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

COURTSHIP IN TWO SPECIES OF , 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 and M. cassini, was studied in the field during the 1970, 1973, and 1974 emergences of these . In areas where 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 females were `courted' with models that could imitate some of male courtship, they were more receptive when the models' `songs' were those of conspecific males . Acoustic differences between species are probably used by females in mate selection, maintaining species separation even in areas where the two species overlap in both space and time.

Introduction It is highly probable that the three species in a Broods of periodical cicadas synchronize their brood do normally remain separate. Although life cycles such that the adult insects emerge interspecific copulation is possible if the females together after nearly 13 or 17 years of subter- are restrained, it seems almost never to occur in ranean life . Within each brood there may be up nature (Alexander & Moore 1958 ; Dybas & to three congeneric species, each of which can be Lloyd 1962 ; White 1973) . Copulation usually distinguished with difficulty on morphological continues for an hour or more, and insects in grounds but whose males sing quite distinctive copula are easily observed in an emergence area . songs (Alexander & Moore 1962) . The three Members of a copulating pair are almost species in a 17-year brood are different from each invariably seen to be of the same species (Dybas other but apparently indistinguishable from the & Lloyd 1962 ; White 1973). three species in a 13-year brood (Simon in press). There are several possible mechanisms that Within a 13-year brood the species are as easily could operate to keep the three species within a discriminated as within a 17-year brood . Since brood separate . Lloyd & Dybas (1966) and even those 13- and 17-year broods whose Dybas & Lloyd (1974) have suggested that emergence areas overlap geographically only Magicicada cassini are primarily insects of the emerge together as adults every 221 years, the lowland forest canopy, while M. septendecim are 13- and 17-year species have been considered most often found in upland woodlands . The separate, sibling species (Alexander & Moore ease with which monospecific copulating pairs 1962), though recent evidence suggests closer and ovipositing females of all species can be genetic relationships (Simon in press) . found within a small, multispecific emergence Within a brood, the three species are usually site suggests that, though these insects probably found in slightly different habitats (Dybas & were geographically isolated in different habitats Lloyd 1974), but they can sometimes be found when they originated and may remain separated together within a small emergence area, in mature woodlands, they are now frequently encompassing perhaps a few hundred square spatially sympatric, especially in areas under- metres. The males of all species commonly sing going secondary succession (Dybas & Lloyd on the same twigs under these circumstances, 1974). often at the same time. Females frequently sit on Alexander & Moore (1962) noted that, even in branch tips within a few centimetres of members a multispecific emergence site (that is, one where of other species . Insects of each species, then, periodical cicadas of more than one species have ample opportunity to hybridize with emerge in the same year), the chorus of songs of members of other species under these circum- each species reached a peak intensity at a stances, and thus may face particular difficulties different time of day . Thus it is possible that in maintaining their own species integrity . allochrony, involving differences in the time of

1073

1074 BEHAVIOUR, 27, 4

maximum activity, may aid in the maintenance phrase or two of their calling song, fly a short of species integrity . The allochrony is far from distance, land on a twig and sing again, fly to perfect, and there are frequently periods when another twig, sing, and so on . In Magicicada cicadas of several species are courting simulta- cassini the males may synchronize the phrases of neously. their calling songs so that they all sing each As a third alternative method of species phrase together, fly together, sing again, etc . This separation, the insects themselves may dis- aggregation phase has been amply described and criminate among the various sexual partners analysed by Alexander & Moore (1958) . available and choose members of their own Normal courtship begins when a male drops species, even though they may now be both out of the sing-fly chorus and remains on a twig spatially and temporally sympatric . Once specia- while continuing to sing. In a dense singing tion has occurred the mechanisms of character centre he will probably be within a few centi- displacement would predict that such discrimina- metres of another cicada, which, if it is silent, may tions would be selectively advantageous (Brown be a female. If the singing centre is multispecific, & Wilson 1956) . The marked differences among that is if more than one species is chorusing in the songs sung by the males of the various the same area, no assumptions are possible species suggests that acoustic cues may be of regarding the probable species of other cicadas central importance in behavioural species dis- in the vicinity . The song that the male sings crimination by the insects themselves . Simmons during this stage is indistinguishable in cadence et al. (1971) have shown that the differences in and form from his calling song, but it is called sound frequency spectra of the songs are matched court I (see Fig . 1) because of the different by the insects' auditory sensitivities . Of course, it circumstances in which he sings it . Since the is quite possible, if not probable, that differences males usually sing only two phrases of their of habitat, time of maximum activity, and calling song between flights, any sequence interspecific behavioural discrimination all comprising four or more phrases without flight operate together to maintain species integrity in has been designated as court I . This stage has emergences of periodical cicadas . also been described by Alexander & Moore Immediately below we shall provide a sum- (1958), though they did not consider it a part of mary of the behaviour sequences and songs courtship. involved in periodical cicada courtship . Most of it has also been reported in more detail by Alexander & Moore (1958) . In the ensuing sections detailed analyses of each stage and experiments designed to probe the biological significance of various aspects of courtship will __ be described. The general description is true for 1 2 sac both Magicicada septendecim and Magicicada Court I : Magicicada septendecim cassini, with occasional exceptions as indicated . Behaviour patterns found in 17-year cicadas can probably be assumed to occur also in the corresponding 13-year broods, although we have studied only those with 17-year life cycles . Cicada courtship, like most examples of animal behaviour, does not comprise a series of discrete stages ; rather it is continuous and has been divided into stages to facilitate analysis. During an emergence the male cicadas sing, their songs combining to a deafening din that can be heard over great distances . The song attracts conspecifics of both sexes, which fly toward the singing centre, the area where the sound is loudest. Once there, the females land on branch Court I : Magicicada cassini tips and generally remain still, though they may walk about . The males join the chorus of their Fig . 1 . Sonagrams of court I songs . Only a single phrase conspecifics . This usually means that they sing a of each song is shown .

DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS 1 075

During the next stage of courtship, the male pursuits, the touch is delivered to the tips of the approaches another cicada while singing, usually other 's folded forewings. The touch may be either court I or court II . Court II (Fig . 2) is accomplished with a straightforward pawing similar to court I in that each phrase is like those motion or he may vibrate the foreleg as he paws . of the calling song, but the interphrase interval is The male may or may not sing a courting song as much shorter and each phrase may be somewhat he paws at the courted cicada . shortened as well. The song thus has a faster If the courted insect remains motionless, the cadence than court I and is equivalent to the male may proceed to the next stage of courtship, first courting song of Alexander & Moore (1958) . or he may return to the wait/pursuit stage . If he After approaching the courted insect, the proceeds singing, the phrases of his song shorten courting male usually stops and remains motion- and the interphrase interval decreases until he is less about 1 cm away while continuing to sing . If singing a series of short, rapid phrases, each of the animal being courted moves away, the which resembles one of the segments of his courting male usually follows, maintaining a calling song in frequency structure. This quick distance of a few centimetres between them. This tempo song is court III (Fig. 3) and is equivalent period of watchful waiting and discreet pursuit to the second courting song of Alexander & may continue for periods ranging from a few Moore (1958). The male may repeat the pawing seconds to hours . It can be recognized as at the courted cicada while creeping closer and courtship only by the singing of one or more closer. If he is not rejected, he climbs upon the courting songs by the male . back of the female and begins probing with his Most courtships are terminated at the wait/ genitalia while turning around and around, pursuit stage, usually by some apparent action of sometimes singing. Shortly thereafter, if the the courted insect, after which the courting male female does not move, coupling is accomplished, leaves. If the courted animal does not move, whereupon any singing abruptly ceases . however, courtship may proceed to the next At any time during all of this the courted stage. During this period, the courting male animal can indicate its non-receptivity by moves closer to the courted cicada and touches moving. If it is definitely not receptive, e .g. if it is it with one of his forelegs . Since he is usually another male, it usually flies away . A milder behind the other animal as a consequence of the degree of rejection is apparently indicated by walking away. In this case the courting male may follow, but a cicada who continues walking usually loses a courting male in a thicket of 3- twigs and leaf petioles . If a courted cicada is not N receptive but unable or unwilling to leave, e .g. if y1 1 2 sec 3- CourtII : Magicicada septendecim • • x 1_ OWN""1 2 sec

Court III : Magicicada septendecim

10

• G • " 2

1 . 5 2 . 0 sec 0 . 5 1-0 sec CourtE : Magicicada cassini Court III : Magicicada cassini, Fig. 2 . Sonagrams of court II songs. Two phrases of the M. septendecim song are shown but only one for M. Fig . 3 . Sonagrams of court III songs . Several phrases of cassini. each song are shown .

1 076 ANIMAL BEHAVIOUR, 27, 4

it is an egg-laying female with her ovipositor by reciprocal song could be courtship . Alexander embedded in the twig, she usually flicks her & Moore (1958) have previously described the wings in response to the pawing contact. This sound and the behaviour, but they included it as commonly elicits a return to the wait/pursuit a part of courtship . Further studies are needed to stage, or the courting male may leave . If the two determine the biological function of this pattern. insects happen to be facing each other on a To summarize periodical cicada courtship, the branch tip, the usual response of a courted initial stage includes a courting song and occurs animal that does not simply depart is to when a male cicada drops out of the chorus. The paw at the courter. The response of the male to second, approach, phase involves the movement this signal is similar to that elicited by a wing of the courting male to within about a centi- flick : he either leaves or returns to the wait/ metre or two of the courted insect while singing pursuit stage . Even after mounting, if the courted a courting song . The wait/pursuit stage always animal moves, the male immediately drops off, includes song and usually follows this approach, ceases whatever song he was singing, and either but it may occur at any point in courtship. When leaves or resumes the wait/pursuit . probable receptivity on the part of the female has In Magicicada cassini there is another signal, been indicated by fairly prolonged immobility, given by a male in response to another male, that the touch phase is initiated . Continued immobi- seems to indicate non-receptivity and may be lity by the female elicits the next stage, the agonistic. This is a wing flick accompanied by a mount, which is usually followed by copulatory short phrase of the `tick' portion of the calling probing, after which coupling occurs . Any of the song (see Figs . 1 and 4B). The flick-tick signal is courtship songs may occur at any stage of often given by a male who is courting a cicada in courtship. Some courting song is necessary for front and simultaneously being courted by the recognition of the initial, approach, and another insect behind him . The response of the wait/pursuit stages, but the other stages may second male to this signal can be the same as to proceed in the the absence of song. an `ordinary' wing flick, a resumption of the wait/pursuit, or he sometimes returns the Methods and Materials flick-tick. In the latter case there are often long Adult cicadas were observed in singing centres sequences where the two males flick-tick at each located in stands of small trees in 1970 (), other for several minutes without moving . In the 1973 (Brood XIII), and 1974 (Brood XIV) . present study the flick-tick sequences were not Brood numbers follow Marlatt (1907) . The scored as courtships because they involve singing Brood X studies, in Ann Arbor, Michigan, by both partners . Females cannot sing, so it included only Magicicada septendecim . We seemed unlikely that an interaction characterized studied both M. septendecim and Magicicada cassini in Argonne, Illinois, in 1973 and in A Brown and Harrison Counties, Indiana, in 1974 . Observations were made throughout the day at most of the sites . Most studies of M. septendecim N3 were made in the morning and of M. cassini in i . the afternoon . Portable stereo cassette recorders 1 2 sec (Sony model TC 126) were used to record simultaneously insect sounds and verbal des- 'Stutter' : Magicicada septendecim criptions of behaviour . The microphones used for recording the cicada songs were fastened to B the ends of extensible poles that could frequently be brought to within a few centimetres of the courting males without disturbing them. Behav- 10- iour was sampled by simply watching for pairs of = 6- «I nlk.atal+d lt~n~~ hi,be,ll , I I •1 Id q << n • cicadas that seemed to be interacting, bringing up r 2- the microphone, and describing the interaction until it was terminated by one of the partners or 0. 5 1 .0 sec until it was evident that it did not meet our Tick' Magicicada cassini criteria as a `courtship' . A variety of objects were tested to determine Fig. 4. Sonagrams of other periodical cicada sounds . their effectiveness in eliciting courtship by

DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS 1077

unrestrained male cicadas in the emergence using these models were done with unrestrained areas. These included live and dead cicadas of female M. septendecim and M. cassini in emer- both sexes of both M. septendecim and M. gence areas of Brood XIV in southern Indiana cassini and black-painted wooden blocks of 1974. different sizes and shapes (Fig. 5). Some of the Contingency tests for x2 were run on the data blocks had cicada forewings glued to their sides . to detect differences in the male courtship All of these objects were fastened onto twigs in signals and in the responses of cicadas belonging the singing centre with insect pins . Most of these to the two species. In all cases, row-column experiments were done in the monospecific horde independence was the null hypothesis . in Ann Arbor, Michigan, with Dr R . D. Alexander in 1970, but a few additional observa- Results tions were made with the same objects in Intraspecific Courships Argonne, Illinois, in 1973 . A total of 241 spontaneous courtships of Model `male cicadas' were constructed to test periodical cicadas were observed in a multi- unrestrained females' ability to discriminate specific emergence near Argonne, Illinois, in courters on the basis of tactile and acoustic cues . 1973. A courtship was defined as an interaction Each of the models was constructed of a spring- that included any one or more of the courtship loaded `grabber' approximately 46 cm long, songs and/or one or more of the male courtship with an earphone and an assemblage of soft wires behaviour patterns that could be recognized as a (to simulate legs) fastened to the tip (Fig. 6). The part of courtship without song . The latter tip with all its appurtenances was then painted included the foreleg touch, mounting, copulatory black. The earphone led from a single pole- probing, and copulation. Magicicada septendecim double throw switch that was, in turn, connected courted in 171 of these interactions and M. to the outputs of one of the stereo cassette cassini in the other 70. recorders . The courtship songs of M. septendecim In 142 of the 171 M. septendecim courtships were recorded on one channel of a cassette and (83 %), the courted cicada was also an M. septendecim . These are defined as intraspecific those of M. cassini on the other. The songs emitted by the earphone on the model could thus courtships. Seventy-six percent of the 70 M. be changed by flipping the switch . Verbal cassini courtships were intraspecific . Homo- descriptions of the responses of females to sexual courtships comprised at least 26 (18 %) of `courtship' by these models were recorded on a the intraspecific M. septendecim courts and at small monaural cassette recorder . Experiments least 4 (7-5%) of the M. cassini ones. It was sometimes difficult to determine the sex of a silent cicada at a distance so few assumptions can be made concerning the sex of courted cicadas.

Fig. 5. Wooden blocks used to elicit courtship from Fig. 6. Model used to imitate male courtship signals . The unrestrained males . Each block was made of balsa wood, distance from the point marked X to the tips of the painted black . `grabber' prongs was 6 .5 cm.

1078 ANIMAL BEHAVIOUR, 27, 4

Each courtship has been divided into signal- receptivity can thus be determined by the propor- exchange bouts, each comprising some courtship tion of immobility responses it evoked. In pattern performed by the male and the response M. septendecim, 106 of the 158 (67 %) male of the courted cicada . In the intraspecific courtship signals that included song elicited courtships of M. septendecim there were a total immobility from the females, while in 40 of the of 271 bouts, for an average of 1 .9 bouts per 113 (35%) silent bouts the female became or courtship . There were 145 bouts in the 53 remained motionless . Similarly M. cassini intraspecific M. cassini courtships, yielding an females were motionless in 67 of 121 (55%) average 2 . 7 bouts per courtship . Most courtships bouts with song but in only 6 of 24 silent bouts did not continue to copulation but were ter- (25 %). It is evident that bouts with song were minated by the departure of one of the partners . more effective in eliciting immobility than silent In the M. septendecim courtships, 158 of the ones in both species . 271 bouts (58 %) included some courtship song ; When the individual courtship bouts of each while in M. cassini 121 of the 145 bouts (83 %) species were compared, there were definite included song. It is clear that male M. cassini differences. Courtship of M. septendecim differed were much more likely to sing during their from that of M. cassini not only in the acoustic courtships than were M. septendecim males characteristics of the courting songs but also in (Fig. 7). The remainder of the bouts in each the proportions of typical courtship behaviour species included courtship patterns performed by patterns performed by the males and in the silent males . Although a courted cicada may do responses of females to these signals . Silent several things in response to male courtship, M. septendecim touched conspecific females with including wing flicking, pawing, and leaving, their forelegs more often than did quiet M. either by walking or flying away, the only cassini, both with foreleg vibration and without . response that apparently indicated receptivity They were also more likely to mount a conspecific was immobility. The relative `effectiveness' of a than were the M. cassini males. The M. cassini, on courtship signal in eliciting or detecting female the other hand, performed more bouts of waiting

∎M.septendecim Courtship Bouts, N=268

. cassini Courtship Bouts, N=165 ®M

10111 1 I Touch Touch Mount Ctpum-' PIh Touch Pwsuit Wait 'Mount ' rrgoula- without 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 : Male probed 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 1079 and pursuit than did the M. septendecim. These court III, . and they were about equally likely to data are shown in Fig . 7. The differences in court- sing courts II and III . In M. septendecim the ship patterns between the species are significant at court I song occasionally differed slightly from the P = 0 .01 level, as revealed by a 2 x 10 contin- the normal court I in that there was sometimes a gency test for X2. slight stutter audible between the phrases (Fig . The responses of courted cicadas of the two 4A). Infrequently a series of stutters was emitted species to intraspecific courtship signals were without any of the rest of the usual phrases . also significantly different at the I % level . As Stutters alone and court I songs with stutters expected, there were more responses of M. seemed to elicit the same responses from the septendecim to courtship without song. The courted as court I without stutters . M. cassini walked away from their courters more Likewise, there were no differences between the often than did courted M. septendecim. In both species in the proportion of immobilization species the most common response to courtship responses to the various courting songs . Both was immobility. These results are shown in Fig . 8. M. septendecim and M. cassini females were In the courtship signals with song, there were equally likely to indicate acceptance in response no significant species differences in the tendency to the conspecific court I, court II, or court III of the males to sing any one of their typical songs. When the immobility responses were courtship songs. There were 113 bouts including compared to the combined rejection signals in court I in M. septendecim, and 101 in which response to different courting songs within each M. cassini sang their characteristic court I song . species, no differences were found for M. cassini M. septendecim sang court II in 35 bouts, and females. A difference, significant at the P = 0.05 M. cassini in 26. Forty-seven of the M. septende- level, was found for M. septendecim, in which cim bouts included court III, as did 32 of the courted cicadas were somewhat more likely to M. cassini bouts. These data include courtships reject conspecific males singing court III than of all objects during our studies of Brood XIII . courts I or II. Males of M. septendecim were as likely as those A total of 25 courtships of live, unrestrained ofM. cassini to sing their particular court I song ; cicadas were observed in the monospecific and the same was true for the court II and court emergence of M. septendecim in 1970 near III songs. Males of both species, however, sang Ann Arbor, Michigan . Most of these courtships their court I songs more than either court II or had to be detected entirely by their characteristic behaviour patterns, as we could not reliably record the courtship songs . Sixteen of these courtships were heterosexual, and the other nine involved the courtship of one male by another . The incidence of homosexual courtship in M. septendecim was thus apparently twice as high (36 %) in this monospecific emergence as in the multispecific one (18 %) . These 25 courtships of unrestrained conspecifics comprised only 28 of all the courtships observed in 1970. The objects of the rest of the 1970 courtships were restrained or dead cicadas and inanimate objects . These are described in the next section . When the behaviour patterns exhibited by the WA WF Pa male M. septendecim courting conspecifics in the I-- Bouts without song--I 4-Bouts with song-4 Michigan emergence of Brood X were compared with those used in intraspecific courtships of Fig. 8. Female behaviour patterns during intraspecific M. septendecim and M. cassini in the Illinois courtship. (Copulations have been omitted, so the total number of bouts in M. septendecim is 268, not 271). Brood XIII, it was evident that the incidence of FA : Fly Away . Courted insect flew away from courter . pursuits and waits was anomalously high in WA: Walk Away . Courted insect walked along branch, M. cassini and low in the M. septendecim in the away from courter. WF : Wing Flick. Courted insect monospecific horde (Fig . 9). This difference is flicked a forewing at courting male behind . Pa : Paw . Courted insect pawed with foreleg at courting male in probably at least partly artifactual, as we were front. I: Immobility. Courted insect became or remained frequently unable to record courtship songs motionless near courting male. during the Michigan emergence, and songs are

1 080 ANIMAL BEHAVIOUR, 27, 4

necessary to recognize pursuits and waits in recognizable courtship signals on the part of the courtship. The greater tendency of male M. male, but in which the object of his attention was cassini than M. septendecim to sing during not only not a female conspecific, it was some- courtship in the Illinois emergence has already times not even a cicada. These included court- been noted (Fig. 7). A more important differ- ships of unrestrained members of other cicada ence may lie in the high incidence of copulatory species, of cicadas pinned to twigs, of dead probing and of copulations among the Michigan cicadas, of black wooden blocks (Fig . 5), and of animals as compared with males of either species the black tips of microphones . The inanimate in the Illinois data . The courtships in Michigan objects that were courted are hereafter referred were more often successful than those observed to as models. The only obvious properties that in Illinois in that they proceeded to copulation all of these objects shared were that they were more frequently. This is evident in that the act of all between 2 and 6 cm long, black, slow-moving coupling was seen only 3 times in M. septendecim or still, and located among the twigs in the in 271 bouts and never in 145 bouts of M. cassini periphery of the trees in the singing centre . courtship in Illinois, while 6 copulations were Most of the courtships of models and of dead seen to occur in only 41 bouts in the Michigan insects were observed in the monospecific horde emergence of M. septendecim. These observa- of M. septendecim in Ann Arbor, Michigan, in tions of the act of copulation do not include the 1970. There were no significant differences in the pairs already in copula found in vast numbers in amount of courtship attention directed toward any emergence. Statistical comparisons of male models of various sizes and shapes, nor did the intraspecific courtship patterns among the three presence or absence of cicada wings on the groups observed (Michigan septendecim, models seem to make a difference . The large Illinois septendecim, and Illinois cassini) revealed proportion of courtships directed to models in that the differences were significant at the these experiments is probably partly artifactual, P = 0.01 level. due to our methods of studying the cicadas at that time : we focussed most of our attention on Courtships of Inappropriate Objects the wooden models and cicadas pinned to the In addition to the courtships of conspecifics, twigs and waited for male cicadas to court them . there were many interactions that included Relatively few of the many courtships among the

M.septendecim ®it cassini Bouts _M, jgptendeci m i Bouts, Brood XIII Brood XIII : N-145 Bouts, Brood X N= 271 N : 41

Touch Touch Pursuit without with Vibration Vibration Fig . 9. Male intraspecific courtship patterns in monospecific and multi- specific emergence area . Behaviour patterns are as described in text and Fig. 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) . DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS 1081 unrestrained cicadas present were observed (only many more episodes of pursuit and waiting while 25, as noted previously) . Nevertheless, when we courting conspecifics than models, and far more performed similar experiments with pinned of the courtships of models proceeded to models and cicadas in the multispecific horde of copulatory probing than did those of con- 1973, the pinned objects received very little specifics . The males also touched the models courtship attention . Wooden models were with their forelegs less than they did in intra- courted only three times in the 1973 emergence . specific courtships . The differences between the In both the 1970 and 1973 emergences there courtships of models and of conspecifics are were many more live cicadas than models significant at the P = 0 .01 level, and are shown available as courtship objects in an emergence in Fig. 11. The average number of bouts in the area. In each of the 1973 courtships observed a courtships of models was 2 . 1, only slightly more black microphone was always within a few than the mean number of bouts in intraspecific centimetres of the courting animal, though it M. septendecim courtships. was not always within easy reach of an animal In addition to courtships of inanimate and walking on a twig. Under these circumstances dead objects, male cicadas of each species many more M. septendecim than M. cassini occasionally courted unrestrained members of turned their courtship attention from the cicada the other species in a multispecific emergence they had been courting to the microphone tip . area. These are defined as interspecific courtships The proportions of courtships directed toward and were much more frequently performed by different objects are shown in Fig . 10. M. cassini than by M. septendecim . Male When the courtships of models and of con- M. septendecim courted M. cassini only 7 times specifics were compared for all M. septendecim in the 171 M. septendecim courtships observed. courtships, pooling the Michigan and Illinois There were a total of 15 bouts in these 7 court- data, several differences appeared . There were ships, for an average of 2 . 1 bouts/courting session. This is similar to the mean number of Intraspecific®Interspecific-Mode ls and bouts in the courtships of other objects by Dead Cicadas M. septendecim . Male M. cassini, on the other hand, courted M. septendecim in 15 out of the 70 M. cassini courtships observed . This difference N =70 N=171 N=89 100 in the proportions of intraspecific and inter- specific courtships in the two species is significant .01 level. There were 36 bouts in the V nlrnueg at the P = 0 15 interspecific M. cassini courtships, yielding an ° 75 C N 50 C-1 Intraspecific courtship bouts, N =303 Bouts courting models and dead 40 Cicadas, N=120 N 7 O _ 30 7 a O O U 25 C O N 20 U a) U d a d) 0 10

M.cassini Mseptendecim Mseptendeclm

BROOD XIII BROOD X Pu ,

Fig. 10. Male courtships directed at different objects . Fig. 11 . Male M. septendecim courtship behaviour Intraspecific : Object was a live, conspecific cicada of patterns directed at different objects in both Brood X either sex . In Brood X many of these live cicadas were and Brood XIH . Objects have been described in text and restrained . Interspecific : Object was a live cicada of in the legend of Fig . 10. ToV: Touch without vibration . another species . None of them were restrained . Models T + V : Touch with vibration. Pu : Pursuit, with court- and Dead Cicadas : Object was a model (defined in text) ship song. W: Wait, with courtship song. M: Mount. or a dead cicada pinned to a twig . CP : Copulatory Probing. Copulations are excluded.

1082 ANIMAL BEHAVIOUR, 27, 4

average bouts/courtship of 2 .4. This is somewhat courtship by the males of both species . The long less than the 2 .8 bouts/courtship average for wire was used to touch the female, in a manner intraspecific courtships in M. cassini. The times that approximated the pawing action of the of day when interspecific courtships were foreleg contact, although we could not vibrate observed were usually those appropriate to the this `foreleg' as the cicadas sometimes did . By courting male. Courtships of M. cassini by M. septendecim were seen mostly in the morning ; MALE COURTSHIP PATTERNS those of M. septendecim by M. cassini mainly in Olntraspecific •Interspecific the afternoon . 50 When the interspecific courtships were N examined in detail, it was evident that there .c0 were few differences between the species in their interspecific courtships . There were no significant 0 differences between the two species in male 0 25 00 behaviour during interspecific courtship . There C was not even a species difference in the propor- tion of signals that included songs as compared aU00 to those that did not, unlike the intraspecific a _1i ,1- P . courtships in which M. cassini sang much more ToV PuW MCIDP ToV PuW MCP often than did M. septendecim. There were also T+V T+V no significant differences in the responses of ~-M. septendecim -+ ' M. cassini--~ courted cicadas of the two species to intraspecific C3N=268 ON=145 courtship. N= 15 • N=36 When intraspecific courtships were compared to interspecific ones within each of the two species, significant differences emerged only for M. cassini (Fig. 12). Male M. septendecim courted the same way, and individuals of this species responded in the same way, regardless of FEMALE COURTSHIP PATTERNS whether or not the courtship partner was a Olntraspecific .Interspecific conspecific. In M. cassini, on the other hand, the males proceeded much further in their courtships W 50 of members of other species than they usually did 0 in intraspecific courtships . There were propor- .0 tionately more interspecific bouts including 0 mounting and copulatory probing than intra- 025 specific ones. Courted M. cassini pawed at 4- courting M. septendecim more than they did at C their conspecifics . The M. cassini differences in a, LU the patterns of both male and female behaviour a, in interspecific and intraspecific courtship were a significant at the I % level . FA WA WF Pa I FA WA WF Pa I 4M. septendecim .- M. cossinl , Responses of Females to Courtships by Models o N=268 C:3 N=145 Although there were definite differences both in the songs and in the proportions of various = N=36 = N=15 courtship patterns performed by males of the Fig. 12. Comparison of intraspecific and interspecific two species, it seemed that only the females of courtship patterns for cicadas of both species and sexes, M. cassini responded to these differences . Brood XIII only. Male courtship behaviour patterns described in text and in the legend to Fig. 11 . Female Accordingly we attempted to court females of courtship behaviour patterns described in text and in the both species with a totally inappropriate object, legend to Fig. 8. Intraspecific courtships : the partner was the model shown in Fig . 6. Although the model a conspecific . Interspecific courtships : the partner was a did not visually resemble a cicada, except in member of the other species . In 15 of these bouts the male being black, it could generate signals similar to was an M. septendecim and the female an M. cassini. Male M. cassini courted female M. septendecim in 36 most of the tactile and auditory cues common to bouts.

DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS 1083

attaching the model to a twig near a female with either species when the tape recorder was turned the grabber prongs the model could perform the off so that there were no sounds at all emitted long waits with song common to both species . from the earphone. Moving it slowly behind a walking female A comparison of the immobility responses of mimicked the pursuits . If a female remained females of the two species to courtship by the motionless when touched several times with the model showed that there were no differences long wire, the model was lifted onto her back so that could not be accounted for by the different that the short wires touched her, and it was proportions of courtships with no songs, gently bounced about to imitate the motions of a conspecific songs, and allospecific songs . Because mounted male, though nothing very similar to of the ambiguity of the immobility `response' the copulatory probing of a real male could be (a female may or may not have `responded' to a attempted. model when she did nothing), courtship bouts A series of courtship songs of each species was involving a moving female and model were recorded on a cassette, proceeding from court I examined. There were a total of 239 bouts of this through court II to court III . The songs of one sort involving M. cassini females, and 141 bouts species were recorded on one channel of the tape, with M. septendecim females. A female was and those of the other species on the other judged receptive to courtship by the model if she channel. The series of songs was then repeated on stopped moving as it pursued her, with or each channel until the tape was full . Because without touching her with the long wire . She was there were no significant differences in the considered unreceptive if she continued walking proportion of acceptances in response to dif- or flew away when pursued, with or without ferent courting songs in either of the species in touch, by the model. The results of this analysis, the courtships performed by conspecific males, shown in Fig. 13, indicate that the responses of as already noted, it was considered that all songs of a species were equivalent in eliciting hi ca ssin i Acceptances ® M.seatendecim Acceptances immobilization. So, although we could not predict what song would be emitted by the M.cassini Rejections M.septendecim Rejections earphone at the onset of any courtship, and 100- though any song could be played during each of the mimicked courtship behaviour patterns, these intraspecific song variables were considered relatively unimportant in determining the re- sponses of the females thus courted. There were 50 courtships of unrestrained female M. septendecim using the models and 48 of female M. cassini . There were 344 bouts in the 50 M. septendecim courtships, for an average of 6.9 bouts/courting session . There were 620 bouts when courting female M. cassini, for a mean of 12 .9 bouts/courtship. It is clear that we were much more persistent in our courtships of females with the models than were the male cicadas. The experiments on M. septendecim were done during periods of maximum septendecim chorusing in the morning, and those on M. cassini in the midst of loud, synchronized cassini choruses in the afternoon . In each of the courtships by models there were 0- N-15 N=7 N :176 N ;11 N :46 N .123 far more bouts in which the song played from the NO SONG M .cassini SONG M .-decim SONG earphone was intraspecific rather than inter- specific. Female M. septendecim were courted Fig . 13 . Responses of intact females to courtship by with septendecim song in 298 of 335 bouts with model. Model described in Fig. 6 and in text. Songs were emitted from earphone on model . Responses of females song, and M. cassini females were courted with were scored as `Acceptances' if she ceased moving and as cassini songs in 409 of 571 bouts with song . `Rejections' if she continued to move while the model There were relatively few bouts in courting pursued her, with or without touching her .

1084 ANIMAL BEHAVIOUR, 27, 4

female M. septendecim were not significantly visually mediated, although the visual stimulus different from those expected on the basis of the necessary to elicit this approach seems to be different proportions of the three types of extremely generalized. There are apparently none courtships (x2 = 4.97 ; df = 2; 0.05 < P < 0 . 10). of the specific visual sign stimuli common in On the other hand, the M. cassini females' butterflies, for example (Crane 1955 ; Emmel responses were significantly different from the 1972) ; rather a male cicada approaches any dark expected proportions at the P = 0.05 level (X2 = blob in the singing centre, even though it may be 6.26; df = 2). very different from a female in both size and shape. The generality of the stimulus is similar to Discussion that eliciting courtship in several bugs, some There are many similarities in the courtship dipterans, and the cockroach Gromphadorhina behaviour of the two species of periodical cicadas (Markl 1974) . In the latter cases, though, any studied. Both species sing courtship songs, each moving object of about the right size is ap- of which is radically different from the songs of proached, while in cicadas the object must be the other species but bears a similar relationship dark and still . The generality of the visual to other songs within each species . These songs stimulus adequate to elicit courtship approach is comprise a continuum of gradually increasing probably partly a consequence of the high tempo, and our division of this gradation into population densities in a periodical cicada sing- three stages is necessarily arbitrary . These songs ing centre, where most of the small, dark blobs have been previously described and sound are cicadas . spectra published by Alexander & Moore If the adequate stimulus for courtship is such a (1958, 1962) . The first courting song is identical vague, visual one, it is difficult to understand why to the calling song but there are more phrases, most of the courtships in both species were and the flight that terminates a sequence of conspecific. There were many cicadas of both calling does not occur following court I in either species in the multispecific emergence sites and, species. The other two courtship songs in both in spite of the allochrony in the level of activity species exhibit phrases of the calling songs that of the two species (Alexander & Moore 1958, are progressively shortened, as are the interphrase 1962), there were large numbers of insects of both intervals, resulting in a sequence of songs with species active throughout the day . On windless, gradually quickening cadence . The phrase hot, sunny days members of even the relatively similarities in the various songs of each species inactive species were usually perched on the are typical of the acoustic courtship sequences branch tips rather than in along the major found in other insects, such as the crickets branches and trunks of the trees . They were studied by Alexander (1960) and the grasshoppers therefore in an optimum position to act as studied by Perdeck (1957). courtship targets for males of the more active Another similarity in the acoustic courtships species, yet they received relatively little court- of these two cicada species is in the evident ship attention . Because most of the courtships absence of differential female response to the observed were already beyond the initial various courting songs. They react the same way approach stage when we detected them, it seems to all of them within each species . The differences likely that the very general cues are adequate between the songs may not, therefore, indicate a only for this very early phase of courtship, and different signal function for the increasing tempo, that its continuation depends on other informa- but might reflect the increasing excitement level tion. of the'individual singing . The continuation of courtship in both species The behaviour patterns exhibited by both apparently depends upon the behaviour, or the males and females of the two species are also lack thereof, of the courted insect. If the courted similar. As Alexander & Moore (1958, 1962) object remains still, courtship usually continues, have noted, the initial acts that bring periodical but it may be broken off if the courted animal cicadas of the two sexes together are first moves. Usually the movements that serve to acoustically and second visually mediated . The disrupt courtship, the rejection signals, are large, aggregation of conspecific cicadas in a singing fairly obvious motions. This is especially true if centre is a consequence of the chorusing behav- the rejection occurs when the courter is some iour of the males singing their calling songs . The centimetres away. At this distance the rejection approach of an individual male cicada to a is signalled by the departure of the courted insect, female within the singing centre is apparently either by walking or flying away . When the DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS 1085 partners are very close together, as following a There are so many cicadas in a singing centre foreleg contact, rejection may seem more subtle that any individual not moving probably and involve the movement of only a part of the becomes a courtship target very quickly . To courted insect, e .g. a wing or a leg. These close- prevent courtship an insect would have to move range rejection signals are similar to those used almost constantly, as do the chorusing males . As by male and unreceptive female Drosophila when movement is metabolically expensive, a conserva- courted (Bastock 1967) . Differences in the degree tion of effort on the part of courted cicadas of of rejection communicated by the various signals both sexes is probably adaptive . It appears that, are evident in the varying responses of the although immobility was the most frequent courting males to them. Courtship is inevitably `response' to male courtship, it probably did not terminated by flight of a partner, even if the usually indicate sexual readiness but simply an insect doesn't fly very far, while it may continue unwillingness to move unless some definite in the pursuit or waiting stage following depar- rejection signal was necessary to prevent copu- ture by walking or after one of the wing or leg lation. It is apparently as difficult for a male signals. In these cases, persistent repetition of the cicada to interpret absence of movement in rejection signals is sometimes necessary to another cicada as it is for us, and a male con- terminate the courtship . The unreceptive insect fronted with a non-moving, cicada-like object must keep walking or repeat the wing flick or leg treated it as a possibly receptive female con- motion several times before the courting male specific and courted it . This may explain why so leaves. It seems that a mild degree of rejection is few courtships were successful in either species . usually sufficient to prevent copulation, although It would also explain why the models continued courtship may continue. Therefore an unrecep- to be so attractive as courtship objects, as they tive cicada will reject contact with a courting seldom moved. male but suffer him to continue singing his There appears to be no particular disadvantage courting songs close by . This is evident in the to the females in long, fruitless courtships, as comparative responses of courted insects of both there are plenty of males available when the species to contacts as opposed to waits in females are ready for mating, and copulation can intraspecific courtships . M. septendecim rejected easily be prevented upon contact when they are 71 of 111 foreleg contacts and 15 of 23 mounts, not. The disadvantage would seem to be with the but remained motionless during 83 of 101 bouts males, who are thus persuaded to spend large of courtship waiting . Similarly, M. cassini amounts of time and effort singing courting songs rejected 26 of 37 foreleg touches and 2 out of and chasing silent cicadas with very little hope of 3 mounts, but sat still during 60 of 71 bouts of mating with the individual courted. Since so few waiting. courtships proceeded to copulation, it is difficult Female sexual receptivity in periodical cicadas, to understand the selective advantage of such as in many other insects, is indicated by immo- persistent courtship, in spite of even mild bility. This also occurs in at least one hymenop- rejection signals, by males of either species . The teran (Markl 1974), several orthopterans (Huber probability of mating in any given courtship is so 1960; Miller 1965 ; Alexander & Otte 1967 ; low, and the rate of copulation in the population Roth & Barth 1967 ; Spooner 1968) and in some as a whole is so high, as shown by the large nymphalid butterflies (Myers & Brower 1969 ; number of pairs in copula and by the evident Emmel 1972). The response evidently facilitates reproductive success of these cicadas, that it the efforts of the male to insert and attach his would seem advantageous for a male to terminate phalomeres and/or the spermatophore to the a courtship at the first hint of rejection and seek genital apparatus of the female. In spite of the another partner . Nevertheless . however wasteful evident importance of female immobility in the process may seem to us, it is evidently mating behaviour, however, it is dangerous to sufficiently effective to permit enormous assume that stillness indicates sexual receptivity . numbers of these cicadas to mate and pro- It can probably reflect other states as well . The duce viable offspring. absence of movement, in many cases, seems The initial contact between the courtship equivalent to an absence of behaviour, and partners occurs the same way in both M . should be interpreted with caution. A motionless septendecim and M. cassini. The males of both cicada may be resting, feeding, frightened, sick, species sing while close to but not touching the wounded, dead, sexually receptive, or doing female, and their first, tentative contact with the nothing because it is unnecessary to do anything . female is usually made with the foreleg. This

108 6 ANIMAL BEHAVIOUR, 27, 4

behaviour is different from the initial contact in were evidently more aware that it was something many other insects whose courtship behaviour different and were frequently frightened by it . has been extensively studied, such as crickets Those M. cassini who were not frightened (Alexander & Otte 1967), katydids (Spooner away by the microphone were more persistent in 1968), cockroaches (Roth & Barth 1967), and their courtships than were the M. septendecim, butterflies (Myers & Brower 1969). In the so that the average number of bouts in the M. orthoptera and lepidoptera studied, the first cassini courtships exceeded those of the M. contact between the partners is usually made by septendecim courtships. This greater persistence the antennae of at least one of the insects . In is also evident in the proportions of pursuits and most of the orthopterans, the antennal stimula- waits performed by males of the two species . tion is probably primarily mechanical, while it Figure 7 shows that male M. cassini were more has been shown to be chemical in queen butter- likely to chase a cicada that walked away during flies (Myers & Brower 1969) . The antennae of a courtship and to remain close by a motionless cicadas are very short, so that the insects' bodies cicada, singing, than were the M. septendecim would have to be practically touching before the males. On the other hand, the M. cassini males antennae could contact the other insect . The were less likely to touch a courted insect than manner of both early antennal touching during were the M. septendecim. These data suggest courtship in other insects and of foreleg pawing that an M. cassini courtship is a longer affair in periodical cicadas suggests that body contact than that of M. septendecim . A male M. septen- at this stage of courtship is somehow inappropri- decim approaches and proceeds to a foreleg- ate. Whether the touch is made by the antennae touch stage fairly quickly and is more likely to or the foreleg, it is brief, and either the appendage terminate courtship after receiving even a mild or the body of the partner is withdrawn before rejection signal . A male M. cassini responds to a the next stroke . There appears to be no behav- walk-away rejection by following and to a wing iour pattern in periodical cicadas similar to the or leg flick by continuing his song nearby . antennal lashing evident during later courtship The greater ease with which an M. septendecim in some orthopterans (Alexander & Otte 1967 ; courtship can be terminated compared to that of Roth & Barth 1967), although there were M. cassini also results in differences in inter- occasional foreleg `boxing matches' between specific courtships . The males court the same way cicadas facing one another on a twig . These whether they are courting conspecifics or occurred infrequently, when a courted cicada members of the other species, but the M. cassini responded to a male's foreleg contact by pawing usually proceeded further when courting back at him, and the male, in turn, pawed again . M. septendecim than M. cassini. This may be In addition to the similarities in the courtship because M. septendecim females typically reject behaviour of cicadas belonging to these two courtship with relatively subtle gestures, while species, there were also marked differences . One M. cassini females are more obvious and usually difference is reflected in the different numbers of leave (Fig. 8). M. septendecim males terminate courtships observed among animals of the two courtship in reaction to the subtle rejections of species. Many more M. septendecim courtships their conspecifics, but male M. cassini do not. were observed than those of M. cassini. Indivi- They proceed with an interspecific courtship even dual M. cassini were much more likely to be though they have been rejected. Since male disturbed by the microphone used to detect and M. cassini more often responded to a mild record any songs sung during courtship than rejection signal by continued courtship than did were the M. septendecim. When the microphone M. septendecim, the courtships of M. septendecim was brought close to a pair that may have been females by M. cassini males continued much courting, one or both of the cicadas were more longer than the courtships of M. cassini females likely to fly or fall away if they were M. cassini by M. septendecim males. Even though the male than if they were M. septendecim. Greater M. cassini were less likely to touch a courted disturbance of M. cassini courtships by the cicada during courtship than were the M. microphone is also reflected in the different septendecim, if they did get to the contact stage proportions of courtships directed at this black, it was more likely to occur with an M. septende- gently weaving object by cicadas of the two cim than with a conspecific cicada (Fig . 12). This species (Fig. 10). M. septendecim males often probably occurred because courted M. cassini apparently mistook the microphone for a female generally terminated a courtship earlier by conspecific and courted it, while male M. cassini leaving. Oddly enough, another difference

DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS 1087

between intraspecific and interspecific courtships order to terminate courtships, but she may in male M. cassini patterns was in contacts receive courtship attention from fewer males than between the partners while the male was singing do female M. septendecim. The problems may as opposed to silent bouts . These were more arise when many easily deterred male M. frequent in interspecific than in intraspecific septendecim wear out female M. cassini who courtships. This is startling, but it should be over-react to their courtships ; while female remembered that there were relatively few bouts M. septendecim under-react to courting male involving either contact or silence in M. cassini M. cassini and thus encourage them to waste (Fig. 7), so this difference may be more apparent effort in courting. When the two species are both than real. temporally and spatially sympatric one would The M. cassini males were much more likely to predict that their courtship communication sing during courtship than were the M. septende- strategies would converge, so that they 'under- cim, although bouts with song were more stand' each others' rejection signals more fully effective than silent ones in eliciting immobility and react accordingly . At the same time, there in both species . One reason for this difference could be selection for increased spatial and may lie in the relative proportions of behaviour temporal separation of the two species, so that patterns that require song to be identified as a interspecific communication would become less part of courtship in the two species. There were important. more bouts of identifiable courtship patterns In either case stronger selection would be that did not require song, i.e. bouts including predicted for interspecific mate discrimination contact between the partners, in M. septendecim in both sexes in multispecific hordes than in than in M. cassini. Therefore only those inter- areas where all the cicadas are members of a actions that included song were likely to be single species . The great propensity of male recognizable as courtship in M. cassini. M. septendecim to court such inappropriate The adaptive significance of the two different objects as microphones indicates that these courtship techniques, the slow, persistent one of insects may be less discriminating than male M. cassini and the fast, easily rejected method of M. cassini with respect to the objects of their M. septendecim. is evident when the typical courtship . When the courtship proclivities of responses of females of the two species are M. septendecim in the monospecific emergence considered . The slow courtship is difficult to term- of 1970 were compared with those in the multi- inate unless the female leaves precipitously, but specific Illinois emergence of 1973 (Fig . 10), it is that is precisely what the unreceptive female M. evident that the cicadas in the multispecific horde cassini is likely to do. If she does not fly away, the were much less likely to court models than were courtship will probably continue, but contact is those in the monospecific emergence . This relatively unlikely so the consequences of suggests that they were able to discriminate tolerating the singing male are not serious. On the among courtship objects in situations where it other hand, a female M. septendecim who does might be important, i .e. where a `mistaken' not promptly indicate her non-receptivity is courtship object may well be a member of likely to have a male crawling over her fairly another species, but they were less discriminating soon. She can, however, signal a rejection with- when there were fewer chances for errors . The out a great deal of effort, and that will probably basis for such mate selection by males remains terminate the courtship . unknown. Not surprisingly, the courtship behaviour The enormous differences in the proportions patterns typical of the two sexes in each of the of such advanced courtship behaviour patterns species are mutually adapted, but problems as copulatory probing and copulation in the seem to arise when interspecific courtships occur . 1970 emergence compared with the observations The more easily rejected M. septendecim males do in 1973 suggests that the probability of success in not long continue an interspecific courtship, but courtship (copulation) was much higher in the they are more easily diverted by other black, monospecific than in the multispecific emer- stationary objects (such as microphones) in the gences. This may mean that the early courtship courting area. This suggests that the M. septende- tactics of these cicadas were similar under the cim males initiate more courtships than do the two circumstances but that the results of the M. cassini. A non-receptive M. cassini female courtships were very different, so that behaviour may have to spend a lot of effort flying away from patterns with a high probability of success in a the unwelcome attentions of conspecifics in monospecific horde were much less likely to

1088 ANIMAL BEHAVIOUR, 27, 4

result in copulation in multispecific emergence that even when both species are found in the areas. This is probably an unstable situation, same trees, the males of the two species are indicating that multispecific emergence areas are singing and the females are on the peripheral rare and/or a relatively new development in the twigs primarily at different times of day . There evolution of these insects . The work of Dybas & can be much overlap, both in space and time, Lloyd (1974) shows that these two species are between the species in a multispecific emergence commonly found in slightly different habitats . site, so these separation mechanisms are far from The studies reported in the present paper of perfect. areas where they overlap indicate that the If, as seems to be the case, unsuccessful animals manage to maintain reproductive isola- courtships are commonly terminated following a tion even in the same habitat . As Dybas & Lloyd rejection signal by the courted insect, what are have noted, multispecific emergence sites are the criteria used by the females to discriminate most common in disturbed areas where there are among the males that court them? If the females many small trees of several species . It seems did not discriminate at all but merely accepted probable that such sites will not decrease in courting males at random in a multispecific abundance as long as man and agriculture emergence area, one would expect the same persist. Because their life cycles are so long, proportion of interspecific copulations as there periodical cicadas probably evolve very slowly, were interspecific courtships ; that is, 4 and the relative abundances of disturbed and interspecific pairs including male M. septendecim mature woodlands in the distant future are and 21 % pairs in which the female was M. difficult to predict . However, insofar as multi- septendecim and the male M. cassini. Actually specific hordes continue to exist, there should be interspecific copulating pairs are extremely rare . further selection for. divergence of male courtship Dybas & Lloyd (1962) found only 7 in 771 pairs, signals (already evident in the different songs) and we have found but one . The female of this and for convergence of both the female rejection pair was a dead M. cassini. We do not know if signals and of the male responses to them. she was dead when coupling occurred . In spite of the cicadas' difficulties in inter- Although the absence of movement may not specific communication, it is evident that females indicate sexual receptivity, since most females in are able to reject effectively males of other a singing centre are motionless, cessation of species and that intraspecific courtship is movement may, indeed, signal acceptance of sufficiently effective for reproductive success. courtship . The responses of moving females to Although most courtships were unsuccessful, it courtship by the models (Fig. 13) indicated that is probable that many, if not most, surviving they were not very discriminating under these females do copulate and lay viable eggs . It is also rather peculiar circumstances . All the females evident that the copulations were almost tended to keep moving when courted by the invariably intraspecific. model and were therefore judged non-receptive . Most of the courtships observed in both Only the M. cassini females were shown to species were intraspecific . If males in the singing discriminate : they were more likely to stop in centres courted silent cicadas sitting on peripheral apparent response to the songs of their own twigs completely at random they would probably species than when the song from the earphone court more members of their own species than of was that of M. septendecim or when there was no others. There are two reasons for this, both of song from the model . Magicicada septendecim which have been noted by Alexander & Moore females did not discriminate as much . Simmons (1962) and by Dybas & Lloyd (1974) . Because et al. (1971) have shown that the frequency conspecifics are attracted by the calling songs spectra of the calling songs of the two species are of the males and the songs of the two species are quite different and that their auditory sensitivities different, there is often, even within a multi- match their respective acoustic output . Since the specific emergence, some geographical separa- non-acoustic courtship patterns are similar for tion of singing centres of the two species. This the two species, it is scarcely surprising that this separation may be very slight, so that there are acoustic information was apparently used by the more M. septendecim on one tree and more female M. cassini in discriminating among M. cassini on an adjacent one that may be only a courters. few feet away. There is also a daily allochrony in Although females could rely on acoustic the time of maximum chorusing and therefore of differences between the species-specific songs of maximum courting activity in the two species, so courting male cicadas to differentiate among DUNNING ET AL. : COURTSHIP IN PERIODICAL CICADAS 1089 them, it is evident that they do not always do so . M. septendecim appear to be less discriminating Female M. septendecim were often `receptive' than those of M. cassini. The males court (immobile) to courting contacts with silent males. inappropriate objects more often, and the females Indeed 35 % of the courtship patterns without appear to accept inappropriate courtships more song elicited immobility in M. septendecim . All often. Although the responses were not statisti- of these were intraspecific courtships, so the cally different, they may be different enough to responses of the females were appropriate, at maintain species separation in a multispecific least in terms of the species of the male . The singing centre . Because M. cassini do discrimi- question remains as to how the females knew to nate better, the consequences of M. septendecim which species the courting male belonged in behaviour are not detrimental to the mainte- these cases . The answer is unknown, though we nance of species integrity, as long as only the two might postulate that the males had been singing species are present in the same place at the same earlier in each silent courtship and that the time. females had already made their decisions before The results of all of these studies demonstrate we began to observe the interactions. In two of that, in periodical cicada emergence sites where the six observed copulations in the Michigan both Magicicada septendecim and M. cassini emergence of 1970 and in one of the three are actively courting, reproductive isolation is copulations seen in Illinois, the whole courtship, maintained mainly through mate selection by from initial approach through copulation, was females who use acoustic differences between recorded. There were no songs produced at all . the songs of the males of the two species to These results remain inexplicable, although we discriminate among them. may hypothesize the existence of other sensory cues, perhaps pheromonal ones . Acknowledgments In spite of these apparently anomalous results, We thank Dr Richard D. Alexander, with whom it appears that the primary sensory information the senior author worked on Brood X in Michigan used by female periodical cicadas to discriminate in 1970. Dr Alexander was most generous of time among courting males is acoustic. Certainly the and research space for a novice cicada person models' visual resemblances to male cicadas and provided an exciting introduction to work on were minimal, and the tactile signals generated these animals . He also read and criticized an only clumsily similar to those used by real males early draft of this paper. in courtship. Yet the females tolerated contact The 1973 experiments were done on sites made with these blundering models amazingly well . available by the Argonne National Laboratory Differential responses could only be detected in Argonne, Illinois . Dr Jerry Klein kindly when a female cicada was moving . Although the sponsored us there, and the laboratory provided differences were not significant for M. trailer parking space on the grounds . Indiana septendecim, even these females did `accept' more University, through Dr Roderick Suthers, courtships from the model when it was singing generously provided camping and laboratory conspecific songs, as opposed to the songs of the facilities at the University field station for the other species or none at all. The models were much 1974 experiments on Brood XIV. We thank more persistent in their 'courtships' than were Drs Klein and Suthers and their respective the M. septendecim males, in that there were institutions for all their assistance . many more bouts in each courtship. In this the We are indebted to Dr Tom Moore, Dr Monte models' courtship `strategies' were more similar Lloyd, Dr JoAnn White, and Christine Simon for to those of M. cassini than to M. septendecim . rewarding discussions of periodical cicada This very persistence, then, may have mediated biology. the females' apparent responses, rather than any The 1973 and 1974 experiments were supported acoustic differences. The female M. septendecim by a grant from the National Institute of Mental under-reacted to the models' courtships as they Health, No . MH-21076. did when courted by live M. cassini males. They were unreceptive and had so indicated by moving away. The fact that they later stopped may have REFERENCES been unrelated to the behaviour of the courting Alexander, R. 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