reviews TREE vol. 8, no. 7, July 1993

level patterns - those found at the 4 Nee, S., Read, A.F., Greenwood, J.J.D.and M.D. (1990) I. Anim. Ecol. 59, 335-345 regional or even intercontinental Harvey, P.H. (1991) Nature351, 312-313 24 Kleiber, M. (1975) The FireofLife (2nd level. Our greatest lack of under- 5 Marquet, P.A., Navarette, S.A. and edn), Wiley standing is at the intermediate CastiJJa,J.C. (1990) Science 250, 1125-l 127 25 Damuth, 1. (1991) Nature351, 268-269 6 Juanes, F. (1986) Am. Nat. 128,921-929 26 Lawton, J.H. ( 199 1) Philos. Trans. R. Sot. level, i.e. within collections of or- 7 Cotgreave, P. and Harvey, P.H. (1992) Land Ser. B 330, 283-291 ganisms that we choose to label Funct. Ecol. 6, 24&256 27 Peters, R.H. (1983) The Ecological communities. Part of that ignorance 8 Brown, J.H. and Maurer, B.A. (1986) Nature Implications of Body Size, Cambridge no doubt stems from a failure to 324,248-250 University Press 9 Morse, D.R., Stork, N.E. and Lawton, J.H. decide what a community really 28 Peters, R.H. and Raelson, J.V. (1984) Am. (1988) Ecol. Entomol. 13, 25-37 Nat. 124,498-5 17 is but it may be partly due to our IO Tokeshi, M. (1990) FreshwaterBiol. 24, 29 Peters, R.H. and Wassenberg, K. (1983) current inability to understand how 613-618 Oecologia 60,89-96 ecological and evolutionary pro- I I Blackbum, T.M. eta/. /. Anim. Eco/. (in 30 Nee, S., Harvey, P.H. and Cotgreave, P. cesses might interact. press) ( 1992) in Conservation of Biodiversity for I2 Griffiths, D. (1992)/. Anim. Eco/. 61, Sustainable Development (Sandlund, O.T., 307-315 Hindar, K. and Brown, A.H.D., eds), pp. Acknowledgements I3 Cotgreave, P., Hill, M.J. and Middleton, 124-I 36, Scandinavian University Press Each of the following people has helped D.A.J. Biol. 1. L&n. Sot. (in press) 31 Maurer, B.A. and Brown, I.H. (I 988) with discussion: Tim Blackbum, Charles 14 Robinson, J.G. and Redford, K.H. (1986) Ecology69, 1923-1932 Godfray, Paul Harvey, Andy Letcher, John Am. Nat. 128,665-680 32 Preston, F.W. (1948) Ecology29, 254-283 Lawton, Anne Magurran, Ame Mooers and I5 Swihart, R.K. (I 986) Acta Therio/. 3 I, 33 Preston, F.W. (1962) Ecology43, 185-215 Andy Purvis. Tim Blackbum and John 139-148 34 Preston, F.W. (1962) Ecology43,410-432 Lawton kindly provided copies of unpub- 16 Gaston, K.J. and Lawton, J.H. (1988) Am. 35 Haila, Y. and Jlrvinen, 0. (1983) Oikos 4 1, lished material. John Damuth, John Lawton Nat. 132,662-680 255-273 and an anonymous referee gave very help- I7 Gaston, K.J. (1988) Oikos 53, 49-57 36 Williamson, K. (1971) BirdStudy 18,81-96 ful comments on an earlier version. This I8 Lawton, J.H. (1989) Oikos 55,429-434 37 May, R.M. (I 978) in Diversity oflnsect work was funded by NERC and the 19 Gaston, K.J., Blackbum, T.M. and Lawton, Faunas (Mound, L.A. and Waloff, N., eds), European Community. J.H. (1993) Oikos66, 172-179 pp. 188-204, Blackwell 20 Blackburn, T.M., Lawton, J.H. and Perry, 38 Sugihara, G. (1980) Am. Nat. 116,770-787 References J.N. (1992) Oikos65, 107-I 12 39 Pagel, M.D., Harvey, P.H. and Godfray, I Damuth, J. (I 981) Nature 290,699-700 21 Blackbum, T.M., Lawton, J.H. and Pimm, H.C.J. (1991) Am. Nat. 138, 836-850 2 Damuth, J. (I 987) Biol. J L&n. Sot. 3 1, S.L. /. Anim. Eco!. (in press) 40 Carrascal, L.M. and Telleria, J.L. 11991) 193-246 22 Cotgreave, P. and Harvey, P.H. (1991) Am. Nat. 138, 777-784 3 Mohr, CO. (1940) Am. Midl. Nat. 24, Nature 353, 123 41 Brown, J.H. and Maurer, B.A. (1987) Am. 58 I-584 23 Blackburn, T.M., Harvey, P.H. and Pagei, Nat. 130, l-17

The Evolutionary Biology of

Morphologicalevidence of auditory Hearing evolution Why have tympanal ears evolved James H. Fullard and Jayne E. Yack independently so many times, and in such different locations? Although it has long been thought Few areas of science have experienced water. Tympanal ears (the only type that insect ears evolved from such a Glending of laboratory and field covered here) are located in at least internal proprioceptors4 (sensory perspectivesas the study of hearing. The ten different places in a diversity structures detecting body move- disciplinesof sensory ecology and neuro- of insect taxa (Fig. I a) - this strongly ments), it is only recently that this ethology interpret the morphology and suggests polyphyletic origins. Some hypothesis has been examined ex- phgsiology of ears in the adaptive context ears, such as the abdominal organ of perimentally. Comparative studies in which this sense organ functions. the grasshopper and the tibia1 organ suggest that the invertebrate ner- , with their enormous diversity, are of the cricket, have been well de- vous system has been conservative valuable candidates for the study of how scribed in the literature, because in its evolution - homologous neur- tympanal ears have evolvedand how they they are conspicuous and belong to ons exhibit few interspecific dif- operate today in different habitats. insects with well-known acoustic ferences compared to peripheral, behaviours. Other, more obscure nonneural structures5f6. Such con- Insect tympanal ears (i.e. those ears, such as the ‘cyclopean’ ear of the servatism is useful for testing evol- using a tympanic membrane or praying mantid’ and the prostemal utionary hypotheses regarding the ‘eardrum’) are specialized organs (thoracic) ear of the parasitoid fly2z3, insect nervous system. designed to detect distant, faint have only been described recently One way of studying the evol- sounds transmitted through air or with the aid of modern techniques. utionary origins of the insect audi- Considering that tympana have tory system is by examining the lames Fullard and JayneYack are at the Dept of been identified in only 5% of all in- tympanal organ homologues of ear- Zoology, Erindale College, Univesity of Toronto, sect orders, we expect that many less taxa and assuming that these Mississauga,Ontario, Canada 151 IC6. more insect ears await discovery. species represent the ancestral deaf

248 0 1993, Elseviet Science Publishers Ltd (UK) reviews TREE vol. 8, no. 7, July 1993

(a)

-Attachment Cell Scolopale Cap condition. offer a special op- portunity for this method: members Scolopale Rods of the superfamily pos- -Scolopale Cell sess metathoracic tympanal ears (used for the detection of the echolocation calls of hunting bats), ‘-Dendrite which are presumably derived from the atympanate condition repre- sented by extant earless Lepi- doptera (e.g. Saturniidae). Sensory cells (Fig. 1b) homologous to those in the noctuoid ear have been identified in several atympanate Lepidoptera7,8. These nonauditory neurons are in the same region as the noctuid ear sensilla, near Fig. 1. (a) The ten regions where tympanal organs have evolved within insect groups. There is diversity the metathoracic wing-hinge, and in-both the locations and complkxi;ies (from the single-celled notodontid moth ear, to that of the appear to act as proprioceptors cicada, which possesses over 1000 auditory neurons). Despite this, all are fundamentally alike: each is monitoring movements of the hind comprised of a thinned region of cuticle (tympanal membrane), an air sac which allows the membrane wing during flight and preflight to resonate to sound-induced pressure changes, and a chordotonal organ (CO). COs are a type of insect mechanoreceptor which are widely distributed throughout the body where they may function as warm-up. Structural comparisons either sound or body-movement detectors. Each CO consists of one to several hundred structural between the auditory chordotonal units called scolopidia. Each scolopidium in turn consists of an assemblage of three cell types: l-3 organ (CO) and its proprioceptor sensory neurons; a scolopale cell with an extracellular cap or tube located at the distal end of the homologue reveal few differences9, dendrite; and one or several attachment cells. Numbers refer to ears described on insect bodies: I. ; Sphingoidea: 2. Orthoptera: Ensifera; 3. Diptera: Tachinidae; 4. Mantodea: Mantidae; and the proprioceptor even re- 5. Lepidoptera: Geometroidea and Pyraloidea; 6. Orthoptera: Acrididae; 7. Hemiptera: Cicadidae; sponds to intense, low-frequency 8. Lepidoptera: Noctuoidea; 9. Hemiptera: Cotixidae; IO. Neuroptera: Chrysopidae. (b) A typical tym- sounds7. The major differences panal scolopidium, characterized by only one sensory cell per scolopidium (monodynal), and a distal between the two organs exist in dendritic segment which is tightly associated with a scolopale cap (mononematic). nonneural structures: enlarged res- piratory chambers (the tympanic is homologous to mechanoreceptive of the ancestral moth wing-hinge air sac), thinned cuticle (the tym- units in these insects’ meso- and CO was to detect small-amplitude panic membrane) and mechanical metathoracic legs. The comparative wing vibrations, such as those pro- isolation from body movements neuroanatomical data described duced during flight warm-up, it may (the tympanic frame). above suggest that insect tympanal have been easily converted into a Similar comparisons of tympanal organs have evolved from proprio- detector of high-frequency sounds ear prototypes have been made ceptors, and that the transition once echolocating bats became a in other atympanate taxa. These between the two forms involved potent selective force. include the prosternal propriocep- minimal neural changes. Insect ears, Another factor influencing which tive CO of Drosophila spp., a pro- apparently, are easy to make. Since CO proprioceptors evolved into posed homologue of the tachinid proprioceptive COs are widely dis- fly tympanal organ2, the pleural CO persed throughout the insect in- of the primitively atympanate tegument (Fig. 11, this may account grasshopper, Heide amiculi, pro- for the diversity of positions in posed homologue of the abdomi- which tympanal organs are found in nal grasshopper tympanal organlo, insects. and possibly the ‘crista acustica’ of When considering why a tym- Phasmodes ranatriformis, the pro- panal organ evolved in a particular posed evolutionary prototype of the region, we can again use compara- ensiferan tibia1 tympanal organ”. tive data. It is likely that only the In addition to comparing tym- nerve cells of those proprioceptive panal organ homologues between COs whose primitive function taxa, we can examine the ear hom- preadapted them for high sen- ologues of atympanate body seg- sitivity were good candidates to ments of the same (serial evolve into auditory receptors. For homology). Comparative develop- example, in crickets and katydids, mental studieslO indicate that the the present-day auditory hom- abdominal ear of short-horned ologues of the meso- and meta- grasshoppers (Acrididae) is homolo- thoracic legs are very sensitive gous to the proprioceptive pleural to faint substrate vibrations12, sug- COs of the six other abdominal seg- gesting that these types of COs ments as well as the wing-hinge were more easily converted into COs of the thoracic segments. It auditory receptors than detectors also appears that the tibia1 ear of of large amplitude leg movements. crickets and katydids (bushcrickets) Similarly, if the pre-auditory function reviews TREE vol. 8, no. 7, July 1993

tympanal receptors was the organ- auditory sensory projections of such cues18,‘9 to which some bats, in turn, ization of their neurons within the widely diverse insects as katydids, may have evolved acoustic coun- ancestral central nervous system cicadas and moths sharing the ter-manoeuvres (e.g. reducing the (CNS). Sensory cells send their same anatomical regions13. The intensity of their close-range calls axons into the CNS where they CNS projections of ancestral recep- or eliminating them altogether). communicate with intemeurons tors may have influenced their Cues about the position and dis- and motor neurons to produce be- evolutionary potential as auditory tance of a sound’s origin also exist haviour. The conservative organiz- cells depending upon their prox- in its frequency structure. Since ation of the CNS has resulted in imity to the neurons responsible high frequencies attenuate more for eliciting the derived adaptive than low frequencies over distance = (a) behaviour. For example, the noctuid (Fig. 2a), an ear equipped with a moth uses its metathoracic ear to template of a sound’s entire spec- rapidly trigger a series of evasive trum should be able to estimate flight manoeuvres; a thoracic CO the sender’s distance independent that already communicated with of its intensity. Recent field studies flight motor neurons would have suggest that katydids can physio- been a better auditory candidate logically determine the distance than an abdominal CO whose of singing ma1es20,2’ (Fig. 2b) but receptor endings were further from experiments also suggest that the flight control centres. high-frequency information in those sounds might be limited at long Adaptivefunction of hearing distances22*23. This would have the Sounds provide the opportunity effect of forcing receivers (e.g. for that can detect them receptive females) to move about (the receivers) to make long-range more to get a ‘fix’ on the sounds, decisions about the origins of those thereby increasing their conspicu- Frequency (kHz) sounds (the senders) without actu- ousness to predators24. An example @I ally contacting them. For short- of such a threat are the insec-

30 I I I lived organisms like insects with tivorous bats that, rather than at- m inter-male distance their plethora of potential pred- tacking their prey in the air, locate ators, selection should favour those them on the ground or vegetation @$j maximum hearing distance individuals who minimize their (surface gleaning) by listening for _I time and energy expenses with their mating or movement sounds. ears that can accurately determine In Panam& the eared insects that the position, distance and identity surface-gleaning bats prey heavily of a sound’s sender. Whether the upon, such as katydids, do not physiological reality of insects’ ears appear to hear the echolocation has lived up to their theoretical ex- calls of the bats as they attack25. 1 pectations, however, remains an Similarly, a North American bat, open question (See Box I). Myotis septentrionalis, when sur- face gleaning, emits echolocation Whereare thesounds? calls that are almost completely in- Mammals locate sounds by com- audible to sitting moths26. Although paring the side-to-side differences surface gleaning may impart a Distance (m) of their intensity (i.e. body shadow- sizable predation pressure, its rela- Fig. 2. (a) As one moves further from a complex sound, ing), time of arrival and/or wave- tive rarity within bat communities the high frequencies are atmospherically absorbed at form phases; such acoustic cues appears to have resulted in an in- a greater rate than the low frequencies. The two song are severely compromised by the sufficient selective force to cause spectra represent calling song at different distances away from the European katydid, Tettigonia cantans; small size of most insects’ bodies. auditory adaptations in insects. the top spectrum is at 7 cm, the lower one at 750 cm. While orthopterans have evolved Instead, insects have responded Although there is an overall reduction in the spectral adaptations that manipulate the with indirect (‘passive’) defences power the greatest loss occurs at higher frequencies physical properties of sound waves such as refined acoustic location of (e.g. the peak near 30 kHz). Adapted from Ref. 21. conspecifics (thus reducing the (b) The ability to hear conspecifics may predict an in- to enhance binaural differences”, dividual’s spacing behaviour. The inter-male distance other location cues exist in the receiver’s requirement to move), is that of the singing Australian katydid, Mygalopsis patterns of sounds. Many insects the use of nonacoustic forms of marki. The maximum hearing distance refers to the listen for the echolocation calls of ca1ling25 and a reduction in move- point at which one of this katydid’s CNS neurons no batsi and as this predator homes ment or the restriction of it to areas longer detects conspecific calls. The inter-male dis- tance is less than the maximum hearing distance, sug in on its target, it increases the or times separated from potential gesting that it is the high frequencies of the call that pulse repetition rate of its calls. predators (compare with the de- determines male spacing behaviour. Whether it is this This cue indicates a very close bat fences of earless moths27). neuron alone that sets the male’s spacing is unknown and triggers defences in tiger but examinations of the physiological hardware under- and praying mantids17. H4atare the sounds? lying an animal’s mating behaviour can provide valu- mothsI able insights into the mechanisms that govern that Insects may have specific sensi- Interspecific recognition. It is expected behaviour. Adapted from Ref 20. tivities to pulse repetition rate that eared insects identify the 250 TREE vol. 8, no. 7, July 1993 reviews

(a)

sounds they encounter for survival of these nocturnal flies and the (e.g. predator versus prey) and re- high-frequency sensitivity of 0. productive (e.g. conspecific versus ochracea suggests it could also heterospecific) purposes. Hypoth- detect hunting bats (R. Hoy, pers. eses about the neural hardware of commun.). As with gleaning bats, conspecific recognition in crickets parasitoids have influenced the range from relatively coarse identi- acoustic component of insect fication abilities to refined, gen- mating systems and may have sel- etically determined recognition ected for alternative reproductive circuits28. These studies further strategies (e.g. nonsinging males). demonstrate the importance of Since singing persists in host (b) I --- or1 time-structure cues for species rec- species, questions arise about the ognition29f30;animals competing with details of this relationship. Do background noise (e.g. leaves males assess parasitoid risks be- rustling) or the sounds of hetero- fore singing? Can males detect specifics should exploit this par- approaching flies? Do parasitized ameter to improve the efficacy of males have any reproductive suc- their own sounds22. Male meadow cess? Can females recognize the katydids (Conocephalos nigropleu- songs of parasitized males? rum) sing in aggregations with het- erospecifics; in this environment, tntraspecies recognition. When male the temporal patterns of individual insects sing, they are often com- songs are obscured at long dis- peting with other males to attract tance. Female C. nigropleurum females. Songs could either act may find their mates by initially as transmitters of detailed infor- Frequency (kHz) approaching any source of high fre- mation (e.g. male vigour) over long Fig. 3. Two species of tachinid fly have ears matched quency sound - even one that is distances or they could simply be to the song frequencies of their hosts. (a) In North not temporally patterned - but beacons drawing in females to a America, egg-laden females of Ormia ochracea with once within the mixed-species point where their other senses threshold intensities (thick line) have ears sensitive to cluster, they recognize conspecific actually determine the male’s the 4-5 kHz calls of the field cricket Gryl/us rubens songs and reject those of the quality. The answer to this ques- (thinner line) while (b) the ear of the European Therobia leonidei responds (thick line) to the 25-35 heterospecificP. tion lies, in part, with the physio- kHz calls of the katydid Poecilimon vehcbianus Parasitoids constitute another logical capacity of ears to decode (thinner line). The r leonidei ears were measured by selective force in insect mating sys- the information provided to them examining the vibration of the eardrum at different fre- tems. Certain female tachinid flies while in the signal-degrading con- quencies. In both cases, the matching of the tachinid ears to the fast Fourier transforms of the hosts’ songs use male orthopterans as hosts for ditions of natural environments. is not exact, which cautions against assuming single their larvae and track their mating Although studies have confirmed ear-sound evolutionary relationships. Both flies prob- calls to find themY2. The tachinid’s that females will discriminate ably listen for an assemblage of hosts, each with ear was recently described simul- songs34, it is unclear whether she slightly different song spectra. (a) Adapted from Ref: 3, taneously for a European species, uses the song to predict the quality (b) adapted from Ref 2. Therobia leonidei2 and a North of males since correlations be- American species, Onnia ochracea3. tween song parameters and male while, conversely, attraction to The flies’ ears are geographically physical attributes (e.g. body mass) social sounds, although rare, exists matched to their hosts’ songs: the have been difficult to interpret35,36. in some moths37. The question European species’ ears are tuned Females may ‘choose’ particular arises as to how these insects have to the 25-35 kHz calls of katydids songs but these could simply be changed their presumably primi- while those of the North American those of the closest male. Although tive auditory responses (e.g. attrac- species listen for the 4-6 kHz calls the costs of making mistakes about tion in the cricket and evasion in of crickets (Fig. 3). The broad a potential mate seem high, the the moth) to the opposite taxes. species diversity in the frequen- physiological constraints of insect The cricket may use specific cies of orthopteran calls combined auditory systems may render most neurons for tasks like bat-detection with the physiological constraint of (but probably not all) of these but moths, with their simpler sys- evolving an infinitely sensitive ear animals incapable of receiving suf- tems, are more constrained. The suggests that the parasitoid makes ficiently unambiguous long-range ear of the Australian whistling moth an evolutionary ‘choice’ as to which acoustic information about a sing- (Hecatesia thyridion) although used end of the acoustic spectrum to ing male’s quality. for the detection of conspecific tune itself to. Whereas low fre- social sounds, resembles a typical quencies carry further, high fre- Secondarychanges in ears bat-detecting ear38. This moth may quencies are more easily located. Although insects have primary have secondarily adapted its ears, Once the fly’s ear is tuned to its uses for their ears, examples exist ancestrally tuned for bat calls, to host (or its assemblage33 of hosts), of supplemental functions. Certain detecting conspecific males who, in it is probably unable to exploit crickets possess high-frequency turn, emit bat-like signals. To deal others. However, finding hosts is sensitivity15 that should enable with bats, this moth appears to not the only auditory requirement them to avoid echolocating bats have become diurnal. 251 reviews TREE vol. 8, no. 7, July 1993

10 Meier, T. and Reichert, H. (1990) I. Neurobiol. 2 I, 592-6 IO 11 Lakes-Harlan, R., Bailey. W.J. and Schikorski, T. ( 1991) /. Exp. Biol. 158, 307-324 12 Kalmring, K. ( 1985) in Acoustic and Vibrational Communication in Insects (Kalmring, K. and Elsner, N., eds), pp. 127-134, Paul Parey 13 Boyan, G., Fullard, I. and Williams, L. ( 1990) I. Comp. Neuroi. 295, 248-267 14 Huber, F., Moore, T.E. and Loher, W., eds (1989) Cricket Behavior and Neurobiology, Cornell University Press 15 Hoy, R.R. (1989) Annu. Rev. Neurosci. 12, 355-375 16 Fullard. 1.H. (1992) /. Comp. Physiol. A 170, 575-588 17 Yager, D.D. and May, M.L. ( 1990) /. Exp. Biol. 152, 41-58 I8 Boyan, G.S. and Fullard, ).H. (1988) J. Comp. Physiol. A 164, 251-258 19 Boyan, G.S. and Miller, L.A. (1991) I. Comp. Physiol. A 168, 727-738 20 Rheinlaender, 1. and RSmer H. (I 990) in The Tettigoniidae: Biology, Systematics and Evolution (Bailey, W.J. and Rentz, D.C.F., eds), pp. 248-264, Springer-Vedag 21 Kalmring, K., Keuper, A. and Kaiser, W. ( 1990) in The Tettigoniidaet Biology, Systematics and Evolution (Bai)ey,W.). and Rentz, D.C.F., eds), pp. 191-216, Springer- Verlag 22 RBmer. H. and Lewald, 1(I 992) Behav. Ecol. Sociobiol. 29, 437-444 23 Mason, A.C., Morris, G.K. and Wall, P. (1991) Natunvissenschaften 78,365-367 24 Heller, K-G. (I 992) Naturwissenschaften 79,89-9 I 25 Belwood, 1.1. (1990)in The Tettigoniidae: Sexual dimorphism in insect ears standing how ears function for Biology, Systematics and Evolution (Bailey, occurs as a result of the different these ‘simple’ animals in their natu- W.J. and Rentz, D.C.F., eds), pp. 8-26. Springer-Verlag life histories of the sexes. Female ral environments will undoubtedly 26 Faure, P.A., Fullard, J.H. and Dawson, gypsy moths (Lymantria dispar) reveal new adaptations and may I.W. /. Exp. Biol. (in press) do not fly and have no need to ultimately demonstrate the details 27 Merrill, S.B. and Fullard, I.H. (1992) Can. detect bats, but males fly through- of insect hearing to be as complex 1. Zoo]. 70, 1097-I 101 28 Doherty, J. and Hoy, R. (1985) 0. Rev. out the night. Compared to males, as this heterogenous taxon itself. Biol. 60,457-472 the ears of females appear degen- 29 Fullard, J.H., Morris, G.K. and Mason, erated in their loss of high-fre- Acknowledgements AC. ( 1989) 1. Comp. Physiol. A 164, 50 I-5 I 2 quency sensitivity39. More dramatic We thank R. Fulthorpe, D. Gwynne, R. 30 Shatral, A. (I 990) in The Tettigoniidae: examples exist in female moths Hoy and two anonymous reviewers for their Biology, Systematics and Evolution (Bailey, helpful comments on this paper. Our re- W.I. and Rentz, D.C.F., eds), pp. 152-165, with completely degenerate wings search has been supported by the Natural Springer-Verlag and ears40. A correlated reduction Sciences and Engineering Research Council 31 Gwynne, D.T. and Morris, G.K. (1986) of wings and ears also exists in of Canada, the University of Toronto and the Evol. Theor. 8, 33-38 praying mantids4’ suggesting a National Geographic Society. 32 Cade, W. ( 1975) Science 190, I3 12-l 3 I3 33 Fullard, I.H. (1988) Experientia 44, genetic link between these two References 423-428 structures. 1 Yager, D.D. and Hoy, R.R. (1986) Science 34 Tuckerman, J.F., Gwynne, D.T. and 23 I, 727-729 Morris, G.K. Behav. Ecol. (in press) Conclusions 2 Lakes-Harlan, R. and Heller, K-G. (1992) 35 Bailey, W.). and Yeoh, P.B. (1988) Physiol. Insect hearing, although con- Naturwissenschat?en 79,224-226 Entomol. 13,363-372 3 Robert, D., Amoroso. J. and Hoy, R.R. 36 Dadour, I.R. and Bailey, W.). (I 990) in servative in its cellular morphology, (1992) Science258, 1135-1137 The Tettigoniidae: Biology, Systematics and exhibits a broad range of adaptive 4 von Kennel, I. and Eggers, F. (I 933) Zoo/. Evolution (Bailey, W.J. and Rentz, D.C.F., modifications. We should, on one Jahrb. Abt. Anat. Ontog. Tiere 57, I-104 eds), pp. 98-l I I, Springer-Vedag hand, appreciate the physiological 5 Dumont, J.P.C. and Robertson, R.M. (1986) 37 Spangler, H.G. (1988)Annu. Rev. Science 233,849-853 Entomol. 33, 59-8 I constraints that exist when specu- 6 Meier, T., Chabaud, F. and Reichert, H. 38 Surlykke, A. and Fullard, J.H. (I 989) lating on what insects can do with (1991) Development 112,241-254 Natutwtssenschaften 76, 132-l 34 their ears, but on the other, be 7 Yack, I.E. and Fullard, 1.H. (1990) /. Comp. 39 Cardone, B. and Fullard, 1.H. (1988) aware that insects represent one of Neural. 300,523-534 Physiol. Entomol. 13,9-l 4 8 Yack, I.E. (1992) I. Comp. Neural. 324, 40 Sattler, K. (1991) Bull. Br. Mus. Nat. Hist. the most diverse animal groups 500-508 (Em) 60, 243-288 in the world and the majority of 9 Yack, I.E. and Roots, B.I. (1992) Cell 41 Yager, D.D. (1990) I. Zoo/. 22 I, their ears remain unstudied. Under- Tissue Res. 676, 455-471 517-537 252