its old stimulus situation (probably dis- chambers completely separated from any reason- turbance) as a result of its having acquired a able possibility of external disturbances.* new function . The situation here suggests that To our knowledge there is no previously re- the continual chirping may attract males into corded instance of a beetle producing a stridulat- the female's burrow, or deter other females from ory sound in the absence of disturbance by entering occupied burrows, or do both. Each other . In other disturbed beetles that burrow was undoubtedly destined to become we have recorded, the stridulation always the home of one pair of these sub-social beetles stopped a few seconds after the disturbance was and their off spring. discontinued. In the particular case of Trox suberosus, even if stridulation in the burrows Aggressive and Other Stridulations in Passalidae was initiated by our footsteps-unlikely because There is little doubt that sound has acquired we were several yards away and motionless a congregating function in the social Passalidae, when the chirps were first noticed-it continued where larvae have evolved the ability to produce during several long periods when we were pro- a sound similar to that of the adults by means of viding no disturbance at all, and it was delivered a strictly juvenile apparatus on the larval legs at thd' same tempo regardless of our activities . (Figs. 11-13). Passalids live in dense colonies, The "spontaneous" stridulation of Trox and stridulate almost continually . The adults suberosus can be analogized with the calling and guard, feed, and otherwise care for their off- congregating noises of male Orthoptera and spring from egg to adult (cf. Miller, 1931 ; Homoptera, often termed spontaneous, not so Ohaus, 1900). Colonies develop from one or much because of the kind of initiating stimulus, two adults isolated with 5-20 juveniles that are but because once started they continue for long kept by the adult in a compact group . Passalid periods unless disturbances cause their cessation . sounds have evolved somewhat farther than Although the thresholds for the production of other beetle noises known, as is revealed by the such sounds can be adjusted by different events distinct aggressive sound of Popilius disjunctus -for example, changes in light intensity (Alex- (Illiger) (Fig. 12), which Mr. William Hebb and ander, 1960) and the presence or absence of a Dr. Thomas J. Walker at the University of spermatophore in the spermatophore pouch in Florida (personal communication) first heard Orthoptera (Huber, 1960)-it is not known and tape-recorded . Subsequently Alexander re- whether any of them are ever initiated in a norm- corded it from Florida and North Carolina al animal without external stimulation ; in fact, beetles just brought in from the field . Hebb without external acoustical stimulation of one and Walker heard it produced by an adult sort or another. We have not yet satisfactorily brought into the laboratory during spring (1960) answered the ancient question : "What makes when individual broods of young larvae were the chirp?" present in the field with one or both parents . "Spontaneous" or long-continued sound pro- We heard it in fall (1960) when only adults and duction could evolve from any kind of signal pupae were present, caged together in large requiring a specific and more or less continual numbers. Always it is produced by an aggressor stimulation through.: (1) a lowering of threshold during fighting . The stridulator advances, biting with respect to the required intensity or specific- at the other beetle, rooting him about with the ity of the external initiating stimuli and (2) a head, and sometimes lifting him into the air tendency to continue the reaction after the in- after seizing some appendage with the man- itiating stimulus has disappeared. The latter can dibles. We have seen reciprocal aggression with be effected through auditory feedback, through aggressive stridulation only once, although the fights were sometimes violent, and once a non- *All sounds were recorded with a Magnemite Portable reciprocating beetle lost an appendage . One Tape Recorder, Model 610-E, or a Magnecorder, of the aggressive beetles in our cages returned Model PT63AH, and a D-33 American Dynamic Microphone, at a tape speed of 15 inches per second . three times to the same crevice and took up Specimens and tape recordings are located in the the same stance after attacking beetles passing University of Michigan Museum of Zoology . near it, suggesting some form of territoriality . ALEXANDER et al. : EVOLUTIONARY DIFFERENTIATION OF STRIDULATORY SIGNALS IN BEETLES PLATE IX

Figs. 1-5 . Audiospectrographs of sounds of Trox species (Trogidae) : Fig . 1 . T. suberosus Fabricius, "spontaneous" stridulation of an adult in a burrow, 61°F . ; Fig . 2. Tsuberosus, disturbed adult, 70°F . ; Fig. 3 . T. variolatus Melsheimer, disturbed adult, 80°-85°F . ; Fig . 4 . T. unistriatus Beauvois, disturbed adult, 80 °-85 ° F. ; Fig . 5 . T.capillaris Say, disturbed adult, 80°-85 °F . Anim. Behav., 11, 1 ANIMAL BEHAVIOUR, XI, I

PLATE X

Figs. 6-10. Audiospectrographs of disturbance sounds of adult Scarabaeidae (Geotrupinae) and Cerambycidae : Fig . 6, Geotrupes splendidus (Fabricius) (Geotrupinae), 80 ° -85 ° F . ; Fig. 7, G . black- burnii (Fabricius), 80°-85°F . ; Fig . 8, G . serniopacus Jekel, 80°-85°F . ; Fig . 9, Tetraopes tetraophthalmus (Forster) (Cerambycidae), 83°F . ; Fig. 10, T. femoratus LeConte, 85°F. ALEXANDER et al. EVOLUTIONARY DIFFERENTIATION OF STRIDULATORY SIGNALS IN BEETLES PLATE X1

Figs . 11-15 . Audiospectrographs of sounds of Passalidae and Scarabaeidae (Acanthocerinae, Apho- diinae) : Fig . 11, Popiliusdisjunctus (Illiger) (Passalidae), disturbed adult, 74°F . (high-pitched sound is cricket in background) ; Fig . 12, P. disjunctus, aggressive adult, 76°F . ; Fig. 13, P. disjunctus, disturbed , 74°F . ; Fig . 14, Cloeotus aphodioides (Illiger) (Acanthocerinae), disturbed adult, 80°-85°F . ; Fig . 15, Aphodius fossor (Linnaeus) (Aphodiinae), disturbed adult, 80 °-85 ° F. Anim. Behav., 11, 1

ALEXANDER et al. : EVOLUTIONARY DIFFERENTIATION OF STRIDULATORY SIGNALS IN BEETLES 113

On another occasion, fighting was induced ing of the species as the second noise of Tetra- several times in succession in two adults in a opes does (compare Figs . 11, 12, this paper, pan. When placed in a head-on position, the with Figs . 12, 13, Alexander, 1957) . However, two individuals moved together and antennated there is no evidence that the "purring" of each other. After a short time in this position, Tetraopes is aggressive in function . one beetle (the same each time) suddenly seized Adult passalid beetles produce noises appar- the other with its mouthparts and wrenched ently identical to their disturbance squawks violently upwards, sideways, and backward . when attacked by other beetles and when they The other beetle in each case lowered its body come into brief antenna! contact with one an- and stood motionless afterward. other while moving about a crowded cage . The It is interesting that the aggressive sound of adults of Cloeotus aphodioides (Illiger) (Scasa- Popilius structurally resembles a second noise baeidae: Acanthocerinae) make a similar noise ("purring") recorded for Tetraopes tetraoph- when caged together (Fig . 14). Eventually they thalmus (Forster), and bears essentially the same congregate into a compact ball in the darkest structural relationship to the disturbance squeak- corner of the cage, there continuing to move about and stridulate so that the squirming mass of beetles emits a steady, shrill chatter. In the field these beetles are found in dense clusters under bark. The disturbance squeak- ing of both adult and larval passalid beetles has often been discussed, but neither the aggressive nor the "con- tact" situation-rarely ob- served because of the specific [stimuli necessary for their release-has been mentioned previously . No one has yet heard a special iii adult sound resulting from contact with the larvae, though there surely must be at least one. Disturbance Stridulations in Congeneric, Sympatric Species Many of the beetles known to stridulate upon disturbance inhabit re- stricted, temporary niches, INTERNAL ~~FILE such as dung, carrion, bracket fungi, and decay-

FILE ing logs, and many of them EXTERNAL ELYTRAL SUTURE are also rudimentarily so- 19 cial (Passalidae, Trogidae, 18 Geotrupinae, Coprinae), re- maining with the larvae and Figs. 16-19 . Trox suberosus Fab. : Fig . 16, dorsal view of adult with elytra removed, guarding and caring for showing folded wings in situ and position of the plegmatium ; Fig . 17, ventral them in various ways . The view of the elytra (circle indicates portion enlarged in Fig . 19) ; Fig . 18, cross section of the elytra in the area shown by the circle ; Fig . 19, enlarged portion of sounds of all these beetles the elytra showing position of the file and the individual teeth, are too soft to operate at

114 ANIMAL BEHAVIOUR, XI, I

very great distances, but in addition to the made upon contact between conspecific males obvious possibilities in parent-offspring inter- and females-is even more difficult to suggest . actions, they could function in several fash- Perhaps the three species of Geotrupes (Scara- ions among adults in close proximity . For baeidae) whose sounds are shown in Figs . 6-8 example, several species of Trox or Geotrupes represent such a case . Stridulation in these can be found in the same pile of dung species is not so easily elicited by disturbance . or carrion . In such a mixed population, individ- Some individuals could not be induced to uals of the same species might through stridu- stridulate at all, and others stridulated only lation find one another and stay together, repel when a front leg was jerked vigorously with individuals of other species, or stimulate court- forceps. There is no tendency for stridulation ship and copulatory activities in con-specific to continue after the disturbance has ceased, individuals. Repellent stridulation (disturbance and although the sounds differ among species, reactions ?) would be expected to retain or evolve they are not as distinct as those of Trox species. toward non-specificity in the eliciting stimuli ; In central Ohio these three species of Geotrupes stridulations causing copulation movements are commonly found living together in the should evolve toward specificity in the eliciting same pile of dung. stimuli ; and congregational stridulations should evolve toward detachment from specific ex- Discussion ternal elicitation. In the last two cases there should be evolution toward species-specificity in The paucity of specific information as to their the nature of the signals themselves ; in the first effects makes it tempting to discount the signific- case this would carry no apparent advantage . ance of the countless soft sounds produced by Among our tape recordings of beetles, we disturbed . But there was a period when have searched with doubtful success among misguidedly parsimonious biologists for the groups of closely related species living together same reason repeatedly pronounced accidental for the beginnings of the three evolutionary and meaningless even the elaborate performance directions suggested above. The milkweed of Orthoptera and Cicadidae . The behaviour of beetles, Tetraopes tetraophthalmus (Forster) and beetles is almost totally unexplored, and situ- T. femoratus LeConte (Cerambycidae), occur ations in which those species that produce together on the same plants and are adult at sounds upon disturbance might also stridulate the same times . These species both stridulate in connection with sexual or social behaviour readily at the slightest disturbance and terminate may be rarely observed. Actually, even intense the reaction immediately when the stimulus orthopteran sounds, which seem a veritable stops ; they also show little species specificity in bedlam to those familiar with them, go com- the nature of their squeaking sounds (Figs. pletely unnoticed by most people, and it is certain 9-10).* All of these characteristics suggest that that we would not have noticed the sound of their sounds are primarily non-specific dis- Trox suberosus-though it was audible several turbance reactions. yards away-if we had not been listening con- Figs. 3-5 compare the disturbance sounds of tinually for the stridulations of nocturnal three Trox species (Trogidae) found together Orthoptera . as adults in various combinations in owl pellets, carrion, and the like . The sounds of the three Obviously the disturbance stridulations of species differ in toothstrike rate and pulse beetles have little taxonomic significance . This length, and in the only Trox species heard in the is not unexpected because they operate only at field-T. suberosus-the long-continued nature close range after the individuals involved have of the signal indicates divorcement from the been brought together by some other kind of eliciting stimulus. These attributes suggest stimulation . However, the rudimentary nature of congregational functions . acoustical behaviour in beetles-coupled with The third possibility-stimulation to court- the great number and' variety of species and ship or copulation through stridulatory sounds systems involved-makes this kind of behaviour *In each case where audiospectrographs are presented in these particular animals an appropriate for comparison, we have used examples that are as subject for the study of evolutionary direction nearly alike as we could find. Low frequency marks- e.g. along the bottom of figs . 1, 5, 7, 9, 12-are back- in the early elaboration of communicative ground noises . systems . ALEXANDER et al. : EVOLUTIONARY DIFFERENTIATION OF STRIDULATORY SIGNALS IN BEETLES 115

REFERENCES Gehirnes bei der Fortbewegung and der Lauter- Alexander, R. D. (1957) . Sound production and associ- zeugung der Grillen . Z. vergl. Physiol., 44, 60- ated behavior in insects. Ohio J. Sci ., 57, 2, 101- 132, 38 figs., 8 tab . 113, 13 figs., 1 text fig. Liles, M. P. (1956). A study of the life history of the forked fungus beetle, Bolitotherus cornutus Alexander, R . D. (1960). Sound communication in (Panzer) (Coleoptera :, Tenebrionidae). Ohio J. Orthoptera and Cicadidae . In : Animal Sounds and Sci., 56, 3, 329-337, 4 figs., I tab. Communication (Lanyon & Tavolga, ed.). Miller, W. C. (1931) . Some observations on the habits of A.LB.S. Publ., 7, 38-92, 16 figs ., 5 recordings . Passalus cornutus (Coleoptera) . Ohio J. Sci., 31, Arrow, G . J. (1904) . Sound-production in the lamellicorn 266. beetles . Trans . ent . Soc . London, 1904,709-751,1 pl Ohaus, F . (1900) . (On the stridulation and social life of Passalus cornutus Fab .) . Stett . ent . Z., 61, 164. Frings, H. & Frings, M . (1960) . Sound production and Sharp, D. (1897) . On the stridulatory organs of Trox. sound reception by insects : a bibliography. Univ. Ent. monthly Mag., 33, 206-207 . Park, Penn : Penn. State Univ. Press. Huber, F . (1960). Untersuchungen fiber die Function des (Accepted for publication 28th June, 1962 Zentral Nerven-systems and inbesondere des Ms. number : 282).