Male Cicadas Research Articles

Ambient temperature and sound power of cicada calling songs (Hemiptera: Cicadidae: Tibicina)

Abstract. Male cicadas produce a loud calling song that attracts females at long range. In some cases, ambient temperature has been shown to have an effect on the temporal structure of this acoustic signal. Here, a positive correlation is reported for the first time between the ambient temperature and the sound power of the calling song. This relationship is illustrated in three species of the Palaearctic genus Tibicina: Tibicina corsica fairmairei Boulard, Tibicina garricola Boulard and Tibicina tomentosa Olivier. It is suggested that the males thermoregulate behaviourally. The minimal ambient temperature range that the Tibicina species need to call is 22–24 °C. The effect of ambient temperature on calling song power is assumed to be the result of thermal effects in the response of the acoustic system (i.e. muscle activity of the acoustic system being temperature‐dependent). Inter‐individual and interspecific differences in calling song power are interpreted in the general context of the Tibicina sound behaviour.

A COMMENT ON GENE INTROGRESSION VERSUS EN MASSE CYCLE SWITCHING IN THE EVOLUTION OF 13-YEAR AND 17-YEAR LIFE CYCLES IN PERIODICAL CICADAS

In companion papers, Simon et al. (2000) and Marshall and Cooley (2000) discuss geographic distributions of phenotypic characters and genetic markers of Magicicada decim spp. in the lower Mississippi valley and vicinity. Periodical cicadas (Magicicada spp.) of eastern North America have spurred many debates concerning the evolutionary origin of their unusual 13-year and 17-year life cycles, and instantaneous speciation through en masse cycle switching has been a recurring hypothesis. En masse switching both from 13to 17-year cycles and from 17to 13-year cycles are components of the cycle-switching model of Magicicada evolution (e.g., Lloyd and Dybas 1966a, 1966b; Lloyd and White 1976; Simon 1979, 1988; Martin and Simon 1988, 1990; Williams and Simon 1995). The new field data of Marshall and Cooley (2000) document character displacement between 13-year cicadas with genotypes similar to northern 17-year populations, and sympatric 13-year cicadas with genotypes similar to southern 13-year populations. Simon et al. (2000) interpret this character displacement and other new genetic data as support for the hypothesis of instantaneous speciation by en masse cycle switching from 17to 13-year cycles. However, it is our view that these authors do not adequately explore conventional gene flow explanations of the observed phenotypic and genetic variation that do not require en masse cycle switching. Evaluation of these competing hypotheses can benefit from an interdisciplinary perspective incorporating paleoecological data. We (Cox and Carlton 1988, 1991, 1998; Cox 1992) previously proposed an alternative selection-gene introgression model for Magicicada evolution incorporating paleoecological reconstructions that also explains these new genetic and phenotypic observations of Simon et al. (2000) and Marshall and Cooley (2000). Our hypothesis offers an important caveat about the use of mtDNA in certain circumstances to interpret the magnitude of gene flow between populations and evolutionary processes. We hypothesize unidirectional gene flow via dispersing male cicadas that transferred limited nuclear DNA and no mtDNA to the recipient population. In brief, our model presented in Cox and Carlton (1988) proposes that life-cycle timing differences between cicada populations arose not from en masse cycle switching, but from stochastic selection processes involving Magicicada temperature thresholds, Pleistocene climate characteristics, and hybridization frequencies between populations having a spectrum of life-cycle lengths. Heath (1967, 1968) reports that periodical cicadas emerge from their burrows when soil temperature is 64.3?F and that the air temperature must reach 68?F for flight and mating. In our quantitative model, during glacial maximum it was much more common than it is now for summers to remain too cold for ancestral periodical cicadas to emerge and/or mate, and the ancestors of periodical cicada populations must have failed to reproduce during those years. This seasonal capriciousness gave rise to periodicity (years without cicadas) and selection of long life cycles (conferring a reduced chance of emerging on a cool summer). By the parameters of our model, selected life cycles would be ? 12 years and would be longer in colder climates. This aspect of our model explains the climatically correlated zonation of Magicicada life cycles (Fig. 1). Once periodicity and long life cycles were established, satiation of predators by synchronized emergence became an important strategy for periodical cicadas. Predator satiation works best with precisely synchronized periodicity, and cycle synchronization is diminished by increased heterozygosity. Thus, cicadas that are hybrids of two populations with different cycle lengths will suffer greater predation losses, as many may emerge on years before or after the main population. Cicadas with prime-numbered cycles (13 years and 17 years) will hybridize significantly less frequently than cicadas with non-prime (composite) cycles and thus will have larger emergences and a greater advantage of predator satiation. See Cox and Carlton (1988) for a full discussion of this topic. Marshall and Cooley (2000) studied M. decim spp. of southern 13-year Brood XIX (each brood consists of all synchronized individuals) within the contact zone with more northern 17-year broods (M. septendecim). These authors document character displacement of call pitch between male 13year cicadas with abdominal coloration like cicadas of contiguous 17-year populations (new 13-year cicadas, M. neotredecim) and sympatric male 13-year cicadas with coloration like contiguous Brood XIX populations in the lower Mississippi valley (old 13-year cicadas, M. tredecim). Marshall and Cooley (2000, see their Figs. 4 and 9) argue that M. tredecim have never been present within the range M. neotredecim north of the contact zone and that these two species have hybridized only along the contact zone at the southern margin of the M. neotredecim range. The steep gradient in call pitch frequency along the southern margin of M. neo-

Behavioral and physiological thermoregulation in male cicada killers ( Sphecius speciosus) during territorial behavior

(1) Male cicada killers had elevated, apparently regulated, thoracic and head temperatures during territorial perching and patrolling in full sunshine. (2) Dead, dry wasps reached near-lethal temperatures on the bare ground, and were hotter with their bodies perpendicular to the sun's rays, as opposed to parallel. (3) The percentage of males perching on the ground, their perch duration, and the percentage oriented perpendicular to the sun decreased during the mid-day. (4) Males used a low-amplitude wing vibration early and late in the day, perhaps boosting heat production. (5) Changes in behavior were related to changes in the intensity of solar radiation.

Effects of Size and Flight Performance on Intermale Mate Competition in the Cicada Killer, Sphecius speciosus Drury (Hymenoptera: Sphecidae)

The characteristics of successfully mating male cicada killers (Sphecius speciosus Drury) were compared to those of unsuccessful males. In the field, successful males were larger and had higher ratios of flight muscle mass to body mass (flight muscle ratios) than unsuccessful males. The elevated flight muscle ratio of successful males was not because of semen transfer to the female nor because of an allometric effect. Better territory-holding ability and flight maneuverability probably contribute to the success of large males with a high flight muscle ratio in nature under most conditions. However, temporal or situational conditions may also exist whereby small males may occasionally have opportunities to mate.

Substrate-transmitted acoustic signals of the primitive cicada, Tettigarcta crinita Distant (Hemiptera Cicadoidea, Tettigarctidae)

Male cicadas are familiar for their unique loud airborne calls used in courtship and mate recognition. Extant Tettigarcta species in Australia are little-known relict survivors of a primitive Mesozoic cicada radiation which do not make loud calls and lack either the apparatus to produce them or the auditory organs to detect them. Field studies on live insects in New South Wales for the first time show that Tettigarcta produce low-intensity, substrate-transmitted acoustic signals in courtship. This habit seems to be a primitive (plesiomorphic) feature.

The use of landmarks to define territorial boundaries

Numerous anecdotal reports suggest that members of many territorial species use naturally occurring landmarks to define the boundaries of their territories. In the work reported here, we first tested whether artificial landmarks would be adopted as boundaries by territorial male cicada killer wasps, Sphecius speciosus . To perform this test, we set out wooden dowels on a flat, grassy lawn on which male wasps were defending mating territories. The dowels were situated so that they did not coincide with any existing territorial boundary. After we provided the dowels, the wasps established new territorial boundaries coinciding with the dowels. We hypothesized that using visual landmarks as territorial borders might lower defensive costs, and indeed, focal samples on territorial wasps revealed that borders that were defined by dowels cost less to defend than did borders that were not defined by any landmark. This result suggests that the use of natural landmarks as territorial boundaries may have evolved as a result of the reduced defensive costs that accrue to these boundaries. Furthermore, defensive costs may not depend directly on territory size: territory owners may be able to reduce defensive costs by selecting sites with high tactical defensibility.

Analysis of Acoustic Signals Produced by the Cicada Platypedia putnami Variety lutea (Homoptera: Tibicinidae)

Most male cicadas produce calling songs to attract females, and most cicadas use a specialized timbal organ to produce sound. However, several cicada genera can produce acoustic signals through stridulation or crepitation either in addition to or in place of the timbal song. We analyzed the acoustic signals produced by a crepitating cicada, Platypedia putnami variety lutea Davis. Peak frequency of the sound pulses produced by crepitation were determined to be 10.18 and 9.66 kHz for males and females, respectively. Individual pulse duration was ≈10 ms. Males produced pulses at a rate of 8.68 Hz and females produced pulses at a rate of 18.76 Hz. We found a delay of ≈40 ms between a male pulse and the response by a female. The mean sound pressure level (89.7 dB) of crepitating P. putnami variety lutea did not differ significantly from the predicted value, based on the regression of call intensity as a function of body mass for cicadas producing timbal songs previously published.

Auditory response and intrinsic link with sound-production in singing male cicada

In the black cicada (C. atrata Fabricius), the quiescent males are sensitive to stimulating sound-pulses of about 70 dB (SPL); the latent periods and amplitudes of compound action potentials of the auditory nerve (called "auditory nerve potential (AP)" for short) which are corresponding one by one to stimulating sound-pulses are (3.92 +/-0.28) ms and (0.32+/-0.22) mV on an average, respectively. Although the singing males are nonreactive to outside stimulating sound-pulses, they are still sensitive to calling pulses mingling in stimulating sound-pulses; the latent periods and amplitudes of auditory nerve potentials are (4.16 +/- 0.43) ms and (0.46 +/- 0.25) mV, respectively. In singing males the negative potential before each auditory nerve potential characterizes that the intrinsic link exists between sounding and auditory nerve system.

THE SCALING OF SONG FREQUENCY IN CICADAS

In male cicadas, sound is generated by a pair of tymbals on the abdomen (Pringle, 1954). The tymbals buckle inwards causing pressure changes in the abdominal cavity, from which sound is radiated through the tympana (Young, 1990). A recent model of sound production in cicadas suggests that the abdominal cavity and tympana act as the components of a Helmholtz resonator that is excited by the drive from the tymbals (Bennet-Clark and Young, 1992). A Helmholtz resonator consists of a cavity open to the outside via a hole which has a real or notional neck, and the resonant frequency fo is given by the general equation: where c is the speed of sound in the fluid, taken as 340 m s-1 for air, A is the area of the neck, L is the length of the neck and V is the volume of the cavity. Where the resonator has two holes, these terms should be somewhat modified: A is the combined area of the two holes, L is 16/3pi r (~1.7r) for a simple hole in a thin-walled vessel and r is the radius of one hole (Seto, 1971). These modifications to equation 1, which include corrections for the acoustic end-effect at either side of a simple hole in the wall of a vessel, are applicable to a model of the male cicada, in which there are two tympana close to the ventral surface of the abdomen.

A Model of the Mechanism of Sound Production in Cicadas

ABSTRACT Dried cicada bodies of the species Cyclochila australasiae and model cicadas made from a miniature earphone driving a plastic cavity were used to study the acoustics of sound production in male cicadas. A model cicada with shape and dimensions similar to those of the abdomen of a male C. australasiae resonates at the natural song frequency of the species (4.3 kHz). The abdominal air sac of C. australasiae also resonates at frequencies close to the natural song frequency when excited by external sounds. In an atmosphere of chlorofluorocarbon (CFC) gas, the resonant frequency is lowered in keeping with the decrease in velocity of sound in the CFC gas. At the model’s resonant frequency, the driving earphone dissipates more electrical power with the cavity attached than without the cavity. The cavity of the model cicada acts as a narrow-band acoustic acceptance filter, tuned to the natural song frequency. When the miniature earphone emits brief clicks, mimicking those produced by the natural tymbal mechanism, the model cicada produces sound pulses that vary in duration and shape according to the number and timing of the clicks. A coherent train of two or three resonant clicks results in a long slowly-decaying sound pulse similar to that in the natural song. The natural song frequency can be predicted from the dimensions of the abdominal cavity and the tympana in C. australasiae using a simple equation for the resonant frequency of a Helmholtz resonator. This equation also predicts the song frequency of Macrotristria angularis and Magicicada cassini, but it fails with the low-frequency song of Magicicada septendecim. This discrepancy can be accounted for by the unusually thick tympana of M. septendecim, which tend to lower the resonant frequency of the system. We conclude that the abdomen of male cicadas forms a Helmholtz resonator, the components of which are the large air sac as the cavity and the tympana as the neck of the resonator. We suggest that cicada sound production depends on the coupling of two resonators, that of the tymbal and that of the abdominal air sac, from which sound is radiated through the tympana. The coupled resonator system would produce the long sound pulses required for stimulating a sensitive sharply tuned auditory organ.

Red-winged blackbird predation on periodical cicadas (Cicadidae: Magicicada spp.): bird behavior and cicada responses.

Predation by red-winged blackbirds Agelaius phoeniceus L. on 13-year periodical cicadas (Magicicada spp.) and reactions by periodical cicadas to predators were studied during emergence of Brood XIX during summer of 1985 in northwestern Arkansas (USA). Emergences of periodical cicadas are classic examples of predator satiation due to high local densities of cicadas and birds are the major predators of adult periodical cicadas. Reactions of periodical cicadas to predators were assessed by recording behaviors exhibited by cicadas when approached in trees by a human hand during the 3-week period of peak adult densitics. Most male cicadas made a noise in association with escape behaviors when approached, and 50% of the females, which are silent, attempted escape behaviors. Observations of predation attempts on cicadas by red-winged blackbirds were made during the period of peak predation pressure. Red-winged blackbirds spent less time searching for cicadas over that 2-week period of increasing predation pressure, and became increasingly efficient at capturing cicadas. Handling time of cicadas by red-winged blackbirds increased by about 20 seconds over that period, as blackbirds spent more time consuming female cicadas. The flysquawk response, used only by male cicadas, was effective in deterring red-winged blackbirds; only 5% of the attacks by blackbirds were successful when that behavior was exhibited. All cicadas that remained motionless and silent when approached by blackbirds were captured and consumed. Because females remained inactive when approached more often than did males, blackbirds may have consumed more female cicadas. Changes that appeared in reactions of preiodical cicadas to the model predator and to the attacks of blackbirds reflect both changes in the sex ratio of the cicada populations and changes in behaviors of cicadas associated with mating and egg laying. The loud noise made by male periodical cicadas at mating centers did not appear to deter predation by blackbirds. Changes in the behavior of blackbirds that appeared to be in association with greater predation on female periodical cicadas relates directly to aspects of foraging theory, particularly predictions concerning more selective foraging during periods of abundant food resources.

A Synchronous Insect Muscle With an Operating Frequency Greater Than 500 Hz*

ABSTRACT The male cicada, Okanagana vanduzeei, produces a calling song with a pulse repetition frequency of 550 Hz. This sound is produced by a pair of tymbals, each of which is buckled by a large tymbal muscle. Males sing in full sun and the operating temperature of the tymbal muscles is 40–45 °C. Analysis of the songs of animals with the tymbal mechanism destroyed on one side, and of the sounds produced by directly manipula-ting a tymbal, indicates that the two tymbals normally buckle synchro-nously and that only one sound pulse is produced per tymbal muscle contraction. This implies that the contraction frequency of each tymbal muscle is 550 Hz. Recordings of calling songs from animals with implanted electrodes show that there is usually synchrony between left and right tymbal muscle contractions and that each tymbal muscle can operate at a frequency of about 550 Hz. The recordings also show that there is a 1:1 correlation between muscle electrical and mechanical activity, i.e. these muscles are synchronous and not asynchronous muscles. The ultrastructure of the tymbal muscle is clearly that of a very fast, synchronous muscle: the myofibrils are small, the sarcoplasmic reticulum is extraordinarily well developed, and the T-tubules lie at the 1/4 and 3/4 positions along the sarcomere. When set up for isometric recording, with their nerve supply severed, the tymbal muscles often show spontaneous electrical and mechanical oscillations. The frequency of these oscillations is strongly temperature dependent, and at higher temperatures approaches the normal operating frequency of the muscle. The tendency to oscillate is so strong that single twitches could only very rarely be evoked by electrical stimulation. A twitch duration of under 6ms was observed at 30°C. We conclude that the tymbal muscle of O. vanduzeei is indeed a synchronous muscle, albeit a highly modified one, capable of operating at 550 Hz. We suggest that the advantages of asynchronous muscles lie chiefly in their greater economy of structure and operation, rather than in an ability to operate at higher frequencies than synchronous muscles.

Observations on the aggregation of adult cicadas (Homoptera: Cicadidae) in tropical forests

The distribution of adult cicadas in various tree species was studied in Costa Rica. These observations indicate that tropical cicadas, mostly males, often congregate in certain tree species in various kinds of secondary forest habitats. Aggregated male cicadas exhibit intense chorusing and females fly into chorusing aggregations, presumably for mating. Trees used for aggregations are also cicada feeding sites. The conspicuous absence of oviposition evidence or nymphal skins suggest that these trees are used primarily for intensive male chorusing which assembles females for mating. Tendency to congregate in particular trees is related to the spatial position of the trees and their exposure to direct sunlight. Highly fragmented forest patches in some regions (central highlands, lowland Guanacaste) function as islands for cicadas to complete their life cycles and mating, whereas the abundant secondary forest habitats in other regions (northeastern lowlands) are being invaded by a few species which use secondary forest trees for completion of life cycles and mating. The apparent absence of dense aggregations of adult cicadas within climax tropical forests, even though nymphal skins are found here, is probably related to the very patchy distribution of individuals of each tree species and perhaps other factors (i.e., shading) affecting the attractiveness of trees for congregating cicadas.

Acoustics of Sound Production and of Hearing in the Bladder Cicada Cystosoma Saundersii (Westwood)

ABSTRACT The male cicada of the species Cystosoma saundersii has a grossly enlarged, hollow abdomen and emits a loud calling song with a fundamental frequency of about 800 Hz. At the song frequency, its hearing is non-directional. The female of C. saundersii lacks sound producing organs, has no enlargement of the abdomen, but possesses an abdominal air sac and has well developed directional hearing at the frequency of the species’ song. Physical mechanisms are proposed that explain these observations in semi-quantitative detail using the standard method of electrical network analogues. The abdomen in the male, with its enclosed air, is found to act as a system resonant at the song frequency, thus contributing a large gain in radiated sound intensity. Coupling between this resonator and the auditory tympana accounts for the observed hearing sensitivity in the male, but destroys directionality. In the female, the abdominal cavity acts in association with the two auditory tympana as part of a phase shift network which results in appreciable directionality of hearing at the unusually low frequency of the male song.

COLCONDAMYIA AUDITRIX NOV. SP. (DIPTERA: SARCOPHAGIDAE), A PARASITE WHICH IS ATTRACTED BY THE MATING SONG OF ITS HOST, OKANAGANA RIMOSA (HOMOPTERA: CICADIDAE)

AbstractA new species of sarcophagid, Colcondamyia auditrix, is described, which locates its cicada host by sound. The fly was shown to respond to the mating song of the male cicada, and the majority of parasitized cicadas were male. Parasitism of females occasionally occurs when they are attracted to males simultaneously with the parasite. Levels of parasitism varied from 18.6% in 1962 to 0.2% in 1967 to 14.1% in 1973. Male cicadas lost their sound producing capability following parasitization, rendering them inaccessible to further female flies and thus apparently preventing multiple parasitism.

Role differentiation in copulating cicada killer wasps.

Copulating male and female cicada killer wasps have distinct behavioral roles independent of reproduction. Males terminate copulation, and females initiate the copulatory flight in which the pair in copulation escape potential danger. Separation and escape behavior are mutually exclusive. Separation occurs because the female clings to the substrate and fails to join the male in his frequent attempts at flight; thus he eventually pulls free. Escape occurs when the female begins flight, which the male readily joins. Differences in thresholds for flight probably largely determine both roles. There appears to be an evolutionary balance in escape and separation behavior determined by the behavior of the female, and illustrative of behavioral homeostasis. The female remains still in the presence of mild stimuli, such as attempted male flights, and thereby aids in separation; she initiates escape in the presence of strong stimuli such as potential enemies.

Territorial Behavior in the Cicada Killer Wasp Sphecius Speciosus (Drury) (Hymenoptera: Sphecidae). I

Male cicada killers (Sphecius speciosus) set up territories which are defended against intrusion by other males, other insects, and even thrown pebbles. Territory owners continually return to territorial perches, usually emergence holes. There is no apparent tendency for wasps to utilize their own holes of emergence as territorial perches. Aggressive flights by the owner terminate in one of four fashions, depending on the type of intruder and its behavior. Non-aggressive males and non-aggressive insects of other species are pursued without the owner getting within striking distance. Nonaggresive, slow-flying forms of other insect species are overtaken, and after an aggressive approach (here termed threat) the owner abruptly ends the chase. Non-aggressive male wasps or slow-flying insects of other species are butted by the owner. Grappling occurs with aggressive conspecific males and occasionally with non-aggressive conspecific males. Aggressive intrusion occurs when the intruder possesses an adjacent territory and first reacts to his neighbor while over his own territory. Most territories are set up in areas of high emergence hole density. Territorial behavior enhances mating efficiency by spacing the males and thereby increasing the frequency of male-female interaction. Localizing of territories in places of high emergence hole density fosters male-female interaction because the owners are more likely to contact emerging females. Mating efficiency is also probably enhanced by a reduction in the frequency of male-male interactions, thereby reducing the interference of superfluous males during precopulatory behavior.