Anim. Behav ., 1979, 27, 1073-1090

COURTSHIP IN TWO SPECIES OF PERIODICAL CICADAS,MAGICICADA SEPTENDECIM AND MAGICICADA CASSINI

BY D. COVALT DUNNING*, JOHN A . BYERSt & C. DWIGHT ZANGER$*Dept. of Biology, West Virginia University, Morgantown, WV 26506, tDept. of Environmental,Population and Organismic Biology, University of Colorado, Boulder, Colorado 80309, $60 Hardgrove

Terrace, Irvington, New Jersey 07111

Abstract . Courtship behaviour of two species of periodical cicadas, Magicicada septendecim andM. cassini, was studied in the field during the 1970, 1973, and 1974 emergences of these insects. In areaswhere both species were courting there were differences in both male and female courtship patterns,both in acoustic and behavioural components. Experiments with models showed that male M. septen-decim were more likely to court crude models of females than were M. cassini males. When femaleswere `courted' with models that could imitate some of male courtship, they were more receptive when themodels' `songs' were those of conspecific males . Acoustic differences between species are probably usedby females in mate selection, maintaining species separation even in areas where the two species overlapin both space and time .

IntroductionBroods of periodical cicadas synchronize theirlife cycles such that the adult insects emergetogether after nearly 13 or 17 years of subter-ranean life . Within each brood there may be upto three congeneric species, each of which can bedistinguished with difficulty on morphologicalgrounds but whose males sing quite distinctivesongs (Alexander & Moore 1962) . The threespecies in a 17-year brood are different from eachother but apparently indistinguishable from thethree species in a 13-year brood (Simon in press) .Within a 13-year brood the species are as easilydiscriminated as within a 17-year brood . Sinceeven those 13- and 17-year broods whoseemergence areas overlap geographically onlyemerge together as adults every 221 years, the13- and 17-year species have been consideredseparate, sibling species (Alexander & Moore1962), though recent evidence suggests closergenetic relationships (Simon in press) .

Within a brood, the three species are usuallyfound in slightly different habitats (Dybas &Lloyd 1974), but they can sometimes be foundtogether within a small emergence area,encompassing perhaps a few hundred squaremetres. The males of all species commonly singon the same twigs under these circumstances,often at the same time. Females frequently sit onbranch tips within a few centimetres of membersof other species . Insects of each species, then,have ample opportunity to hybridize withmembers of other species under these circum-stances, and thus may face particular difficultiesin maintaining their own species integrity .

1073

It is highly probable that the three species in abrood do normally remain separate. Althoughinterspecific copulation is possible if the femalesare restrained, it seems almost never to occur innature (Alexander & Moore 1958 ; Dybas &Lloyd 1962 ; White 1973) . Copulation usuallycontinues for an hour or more, and insects incopula are easily observed in an emergence area .Members of a copulating pair are almostinvariably seen to be of the same species (Dybas& Lloyd 1962 ; White 1973) .There are several possible mechanisms that

could operate to keep the three species within abrood separate . Lloyd & Dybas (1966) andDybas & Lloyd (1974) have suggested thatMagicicada cassini are primarily insects of thelowland forest canopy, while M. septendecim aremost often found in upland woodlands . Theease with which monospecific copulating pairsand ovipositing females of all species can befound within a small, multispecific emergencesite suggests that, though these insects probablywere geographically isolated in different habitatswhen they originated and may remain separatedin mature woodlands, they are now frequentlyspatially sympatric, especially in areas under-going secondary succession (Dybas & Lloyd1974) .

Alexander & Moore (1962) noted that, even ina multispecific emergence site (that is, one whereperiodical cicadas of more than one speciesemerge in the same year), the chorus of songs ofeach species reached a peak intensity at adifferent time of day . Thus it is possible thatallochrony, involving differences in the time of

1074

maximum activity, may aid in the maintenanceof species integrity . The allochrony is far fromperfect, and there are frequently periods whencicadas of several species are courting simulta-neously .

As a third alternative method of speciesseparation, the insects themselves may dis-criminate among the various sexual partnersavailable and choose members of their ownspecies, even though they may now be bothspatially and temporally sympatric . Once specia-tion has occurred the mechanisms of characterdisplacement would predict that such discrimina-tions would be selectively advantageous (Brown& Wilson 1956) . The marked differences amongthe songs sung by the males of the variousspecies suggests that acoustic cues may be ofcentral importance in behavioural species dis-crimination by the insects themselves . Simmonset al. (1971) have shown that the differences insound frequency spectra of the songs are matchedby the insects' auditory sensitivities . Of course, itis quite possible, if not probable, that differencesof habitat, time of maximum activity, andinterspecific behavioural discrimination alloperate together to maintain species integrity inemergences of periodical cicadas .

Immediately below we shall provide a sum-mary of the behaviour sequences and songsinvolved in periodical cicada courtship . Most ofit has also been reported in more detail byAlexander & Moore (1958) . In the ensuingsections detailed analyses of each stage andexperiments designed to probe the biologicalsignificance of various aspects of courtship willbe described. The general description is true forboth Magicicada septendecim and Magicicadacassini, with occasional exceptions as indicated .Behaviour patterns found in 17-year cicadas canprobably be assumed to occur also in thecorresponding 13-year broods, although we havestudied only those with 17-year life cycles .Cicada courtship, like most examples of animalbehaviour, does not comprise a series of discretestages ; rather it is continuous and has beendivided into stages to facilitate analysis .

During an emergence the male cicadas sing,their songs combining to a deafening din that canbe heard over great distances . The song attractsconspecifics of both sexes, which fly toward thesinging centre, the area where the sound isloudest. Once there, the females land on branchtips and generally remain still, though they maywalk about . The males join the chorus of theirconspecifics . This usually means that they sing a

ANIMAL BEHAVIOUR, 27, 4

phrase or two of their calling song, fly a shortdistance, land on a twig and sing again, fly toanother twig, sing, and so on . In Magicicadacassini the males may synchronize the phrases oftheir calling songs so that they all sing eachphrase together, fly together, sing again, etc . Thisaggregation phase has been amply described andanalysed by Alexander & Moore (1958) .Normal courtship begins when a male drops

out of the sing-fly chorus and remains on a twigwhile continuing to sing. In a dense singingcentre he will probably be within a few centi-metres of another cicada, which, if it is silent, maybe a female. If the singing centre is multispecific,that is if more than one species is chorusing inthe same area, no assumptions are possibleregarding the probable species of other cicadasin the vicinity . The song that the male singsduring this stage is indistinguishable in cadenceand form from his calling song, but it is calledcourt I (see Fig . 1) because of the differentcircumstances in which he sings it . Since themales usually sing only two phrases of theircalling song between flights, any sequencecomprising four or more phrases without flighthas been designated as court I . This stage hasalso been described by Alexander & Moore(1958), though they did not consider it a part ofcourtship.

__

1

2 sacCourt I : Magicicada septendecim

Court I : Magicicada cassini

Fig . 1 . Sonagrams of court I songs . Only a single phraseof each song is shown .

During the next stage of courtship, the maleapproaches another cicada while singing, usuallyeither court I or court II . Court II (Fig . 2) issimilar to court I in that each phrase is like thoseof the calling song, but the interphrase interval ismuch shorter and each phrase may be somewhatshortened as well. The song thus has a fastercadence than court I and is equivalent to thefirst courting song of Alexander & Moore (1958) .After approaching the courted insect, thecourting male usually stops and remains motion-less about 1 cm away while continuing to sing . Ifthe animal being courted moves away, thecourting male usually follows, maintaining adistance of a few centimetres between them. Thisperiod of watchful waiting and discreet pursuitmay continue for periods ranging from a fewseconds to hours. It can be recognized ascourtship only by the singing of one or morecourting songs by the male .

Most courtships are terminated at the wait/pursuit stage, usually by some apparent action ofthe courted insect, after which the courting maleleaves. If the courted animal does not move,however, courtship may proceed to the nextstage. During this period, the courting malemoves closer to the courted cicada and touchesit with one of his forelegs . Since he is usuallybehind the other animal as a consequence of the

3-Ny1

DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS

1 075

1

2 sec

CourtII : Magicicada septendecim

1 . 5

2.0 secCourtE : Magicicada cassini

Fig. 2 . Sonagrams of court II songs. Two phrases of theM. septendecim song are shown but only one for M.cassini.

pursuits, the touch is delivered to the tips of theother insect's folded forewings. The touch may beaccomplished with a straightforward pawingmotion or he may vibrate the foreleg as he paws .The male may or may not sing a courting song ashe paws at the courted cicada .

If the courted insect remains motionless, themale may proceed to the next stage of courtship,or he may return to the wait/pursuit stage . If heproceeds singing, the phrases of his song shortenand the interphrase interval decreases until he issinging a series of short, rapid phrases, each ofwhich resembles one of the segments of hiscalling song in frequency structure. This quicktempo song is court III (Fig. 3) and is equivalentto the second courting song of Alexander &Moore (1958). The male may repeat the pawingat the courted cicada while creeping closer andcloser. If he is not rejected, he climbs upon theback of the female and begins probing with hisgenitalia while turning around and around,sometimes singing. Shortly thereafter, if thefemale does not move, coupling is accomplished,whereupon any singing abruptly ceases .At any time during all of this the courted

animal can indicate its non-receptivity bymoving. If it is definitely not receptive, e .g . if it isanother male, it usually flies away . A milderdegree of rejection is apparently indicated bywalking away. In this case the courting male mayfollow, but a cicada who continues walkingusually loses a courting male in a thicket oftwigs and leaf petioles . If a courted cicada is notreceptive but unable or unwilling to leave, e .g. if

•

3-

x• 1_OWN""1

2 sec

Court III : Magicicada septendecim

10

•

•G

" 2

0 .5

1-0 sec

Court III : Magicicada cassini,

Fig . 3 . Sonagrams of court III songs . Several phrases ofeach song are shown .

1076

it is an egg-laying female with her ovipositorembedded in the twig, she usually flicks herwings in response to the pawing contact. Thiscommonly elicits a return to the wait/pursuitstage, or the courting male may leave . If the twoinsects happen to be facing each other on abranch tip, the usual response of a courtedanimal that does not simply depart is topaw at the courter. The response of the male tothis signal is similar to that elicited by a wingflick : he either leaves or returns to the wait/pursuit stage . Even after mounting, if the courtedanimal moves, the male immediately drops off,ceases whatever song he was singing, and eitherleaves or resumes the wait/pursuit .

In Magicicada cassini there is another signal,given by a male in response to another male, thatseems to indicate non-receptivity and may beagonistic. This is a wing flick accompanied by ashort phrase of the `tick' portion of the callingsong (see Figs . 1 and 4B) . The flick-tick signal isoften given by a male who is courting a cicada infront and simultaneously being courted byanother insect behind him . The response of thesecond male to this signal can be the same as toan `ordinary' wing flick, a resumption of thewait/pursuit, or he sometimes returns theflick-tick . In the latter case there are often longsequences where the two males flick-tick at eachother for several minutes without moving . In thepresent study the flick-tick sequences were notscored as courtships because they involve singingby both partners . Females cannot sing, so itseemed unlikely that an interaction characterized

A

B

10-

= 6-r 2-

N3

i .1

2 sec

'Stutter' : Magicicada septendecim

«I nlk.atal+d lt~n~~ hi,be,ll ,

I I •1 Id q

<< n •

0 . 5

1 .0 secTick' Magicicada cassini

Fig. 4. Sonagrams of other periodical cicada sounds .

ANIMAL BEHAVIOUR, 27, 4

by reciprocal song could be courtship . Alexander& Moore (1958) have previously described thesound and the behaviour, but they included it asa part of courtship . Further studies are needed todetermine the biological function of this pattern .

To summarize periodical cicada courtship, theinitial stage includes a courting song and occurswhen a male cicada drops out of the chorus. Thesecond, approach, phase involves the movementof the courting male to within about a centi-metre or two of the courted insect while singinga courting song . The wait/pursuit stage alwaysincludes song and usually follows this approach,but it may occur at any point in courtship. Whenprobable receptivity on the part of the female hasbeen indicated by fairly prolonged immobility,the touch phase is initiated . Continued immobi-lity by the female elicits the next stage, themount, which is usually followed by copulatoryprobing, after which coupling occurs . Any of thecourtship songs may occur at any stage ofcourtship. Some courting song is necessary forthe recognition of the initial, approach, andwait/pursuit stages, but the other stages mayproceed in the the absence of song .

Methods and MaterialsAdult cicadas were observed in singing centreslocated in stands of small trees in 1970 (Brood X),1973 (Brood XIII), and 1974 (Brood XIV) .Brood numbers follow Marlatt (1907) . TheBrood X studies, in Ann Arbor, Michigan,included only Magicicada septendecim . Westudied both M. septendecim and Magicicadacassini in Argonne, Illinois, in 1973 and inBrown and Harrison Counties, Indiana, in 1974 .Observations were made throughout the day atmost of the sites . Most studies of M. septendecimwere made in the morning and of M. cassini inthe afternoon . Portable stereo cassette recorders(Sony model TC 126) were used to recordsimultaneously insect sounds and verbal des-criptions of behaviour . The microphones usedfor recording the cicada songs were fastened tothe ends of extensible poles that could frequentlybe brought to within a few centimetres of thecourting males without disturbing them. Behav-iour was sampled by simply watching for pairs ofcicadas that seemed to be interacting, bringing upthe microphone, and describing the interactionuntil it was terminated by one of the partners oruntil it was evident that it did not meet ourcriteria as a `courtship' .

A variety of objects were tested to determinetheir effectiveness in eliciting courtship by

DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS

1077

unrestrained male cicadas in the emergenceareas. These included live and dead cicadas ofboth sexes of both M. septendecim and M.cassini and black-painted wooden blocks ofdifferent sizes and shapes (Fig. 5). Some of theblocks had cicada forewings glued to their sides .All of these objects were fastened onto twigs inthe singing centre with insect pins . Most of theseexperiments were done in the monospecific hordein Ann Arbor, Michigan, with Dr R . D .Alexander in 1970, but a few additional observa-tions were made with the same objects inArgonne, Illinois, in 1973 .

Model `male cicadas' were constructed to testunrestrained females' ability to discriminatecourters on the basis of tactile and acoustic cues .Each of the models was constructed of a spring-loaded `grabber' approximately 46 cm long,with an earphone and an assemblage of soft wires(to simulate legs) fastened to the tip (Fig. 6) . Thetip with all its appurtenances was then paintedblack. The earphone led from a single pole-double throw switch that was, in turn, connectedto the outputs of one of the stereo cassetterecorders . The courtship songs ofM. septendecimwere recorded on one channel of a cassette andthose of M. cassini on the other. The songsemitted by the earphone on the model could thusbe changed by flipping the switch . Verbaldescriptions of the responses of females to`courtship' by these models were recorded on asmall monaural cassette recorder . Experiments

Fig . 5 . Wooden blocks used to elicit courtship fromunrestrained males . Each block was made of balsa wood,painted black .

using these models were done with unrestrainedfemale M. septendecim and M. cassini in emer-gence areas of Brood XIV in southern Indiana1974 .Contingency tests for x2 were run on the data

to detect differences in the male courtshipsignals and in the responses of cicadas belongingto the two species. In all cases, row-columnindependence was the null hypothesis .

ResultsIntraspecific Courships

A total of 241 spontaneous courtships ofperiodical cicadas were observed in a multi-specific emergence near Argonne, Illinois, in1973. A courtship was defined as an interactionthat included any one or more of the courtshipsongs and/or one or more of the male courtshipbehaviour patterns that could be recognized as apart of courtship without song . The latterincluded the foreleg touch, mounting, copulatoryprobing, and copulation . Magicicada septendecimcourted in 171 of these interactions and M.cassini in the other 70.

In 142 of the 171 M. septendecim courtships(83 %), the courted cicada was also an M.septendecim . These are defined as intraspecificcourtships. Seventy-six percent of the 70 M.cassini courtships were intraspecific . Homo-sexual courtships comprised at least 26 (18 %) ofthe intraspecific M. septendecim courts and atleast 4 (7-5%) of the M. cassini ones. It wassometimes difficult to determine the sex of asilent cicada at a distance so few assumptionscan be made concerning the sex of courtedcicadas .

Fig. 6. Model used to imitate male courtship signals . Thedistance from the point marked X to the tips of the`grabber' prongs was 6 . 5 cm.

1 078

Each courtship has been divided into signal-exchange bouts, each comprising some courtshippattern performed by the male and the responseof the courted cicada . In the intraspecificcourtships of M. septendecim there were a totalof 271 bouts, for an average of 1 .9 bouts percourtship . There were 145 bouts in the 53intraspecific M. cassini courtships, yielding anaverage 2 .7 bouts per courtship . Most courtshipsdid not continue to copulation but were ter-minated by the departure of one of the partners .

In the M. septendecim courtships, 158 of the271 bouts (58 %) included some courtship song ;while in M. cassini 121 of the 145 bouts (83 %)included song. It is clear that male M. cassiniwere much more likely to sing during theircourtships than were M. septendecim males(Fig. 7). The remainder of the bouts in eachspecies included courtship patterns performed bysilent males . Although a courted cicada may doseveral things in response to male courtship,including wing flicking, pawing, and leaving,either by walking or flying away, the onlyresponse that apparently indicated receptivitywas immobility. The relative `effectiveness' of acourtship signal in eliciting or detecting female

ANIMAL BEHAVIOUR, 27, 4

receptivity can thus be determined by the propor-tion of immobility responses it evoked. InM. septendecim, 106 of the 158 (67 %) malecourtship signals that included song elicitedimmobility from the females, while in 40 of the113 (35%) silent bouts the female became orremained motionless . Similarly M. cassinifemales were motionless in 67 of 121 (55%)bouts with song but in only 6 of 24 silent bouts(25 %). It is evident that bouts with song weremore effective in eliciting immobility than silentones in both species .

When the individual courtship bouts of eachspecies were compared, there were definitedifferences . Courtship of M. septendecim differedfrom that ofM. cassini not only in the acousticcharacteristics of the courting songs but also inthe proportions of typical courtship behaviourpatterns performed by the males and in theresponses of females to these signals . SilentM. septendecim touched conspecific females withtheir forelegs more often than did quiet M.cassini, both with foreleg vibration and without .They were also more likely to mount a conspecificthan were theM. cassini males. TheM. cassini, onthe other hand, performed more bouts of waiting

∎M.septendecim Courtship Bouts, N=268

®M. cassini Courtship Bouts, N=165

10111 1Touch Touch Mount Ctpum-' PIh Touch Pwsuit Wait 'Mount ' rrgoula- Iwithout with toly without with tort'Vibration Wbiation

Probing t6bration N'bratan

Probing

COURTSHIP PATTERNS without SONG COURTSHIP PAT TER N S with SONG

Fig. 7 . Male courtship patterns during intraspecific courtships . Touch with-out vibration : Male touched courted insect with foreleg using pawing motion .Touch with vibration : Male vibrated foreleg as he pawed at other insect .Pursuit: Male followed courted animal, singing, as it walked away . Mount :Male climbed onto back of courted insect . Copulatory probing : Maleprobed with his genitalia as he turned about on back of courted insect .(Copulations have been omitted, so the total number of bouts in M .septendecim is 268, not 271) .

DUNNING ET AL . : COURTSHIP IN PERIODICAL CICADAS

and pursuit than did the M. septendecim. Thesedata are shown in Fig . 7 . The differences in court-ship patterns between the species are significant atthe P = 0 .01 level, as revealed by a 2 x 10 contin-gency test for X2 .

The responses of courted cicadas of the twospecies to intraspecific courtship signals werealso significantly different at the I % level . Asexpected, there were more responses of M.septendecim to courtship without song. TheM. cassini walked away from their courters moreoften than did courted M. septendecim . In bothspecies the most common response to courtshipwas immobility. These results are shown in Fig . 8 .

In the courtship signals with song, there wereno significant species differences in the tendencyof the males to sing any one of their typicalcourtship songs. There were 113 bouts includingcourt I in M. septendecim, and 101 in whichM. cassini sang their characteristic court I song .M. septendecim sang court II in 35 bouts, andM. cassini in 26. Forty-seven of the M. septende-cim bouts included court III, as did 32 of theM. cassini bouts. These data include courtshipsof all objects during our studies of Brood XIII .Males of M. septendecim were as likely as thoseofM. cassini to sing their particular court I song ;and the same was true for the court II and courtIII songs. Males of both species, however, sangtheir court I songs more than either court II or

WA WF PaI--Bouts without song--I 4-Bouts with song-4

Fig . 8 . Female behaviour patterns during intraspecificcourtship. (Copulations have been omitted, so the totalnumber of bouts in M. septendecim is 268, not 271).FA : Fly Away . Courted insect flew away from courter .WA: Walk Away . Courted insect walked along branch,away from courter. WF : Wing Flick. Courted insectflicked a forewing at courting male behind . Pa : Paw .Courted insect pawed with foreleg at courting male infront. I : Immobility. Courted insect became or remainedmotionless near courting male.

1079

court III, . and they were about equally likely tosing courts II and III . In M. septendecim thecourt I song occasionally differed slightly fromthe normal court I in that there was sometimes aslight stutter audible between the phrases (Fig .4A). Infrequently a series of stutters was emittedwithout any of the rest of the usual phrases .Stutters alone and court I songs with stuttersseemed to elicit the same responses from thecourted animals as court I without stutters .Likewise, there were no differences between thespecies in the proportion of immobilizationresponses to the various courting songs . BothM. septendecim and M. cassini females wereequally likely to indicate acceptance in responseto the conspecific court I, court II, or court IIIsongs. When the immobility responses werecompared to the combined rejection signals inresponse to different courting songs within eachspecies, no differences were found for M. cassinifemales. A difference, significant at the P = 0 . 05level, was found for M. septendecim, in whichcourted cicadas were somewhat more likely toreject conspecific males singing court III thancourts I or II .

A total of 25 courtships of live, unrestrainedcicadas were observed in the monospecificemergence of M. septendecim in 1970 nearAnn Arbor, Michigan . Most of these courtshipshad to be detected entirely by their characteristicbehaviour patterns, as we could not reliablyrecord the courtship songs . Sixteen of thesecourtships were heterosexual, and the other nineinvolved the courtship of one male by another .The incidence of homosexual courtship inM. septendecim was thus apparently twice ashigh (36 %) in this monospecific emergence as inthe multispecific one (18 %) . These 25 courtshipsof unrestrained conspecifics comprised only 28of all the courtships observed in 1970. Theobjects of the rest of the 1970 courtships wererestrained or dead cicadas and inanimate objects .These are described in the next section .

When the behaviour patterns exhibited by themale M. septendecim courting conspecifics in theMichigan emergence of Brood X were comparedwith those used in intraspecific courtships ofM. septendecim and M. cassini in the IllinoisBrood XIII, it was evident that the incidence ofpursuits and waits was anomalously high inM. cassini and low in the M. septendecim in themonospecific horde (Fig . 9). This difference isprobably at least partly artifactual, as we werefrequently unable to record courtship songsduring the Michigan emergence, and songs are

1080

necessary to recognize pursuits and waits incourtship. The greater tendency of male M.cassini than M. septendecim to sing duringcourtship in the Illinois emergence has alreadybeen noted (Fig. 7). A more important differ-ence may lie in the high incidence of copulatoryprobing and of copulations among the Michigananimals as compared with males of either speciesin the Illinois data . The courtships in Michiganwere more often successful than those observedin Illinois in that they proceeded to copulationmore frequently. This is evident in that the act ofcoupling was seen only 3 times inM. septendecimin 271 bouts and never in 145 bouts of M. cassinicourtship in Illinois, while 6 copulations wereseen to occur in only 41 bouts in the Michiganemergence of M. septendecim . These observa-tions of the act of copulation do not include thepairs already in copula found in vast numbers inany emergence. Statistical comparisons of maleintraspecific courtship patterns among the threegroups observed (Michigan septendecim,Illinois septendecim, and Illinois cassini) revealedthat the differences were significant at theP = 0 .01 level .

Courtships of Inappropriate ObjectsIn addition to the courtships of conspecifics,

there were many interactions that included

M.septendecimBouts, Brood XIII

N= 271

ANIMAL BEHAVIOUR, 27, 4

recognizable courtship signals on the part of themale, but in which the object of his attention wasnot only not a female conspecific, it was some-times not even a cicada. These included court-ships of unrestrained members of other cicadaspecies, of cicadas pinned to twigs, of deadcicadas, of black wooden blocks (Fig . 5), and ofthe black tips of microphones . The inanimateobjects that were courted are hereafter referredto as models . The only obvious properties thatall of these objects shared were that they wereall between 2 and 6 cm long, black, slow-movingor still, and located among the twigs in theperiphery of the trees in the singing centre .

Most of the courtships of models and of deadinsects were observed in the monospecific hordeof M. septendecim in Ann Arbor, Michigan, in1970. There were no significant differences in theamount of courtship attention directed towardmodels of various sizes and shapes, nor did thepresence or absence of cicada wings on themodels seem to make a difference . The largeproportion of courtships directed to models inthese experiments is probably partly artifactual,due to our methods of studying the cicadas atthat time : we focussed most of our attention onthe wooden models and cicadas pinned to thetwigs and waited for male cicadas to court them .Relatively few of the many courtships among the

®it cassini BoutsBrood XIII : N-145 i

_M, jgptendeci mBouts, Brood XN : 41

Touch

Touch

Pursuitwithout

withVibration

Vibration

Fig . 9 . Male intraspecific courtship patterns in monospecific and multi-specific emergence area . Behaviour patterns are as described in text andFig. 7. Brood XIII was studied in an area where both species were present(multispecific emergence area) . Brood X was studied in an area where M .septendecim was the only species present (monospecific emergence area) .

unrestrained cicadas present were observed (only25, as noted previously) . Nevertheless, when weperformed similar experiments with pinnedmodels and cicadas in the multispecific horde of1973, the pinned objects received very littlecourtship attention . Wooden models werecourted only three times in the 1973 emergence .In both the 1970 and 1973 emergences therewere many more live cicadas than modelsavailable as courtship objects in an emergencearea. In each of the 1973 courtships observed ablack microphone was always within a fewcentimetres of the courting animal, though itwas not always within easy reach of an animalwalking on a twig. Under these circumstancesmany more M. septendecim than M. cassiniturned their courtship attention from the cicadathey had been courting to the microphone tip .The proportions of courtships directed towarddifferent objects are shown in Fig . 10 .When the courtships of models and of con-

specifics were compared for all M. septendecimcourtships, pooling the Michigan and Illinoisdata, several differences appeared . There were

Intraspecific®Interspecific-Mode ls andDead Cicadas

V

° 75CN

7OUCNUda

BROOD XIII

100

25

N =70

DUNNING ET AL . : COURTSHIP IN PERIODICAL CICADAS

N=171

nlrnueg

N=89

M.cassini Mseptendecim Mseptendeclm

BROOD X

Fig. 10. Male courtships directed at different objects .Intraspecific : Object was a live, conspecific cicada ofeither sex . In Brood X many of these live cicadas wererestrained . Interspecific : Object was a live cicada ofanother species . None of them were restrained . Modelsand Dead Cicadas : Object was a model (defined in text)or a dead cicada pinned to a twig .

many more episodes of pursuit and waiting whilecourting conspecifics than models, and far moreof the courtships of models proceeded tocopulatory probing than did those of con-specifics . The males also touched the modelswith their forelegs less than they did in intra-specific courtships . The differences between thecourtships of models and of conspecifics aresignificant at the P = 0 . 01 level, and are shownin Fig. 11. The average number of bouts in thecourtships of models was 2 . 1, only slightly morethan the mean number of bouts in intraspecificM. septendecim courtships .

In addition to courtships of inanimate anddead objects, male cicadas of each speciesoccasionally courted unrestrained members ofthe other species in a multispecific emergencearea. These are defined as interspecific courtshipsand were much more frequently performed byM. cassini than by M. septendecim . MaleM. septendecim courted M. cassini only 7 timesin the 171 M. septendecim courtships observed .There were a total of 15 bouts in these 7 court-ships, for an average of 2 . 1 bouts/courtingsession . This is similar to the mean number ofbouts in the courtships of other objects byM. septendecim . Male M. cassini, on the otherhand, courted M. septendecim in 15 out of the70 M . cassini courtships observed . This differencein the proportions of intraspecific and inter-specific courtships in the two species is significantat the P = 0 .01 level . There were 36 bouts in the15 interspecific M. cassini courtships, yielding an

50

40N7O

30_aO

O20a)

Ud)0

10

C-1 Intraspecific courtship bouts, N =303

Bouts courting models and deadCicadas, N=120

Pu ,

1081

Fig. 11 . Male M. septendecim courtship behaviourpatterns directed at different objects in both Brood Xand Brood XIH . Objects have been described in text andin the legend of Fig . 10. ToV: Touch without vibration .T + V : Touch with vibration. Pu : Pursuit, with court-ship song. W: Wait, with courtship song. M: Mount.CP : Copulatory Probing. Copulations are excluded.

1 08 2

average bouts/courtship of 2 .4. This is somewhatless than the 2 .8 bouts/courtship average forintraspecific courtships in M. cassini . The timesof day when interspecific courtships wereobserved were usually those appropriate to thecourting male. Courtships of M. cassini byM. septendecim were seen mostly in the morning ;those of M. septendecim by M. cassini mainly inthe afternoon .When the interspecific courtships were

examined in detail, it was evident that therewere few differences between the species in theirinterspecific courtships . There were no significantdifferences between the two species in malebehaviour during interspecific courtship . Therewas not even a species difference in the propor-tion of signals that included songs as comparedto those that did not, unlike the intraspecificcourtships in which M. cassini sang much moreoften than did M. septendecim . There were alsono significant differences in the responses ofcourted cicadas of the two species to intraspecificcourtship .

When intraspecific courtships were comparedto interspecific ones within each of the twospecies, significant differences emerged only forM. cassini (Fig. 12). Male M. septendecimcourted the same way, and individuals of thisspecies responded in the same way, regardless ofwhether or not the courtship partner was aconspecific. InM. cassini, on the other hand, themales proceeded much further in their courtshipsof members of other species than they usually didin intraspecific courtships . There were propor-tionately more interspecific bouts includingmounting and copulatory probing than intra-specific ones . Courted M. cassini pawed atcourting M. septendecim more than they did attheir conspecifics . The M. cassini differences inthe patterns of both male and female behaviourin interspecific and intraspecific courtship weresignificant at the I % level .

Responses of Females to Courtships by ModelsAlthough there were definite differences both

in the songs and in the proportions of variouscourtship patterns performed by males of thetwo species, it seemed that only the females ofM. cassini responded to these differences .Accordingly we attempted to court females ofboth species with a totally inappropriate object,the model shown in Fig . 6. Although the modeldid not visually resemble a cicada, except inbeing black, it could generate signals similar tomost of the tactile and auditory cues common to

ANIMAL BEHAVIOUR, 27, 4

courtship by the males of both species . The longwire was used to touch the female, in a mannerthat approximated the pawing action of theforeleg contact, although we could not vibratethis `foreleg' as the cicadas sometimes did . By

MALE COURTSHIP PATTERNS

Olntraspecific

•Interspecific50N

00.c00 2500C00Uaa

W 50

0.000254-

Ca,ULa,a

_1i ,1-PP .ToV PuW MCID ToV PuW MCP

T+V

T+V~-M. septendecim -+ ' M. cassini--~C3N=268

ON=145N= 15

• N=36

FEMALE COURTSHIP PATTERNSOlntraspecific .Interspecific

FA WA WF Pa I FA WA WF Pa I

Fig. 12. Comparison of intraspecific and interspecificcourtship patterns for cicadas of both species and sexes,Brood XIII only. Male courtship behaviour patternsdescribed in text and in the legend to Fig. 11 . Femalecourtship behaviour patterns described in text and in thelegend to Fig. 8 . Intraspecific courtships : the partner wasa conspecific . Interspecific courtships : the partner was amember of the other species . In 15 of these bouts the malewas an M. septendecim and the female an M. cassini.Male M. cassini courted female M. septendecim in 36bouts.

4M. septendecim .- M. cossinl,o N=268 C:3 N=145= N=36 = N=15

DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS

attaching the model to a twig near a female withthe grabber prongs the model could perform thelong waits with song common to both species .Moving it slowly behind a walking femalemimicked the pursuits . If a female remainedmotionless when touched several times with thelong wire, the model was lifted onto her back sothat the short wires touched her, and it wasgently bounced about to imitate the motions of amounted male, though nothing very similar tothe copulatory probing of a real male could beattempted .

A series of courtship songs of each species wasrecorded on a cassette, proceeding from court Ithrough court II to court III . The songs of onespecies were recorded on one channel of the tape,and those of the other species on the otherchannel. The series of songs was then repeated oneach channel until the tape was full . Becausethere were no significant differences in theproportion of acceptances in response to dif-ferent courting songs in either of the species inthe courtships performed by conspecific males,as already noted, it was considered that all songsof a species were equivalent in elicitingimmobilization. So, although we could notpredict what song would be emitted by theearphone at the onset of any courtship, andthough any song could be played during each ofthe mimicked courtship behaviour patterns,these intraspecific song variables were consideredrelatively unimportant in determining the re-sponses of the females thus courted .

There were 50 courtships of unrestrainedfemale M. septendecim using the models and48 of female M. cassini . There were 344 bouts inthe 50 M. septendecim courtships, for an averageof 6 .9 bouts/courting session . There were 620bouts when courting female M. cassini, for amean of 12 .9 bouts/courtship. It is clear that wewere much more persistent in our courtships offemales with the models than were the malecicadas. The experiments on M. septendecim weredone during periods of maximum septendecimchorusing in the morning, and those on M.cassini in the midst of loud, synchronized cassinichoruses in the afternoon .

In each of the courtships by models there werefar more bouts in which the song played from theearphone was intraspecific rather than inter-specific. Female M. septendecim were courtedwith septendecim song in 298 of 335 bouts withsong, and M. cassini females were courted withcassini songs in 409 of 571 bouts with song .There were relatively few bouts in courting

either species when the tape recorder was turnedoff so that there were no sounds at all emittedfrom the earphone.

A comparison of the immobility responses offemales of the two species to courtship by themodel showed that there were no differencesthat could not be accounted for by the differentproportions of courtships with no songs,conspecific songs, and allospecific songs . Becauseof the ambiguity of the immobility `response'(a female may or may not have `responded' to amodel when she did nothing), courtship boutsinvolving a moving female and model wereexamined. There were a total of 239 bouts of thissort involving M. cassini females, and 141 boutswith M. septendecim females. A female wasjudged receptive to courtship by the model if shestopped moving as it pursued her, with orwithout touching her with the long wire . She wasconsidered unreceptive if she continued walkingor flew away when pursued, with or withouttouch, by the model. The results of this analysis,shown in Fig. 13, indicate that the responses of

hi ca ssin i Acceptances

®M.seatendecim Acceptances

M.cassini Rejections

M.septendecim Rejections

100-

1083

0-N-15

N=7

N :176 N ;11

N :46 N.123NO SONG

M.cassini SONG

M.-decim SONG

Fig . 13 . Responses of intact females to courtship bymodel. Model described in Fig. 6 and in text . Songs wereemitted from earphone on model . Responses of femaleswere scored as `Acceptances' if she ceased moving and as`Rejections' if she continued to move while the modelpursued her, with or without touching her .

1084

ANIMAL BEHAVIOUR, 27, 4

female M. septendecim were not significantlydifferent from those expected on the basis of thedifferent proportions of the three types ofcourtships (x2 = 4 .97 ; df = 2 ; 0 . 05 < P < 0 . 10) .On the other hand, the M. cassini females'responses were significantly different from theexpected proportions at the P = 0 .05 level (X2 =6 .26; df = 2) .

DiscussionThere are many similarities in the courtshipbehaviour of the two species of periodical cicadasstudied. Both species sing courtship songs, eachof which is radically different from the songs ofthe other species but bears a similar relationshipto other songs within each species . These songscomprise a continuum of gradually increasingtempo, and our division of this gradation intothree stages is necessarily arbitrary . These songshave been previously described and soundspectra published by Alexander & Moore(1958, 1962) . The first courting song is identicalto the calling song but there are more phrases,and the flight that terminates a sequence ofcalling does not occur following court I in eitherspecies. The other two courtship songs in bothspecies exhibit phrases of the calling songs thatare progressively shortened, as are the interphraseintervals, resulting in a sequence of songs withgradually quickening cadence . The phrasesimilarities in the various songs of each speciesare typical of the acoustic courtship sequencesfound in other insects, such as the cricketsstudied by Alexander (1960) and the grasshoppersstudied by Perdeck (1957) .

Another similarity in the acoustic courtshipsof these two cicada species is in the evidentabsence of differential female response to thevarious courting songs. They react the same wayto all of them within each species . The differencesbetween the songs may not, therefore, indicate adifferent signal function for the increasing tempo,but might reflect the increasing excitement levelof the'individual singing .The behaviour patterns exhibited by both

males and females of the two species are alsosimilar. As Alexander & Moore (1958, 1962)have noted, the initial acts that bring periodicalcicadas of the two sexes together are firstacoustically and second visually mediated . Theaggregation of conspecific cicadas in a singingcentre is a consequence of the chorusing behav-iour of the males singing their calling songs . Theapproach of an individual male cicada to afemale within the singing centre is apparently

visually mediated, although the visual stimulusnecessary to elicit this approach seems to beextremely generalized. There are apparently noneof the specific visual sign stimuli common inbutterflies, for example (Crane 1955 ; Emmel1972) ; rather a male cicada approaches any darkblob in the singing centre, even though it may bevery different from a female in both size andshape. The generality of the stimulus is similar tothat eliciting courtship in several bugs, somedipterans, and the cockroach Gromphadorhina(Markl 1974) . In the latter cases, though, anymoving object of about the right size is ap-proached, while in cicadas the object must bedark and still . The generality of the visualstimulus adequate to elicit courtship approach isprobably partly a consequence of the highpopulation densities in a periodical cicada sing-ing centre, where most of the small, dark blobsare cicadas .

If the adequate stimulus for courtship is such avague, visual one, it is difficult to understand whymost of the courtships in both species wereconspecific . There were many cicadas of bothspecies in the multispecific emergence sites and,in spite of the allochrony in the level of activityof the two species (Alexander & Moore 1958,1962), there were large numbers of insects of bothspecies active throughout the day . On windless,hot, sunny days members of even the relativelyinactive species were usually perched on thebranch tips rather than in along the majorbranches and trunks of the trees . They weretherefore in an optimum position to act ascourtship targets for males of the more activespecies, yet they received relatively little court-ship attention . Because most of the courtshipsobserved were already beyond the initialapproach stage when we detected them, it seemslikely that the very general cues are adequateonly for this very early phase of courtship, andthat its continuation depends on other informa-tion .

The continuation of courtship in both speciesapparently depends upon the behaviour, or thelack thereof, of the courted insect. If the courtedobject remains still, courtship usually continues,but it may be broken off if the courted animalmoves. Usually the movements that serve todisrupt courtship, the rejection signals, are large,fairly obvious motions. This is especially true ifthe rejection occurs when the courter is somecentimetres away. At this distance the rejectionis signalled by the departure of the courted insect,either by walking or flying away . When the

DUNNING ET AL . : COURTSHIP IN PERIODICAL CICADAS

partners are very close together, as following aforeleg contact, rejection may seem more subtleand involve the movement of only a part of thecourted insect, e .g. a wing or a leg. These close-range rejection signals are similar to those usedby male and unreceptive female Drosophila whencourted (Bastock 1967) . Differences in the degreeof rejection communicated by the various signalsare evident in the varying responses of thecourting males to them. Courtship is inevitablyterminated by flight of a partner, even if theinsect doesn't fly very far, while it may continuein the pursuit or waiting stage following depar-ture by walking or after one of the wing or legsignals. In these cases, persistent repetition of therejection signals is sometimes necessary toterminate the courtship . The unreceptive insectmust keep walking or repeat the wing flick or legmotion several times before the courting maleleaves. It seems that a mild degree of rejection isusually sufficient to prevent copulation, althoughcourtship may continue. Therefore an unrecep-tive cicada will reject contact with a courtingmale but suffer him to continue singing hiscourting songs close by . This is evident in thecomparative responses of courted insects of bothspecies to contacts as opposed to waits inintraspecific courtships . M. septendecim rejected71 of 111 foreleg contacts and 15 of 23 mounts,but remained motionless during 83 of 101 boutsof courtship waiting . Similarly, M. cassinirejected 26 of 37 foreleg touches and 2 out of3 mounts, but sat still during 60 of 71 bouts ofwaiting .

Female sexual receptivity in periodical cicadas,as in many other insects, is indicated by immo-bility. This also occurs in at least one hymenop-teran (Markl 1974), several orthopterans (Huber1960; Miller 1965 ; Alexander & Otte 1967 ;Roth & Barth 1967 ; Spooner 1968) and in somenymphalid butterflies (Myers & Brower 1969 ;Emmel 1972). The response evidently facilitatesthe efforts of the male to insert and attach hisphalomeres and/or the spermatophore to thegenital apparatus of the female. In spite of theevident importance of female immobility inmating behaviour, however, it is dangerous toassume that stillness indicates sexual receptivity .It can probably reflect other states as well . Theabsence of movement, in many cases, seemsequivalent to an absence of behaviour, andshould be interpreted with caution. A motionlesscicada may be resting, feeding, frightened, sick,wounded, dead, sexually receptive, or doingnothing because it is unnecessary to do anything .

1085

There are so many cicadas in a singing centrethat any individual not moving probablybecomes a courtship target very quickly . Toprevent courtship an insect would have to movealmost constantly, as do the chorusing males . Asmovement is metabolically expensive, a conserva-tion of effort on the part of courted cicadas ofboth sexes is probably adaptive . It appears that,although immobility was the most frequent`response' to male courtship, it probably did notusually indicate sexual readiness but simply anunwillingness to move unless some definiterejection signal was necessary to prevent copu-lation. It is apparently as difficult for a malecicada to interpret absence of movement inanother cicada as it is for us, and a male con-fronted with a non-moving, cicada-like objecttreated it as a possibly receptive female con-specific and courted it . This may explain why sofew courtships were successful in either species .It would also explain why the models continuedto be so attractive as courtship objects, as theyseldom moved .

There appears to be no particular disadvantageto the females in long, fruitless courtships, asthere are plenty of males available when thefemales are ready for mating, and copulation caneasily be prevented upon contact when they arenot. The disadvantage would seem to be with themales, who are thus persuaded to spend largeamounts of time and effort singing courting songsand chasing silent cicadas with very little hope ofmating with the individual courted . Since so fewcourtships proceeded to copulation, it is difficultto understand the selective advantage of suchpersistent courtship, in spite of even mildrejection signals, by males of either species . Theprobability of mating in any given courtship is solow, and the rate of copulation in the populationas a whole is so high, as shown by the largenumber of pairs in copula and by the evidentreproductive success of these cicadas, that itwould seem advantageous for a male to terminatea courtship at the first hint of rejection and seekanother partner . Nevertheless . however wastefulthe process may seem to us, it is evidentlysufficiently effective to permit enormousnumbers of these cicadas to mate and pro-duce viable offspring.

The initial contact between the courtshippartners occurs the same way in both M .septendecim and M. cassini. The males of bothspecies sing while close to but not touching thefemale, and their first, tentative contact with thefemale is usually made with the foreleg. This

1 086

ANIMAL BEHAVIOUR, 27, 4

behaviour is different from the initial contact inmany other insects whose courtship behaviourhas been extensively studied, such as crickets(Alexander & Otte 1967), katydids (Spooner1968), cockroaches (Roth & Barth 1967), andbutterflies (Myers & Brower 1969). In theorthoptera and lepidoptera studied, the firstcontact between the partners is usually made bythe antennae of at least one of the insects . Inmost of the orthopterans, the antennal stimula-tion is probably primarily mechanical, while ithas been shown to be chemical in queen butter-flies (Myers & Brower 1969) . The antennae ofcicadas are very short, so that the insects' bodieswould have to be practically touching before theantennae could contact the other insect . Themanner of both early antennal touching duringcourtship in other insects and of foreleg pawingin periodical cicadas suggests that body contactat this stage of courtship is somehow inappropri-ate. Whether the touch is made by the antennaeor the foreleg, it is brief, and either the appendageor the body of the partner is withdrawn beforethe next stroke . There appears to be no behav-iour pattern in periodical cicadas similar to theantennal lashing evident during later courtshipin some orthopterans (Alexander & Otte 1967 ;Roth & Barth 1967), although there wereoccasional foreleg `boxing matches' betweencicadas facing one another on a twig . Theseoccurred infrequently, when a courted cicadaresponded to a male's foreleg contact by pawingback at him, and the male, in turn, pawed again .

In addition to the similarities in the courtshipbehaviour of cicadas belonging to these twospecies, there were also marked differences . Onedifference is reflected in the different numbers ofcourtships observed among animals of the twospecies. Many more M. septendecim courtshipswere observed than those of M. cassini . Indivi-dual M. cassini were much more likely to bedisturbed by the microphone used to detect andrecord any songs sung during courtship thanwere the M. septendecim. When the microphonewas brought close to a pair that may have beencourting, one or both of the cicadas were morelikely to fly or fall away if they were M. cassinithan if they were M. septendecim . Greaterdisturbance of M. cassini courtships by themicrophone is also reflected in the differentproportions of courtships directed at this black,gently weaving object by cicadas of the twospecies (Fig. 10) . M. septendecim males oftenapparently mistook the microphone for a femaleconspecific and courted it, while male M. cassini

were evidently more aware that it was somethingdifferent and were frequently frightened by it .Those M. cassini who were not frightened

away by the microphone were more persistent intheir courtships than were the M. septendecim,so that the average number of bouts in the M.cassini courtships exceeded those of the M.septendecim courtships. This greater persistenceis also evident in the proportions of pursuits andwaits performed by males of the two species .Figure 7 shows that male M. cassini were morelikely to chase a cicada that walked away duringa courtship and to remain close by a motionlesscicada, singing, than were the M. septendecimmales. On the other hand, the M. cassini maleswere less likely to touch a courted insect thanwere the M. septendecim . These data suggestthat an M. cassini courtship is a longer affairthan that of M. septendecim . A male M. septen-decim approaches and proceeds to a foreleg-touch stage fairly quickly and is more likely toterminate courtship after receiving even a mildrejection signal . A male M. cassini responds to awalk-away rejection by following and to a wingor leg flick by continuing his song nearby .

The greater ease with which an M. septendecimcourtship can be terminated compared to that ofM. cassini also results in differences in inter-specific courtships . The males court the same waywhether they are courting conspecifics ormembers of the other species, but the M. cassiniusually proceeded further when courtingM. septendecim than M. cassini. This may bebecause M. septendecim females typically rejectcourtship with relatively subtle gestures, whileM. cassini females are more obvious and usuallyleave (Fig. 8). M. septendecim males terminatecourtship in reaction to the subtle rejections oftheir conspecifics, but male M. cassini do not .They proceed with an interspecific courtship eventhough they have been rejected . Since maleM. cassini more often responded to a mildrejection signal by continued courtship than didM. septendecim, the courtships ofM. septendecimfemales by M. cassini males continued muchlonger than the courtships ofM. cassini femalesby M. septendecim males. Even though the maleM. cassini were less likely to touch a courtedcicada during courtship than were the M.septendecim, if they did get to the contact stageit was more likely to occur with an M. septende-cim than with a conspecific cicada (Fig . 12) . Thisprobably occurred because courted M. cassinigenerally terminated a courtship earlier byleaving . Oddly enough, another difference

DUNNING ET AL . : COURTSHIP IN PERIODICAL

between intraspecific and interspecific courtshipsin male M. cassini patterns was in contactsbetween the partners while the male was singingas opposed to silent bouts . These were morefrequent in interspecific than in intraspecificcourtships. This is startling, but it should beremembered that there were relatively few boutsinvolving either contact or silence in M. cassini(Fig. 7), so this difference may be more apparentthan real .The M. cassini males were much more likely to

sing during courtship than were theM. septende-cim, although bouts with song were moreeffective than silent ones in eliciting immobilityin both species . One reason for this differencemay lie in the relative proportions of behaviourpatterns that require song to be identified as apart of courtship in the two species . There weremore bouts of identifiable courtship patternsthat did not require song, i .e. bouts includingcontact between the partners, in M. septendecimthan in M. cassini. Therefore only those inter-actions that included song were likely to berecognizable as courtship in M. cassini .

The adaptive significance of the two differentcourtship techniques, the slow, persistent one ofM. cassini and the fast, easily rejected method ofM. septendecim . is evident when the typicalresponses of females of the two species areconsidered . The slow courtship is difficult to term-inate unless the female leaves precipitously, butthat is precisely what the unreceptive female M.cassini is likely to do. If she does not fly away, thecourtship will probably continue, but contact isrelatively unlikely so the consequences oftolerating the singing male are not serious . On theother hand, a female M. septendecim who doesnot promptly indicate her non-receptivity islikely to have a male crawling over her fairlysoon. She can, however, signal a rejection with-out a great deal of effort, and that will probablyterminate the courtship .Not surprisingly, the courtship behaviour

patterns typical of the two sexes in each of thespecies are mutually adapted, but problemsseem to arise when interspecific courtships occur .The more easily rejectedM. septendecim males donot long continue an interspecific courtship, butthey are more easily diverted by other black,stationary objects (such as microphones) in thecourting area. This suggests that theM. septende-cim males initiate more courtships than do theM. cassini. A non-receptive M. cassini femalemay have to spend a lot of effort flying away fromthe unwelcome attentions of conspecifics in

CICADAS

1087

order to terminate courtships, but she mayreceive courtship attention from fewer males thando female M. septendecim. The problems mayarise when many easily deterred male M.septendecim wear out female M. cassini whoover-react to their courtships ; while femaleM. septendecim under-react to courting maleM. cassini and thus encourage them to wasteeffort in courting. When the two species are bothtemporally and spatially sympatric one wouldpredict that their courtship communicationstrategies would converge, so that they 'under-stand' each others' rejection signals more fullyand react accordingly . At the same time, therecould be selection for increased spatial andtemporal separation of the two species, so thatinterspecific communication would become lessimportant .In either case stronger selection would be

predicted for interspecific mate discriminationin both sexes in multispecific hordes than inareas where all the cicadas are members of asingle species . The great propensity of maleM. septendecim to court such inappropriateobjects as microphones indicates that theseinsects may be less discriminating than maleM. cassini with respect to the objects of theircourtship . When the courtship proclivities ofM. septendecim in the monospecific emergenceof 1970 were compared with those in the multi-specific Illinois emergence of 1973 (Fig . 10), it isevident that the cicadas in the multispecific hordewere much less likely to court models than werethose in the monospecific emergence . Thissuggests that they were able to discriminateamong courtship objects in situations where itmight be important, i .e. where a `mistaken'courtship object may well be a member ofanother species, but they were less discriminatingwhen there were fewer chances for errors . Thebasis for such mate selection by males remainsunknown .

The enormous differences in the proportionsof such advanced courtship behaviour patternsas copulatory probing and copulation in the1970 emergence compared with the observationsin 1973 suggests that the probability of success incourtship (copulation) was much higher in themonospecific than in the multispecific emer-gences . This may mean that the early courtshiptactics of these cicadas were similar under thetwo circumstances but that the results of thecourtships were very different, so that behaviourpatterns with a high probability of success in amonospecific horde were much less likely to

1088

ANIMAL BEHAVIOUR, 27, 4

result in copulation in multispecific emergenceareas. This is probably an unstable situation,indicating that multispecific emergence areas arerare and/or a relatively new development in theevolution of these insects . The work of Dybas &Lloyd (1974) shows that these two species arecommonly found in slightly different habitats .The studies reported in the present paper ofareas where they overlap indicate that theanimals manage to maintain reproductive isola-tion even in the same habitat . As Dybas & Lloydhave noted, multispecific emergence sites aremost common in disturbed areas where there aremany small trees of several species . It seemsprobable that such sites will not decrease inabundance as long as man and agriculturepersist. Because their life cycles are so long,periodical cicadas probably evolve very slowly,and the relative abundances of disturbed andmature woodlands in the distant future aredifficult to predict . However, insofar as multi-specific hordes continue to exist, there should befurther selection for . divergence of male courtshipsignals (already evident in the different songs)and for convergence of both the female rejectionsignals and of the male responses to them .

In spite of the cicadas' difficulties in inter-specific communication, it is evident that femalesare able to reject effectively males of otherspecies and that intraspecific courtship issufficiently effective for reproductive success .Although most courtships were unsuccessful, itis probable that many, if not most, survivingfemales do copulate and lay viable eggs . It is alsoevident that the copulations were almostinvariably intraspecific .

Most of the courtships observed in bothspecies were intraspecific . If males in the singingcentres courted silent cicadas sitting on peripheraltwigs completely at random they would probablycourt more members of their own species than ofothers . There are two reasons for this, both ofwhich have been noted by Alexander & Moore(1962) and by Dybas & Lloyd (1974) . Becauseconspecifics are attracted by the calling songsof the males and the songs of the two species aredifferent, there is often, even within a multi-specific emergence, some geographical separa-tion of singing centres of the two species. Thisseparation may be very slight, so that there aremore M. septendecim on one tree and moreM. cassini on an adjacent one that may be only afew feet away. There is also a daily allochrony inthe time of maximum chorusing and therefore ofmaximum courting activity in the two species, so

that even when both species are found in thesame trees, the males of the two species aresinging and the females are on the peripheraltwigs primarily at different times of day . Therecan be much overlap, both in space and time,between the species in a multispecific emergencesite, so these separation mechanisms are far fromperfect .

If, as seems to be the case, unsuccessfulcourtships are commonly terminated following arejection signal by the courted insect, what arethe criteria used by the females to discriminateamong the males that court them? If the femalesdid not discriminate at all but merely acceptedcourting males at random in a multispecificemergence area, one would expect the sameproportion of interspecific copulations as therewere interspecific courtships ; that is, 4interspecific pairs including male M. septendecimand 21 % pairs in which the female was M.septendecim and the male M. cassini. Actuallyinterspecific copulating pairs are extremely rare .Dybas & Lloyd (1962) found only 7 in 771 pairs,and we have found but one . The female of thispair was a dead M. cassini. We do not know ifshe was dead when coupling occurred .Although the absence of movement may not

indicate sexual receptivity, since most females ina singing centre are motionless, cessation ofmovement may, indeed, signal acceptance ofcourtship . The responses of moving females tocourtship by the models (Fig . 13) indicated thatthey were not very discriminating under theserather peculiar circumstances . All the femalestended to keep moving when courted by themodel and were therefore judged non-receptive .Only the M. cassini females were shown todiscriminate : they were more likely to stop inapparent response to the songs of their ownspecies than when the song from the earphonewas that ofM. septendecim or when there was nosong from the model . Magicicada septendecimfemales did not discriminate as much . Simmonset al. (1971) have shown that the frequencyspectra of the calling songs of the two species arequite different and that their auditory sensitivitiesmatch their respective acoustic output . Since thenon-acoustic courtship patterns are similar forthe two species, it is scarcely surprising that thisacoustic information was apparently used by thefemale M. cassini in discriminating amongcourters .Although females could rely on acoustic

differences between the species-specific songs ofcourting male cicadas to differentiate among

DUNNING ET AL . : COURTSHIP IN PERIODICAL CICADAS

them, it is evident that they do not always do so .Female M. septendecim were often `receptive'(immobile) to courting contacts with silent males.Indeed 35 % of the courtship patterns withoutsong elicited immobility in M. septendecim . Allof these were intraspecific courtships, so theresponses of the females were appropriate, atleast in terms of the species of the male . Thequestion remains as to how the females knew towhich species the courting male belonged inthese cases . The answer is unknown, though wemight postulate that the males had been singingearlier in each silent courtship and that thefemales had already made their decisions beforewe began to observe the interactions. In two ofthe six observed copulations in the Michiganemergence of 1970 and in one of the threecopulations seen in Illinois, the whole courtship,from initial approach through copulation, wasrecorded. There were no songs produced at all .These results remain inexplicable, although wemay hypothesize the existence of other sensorycues, perhaps pheromonal ones .

In spite of these apparently anomalous results,it appears that the primary sensory informationused by female periodical cicadas to discriminateamong courting males is acoustic. Certainly themodels' visual resemblances to male cicadaswere minimal, and the tactile signals generatedonly clumsily similar to those used by real malesin courtship . Yet the females tolerated contactwith these blundering models amazingly well .Differential responses could only be detectedwhen a female cicada was moving . Although thedifferences were not significant for M.septendecim, even these females did `accept' morecourtships from the model when it was singingconspecific songs, as opposed to the songs of theother species or none at all. The models were muchmore persistent in their 'courtships' than werethe M. septendecim males, in that there weremany more bouts in each courtship. In this themodels' courtship `strategies' were more similarto those of M. cassini than to M. septendecim .This very persistence, then, may have mediatedthe females' apparent responses, rather than anyacoustic differences . The female M. septendecimunder-reacted to the models' courtships as theydid when courted by live M. cassini males. Theywere unreceptive and had so indicated by movingaway. The fact that they later stopped may havebeen unrelated to the behaviour of the courtingmodel, although both we and the courtingM. cassini may have interpreted this as accep-tance of courtship . Cicadas of both sexes of

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M. septendecim appear to be less discriminatingthan those of M. cassini. The males courtinappropriate objects more often, and the femalesappear to accept inappropriate courtships moreoften. Although the responses were not statisti-cally different, they may be different enough tomaintain species separation in a multispecificsinging centre . Because M. cassini do discrimi-nate better, the consequences of M. septendecimbehaviour are not detrimental to the mainte-nance of species integrity, as long as only the twospecies are present in the same place at the sametime .

The results of all of these studies demonstratethat, in periodical cicada emergence sites whereboth Magicicada septendecim and M. cassiniare actively courting, reproductive isolation ismaintained mainly through mate selection byfemales who use acoustic differences betweenthe songs of the males of the two species todiscriminate among them .

AcknowledgmentsWe thank Dr Richard D. Alexander, with whomthe senior author worked on Brood X in Michiganin 1970 . Dr Alexander was most generous of timeand research space for a novice cicada personand provided an exciting introduction to work onthese animals . He also read and criticized anearly draft of this paper .

The 1973 experiments were done on sites madeavailable by the Argonne National Laboratoryin Argonne, Illinois . Dr Jerry Klein kindlysponsored us there, and the laboratory providedtrailer parking space on the grounds . IndianaUniversity, through Dr Roderick Suthers,generously provided camping and laboratoryfacilities at the University field station for the1974 experiments on Brood XIV. We thankDrs Klein and Suthers and their respectiveinstitutions for all their assistance .

We are indebted to Dr Tom Moore, Dr MonteLloyd, Dr JoAnn White, and Christine Simon forrewarding discussions of periodical cicadabiology.

The 1973 and 1974 experiments were supportedby a grant from the National Institute of MentalHealth, No. MH-21076 .

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(Received 7 August 1978 ; revised 4 December 1978 ;MS. number : A2194)