Phonotactic parasitoids and cricket song structure: An evaluation of alternative hypotheses

Summary Calling characteristics of field crickets (Teleogryllus oceanicus) differ between Pacific populations parasitized and unparasitized by a phonotactic fly (Ormia ochracea). Although we inferred that these song differences were due to natural selection by the fly, other environmental differences among sampling localities may also influence the cricket song. To evaluate the contribution of parasitoid pressure to variation in song structure, we analysed calls of crickets from five areas arrayed along a gradient of prevalence of parasitization. A novel use of canonical correlation analysis allowed us to test simultaneously the robustness of alternative hypotheses and their predictions. There is strong inference that selection pressures by phonotactic parasitoid flies have shaped song characteristics of field crickets in the Hawaiian Islands. Not all song components appear to have been equally affected by parasitoid selection and approximately 80–90% of total song variation among individuals is associated with other, unmeasured ecological and environmental attributes.That songs evolve is not disputed, but that they evolved in certain directions or that song structure is due to the action of certain forces, or that differences are due to random evolutionary events, or that they are the result of selection, or that they arise mainly in association with speciation — these are matters for speculation, debate, and analysis.Otte (1992, P. 25)     

Calling song and selective phonotaxis in the field crickets,Gryllus firmus andG. pennsylvanicus (Orthoptera: Gryllidae)

The field cricket species, Gryllus firmusand G. pennsylvanicus,occur in a mosaic hybrid zone that roughly parallels the eastern slope of the Appalachian mountains in the northeastern United States. It is important to know what role, if any, the calling song plays in mate choice in sympatric and allopatric populations. In this report, we present results on the variability of calling song properties along transects across this hybrid zone. We also present the results of experiments on phonotactic selectivity of females from an allopatric population of G. firmus.The male calling song of allopatric G. firmuswas significantly slower in temporal rhythm (i. e., chirp and pulse repetition rates) and lower in pitch (i.e., dominant frequency) than that of allopatric G. pennsylvanicus.Calling song properties of males recorded in the hybrid zone varied considerably in temporal and spectral properties. In two-stimulus (choice) phonotaxis experiments, allopatric females of G. firmuspreferred synthetic calling songs with conspecific pulse repetition rates over songs that had lower and higher pulse rates. This preference persisted even when the sound pressure levels of alternative stimuli were unequal. Therefore, allopatric females of G. firmuscan discriminate between conspecific and heterospecific calling songs. Whether or not this same selectivity is present in sympatric populations remains unclear. Investigations of phonotactic selectivity in other allopatric and sympatric populations of both species are currently under way.     

The influence of auditory and visual experience on the phonotactic behavior of the cricket,Gryllus bimaculatus

Female crickets lacking experience with phonotaxis to conspecific calling song respond to trains of continuously repeated sound pulses (trill), whereas experienced females do not. In the present study such inexperienced crickets were tested for their responsiveness to trills of pulse repetition periods from 30 to 70 ms on a Y- shaped maze. Stimulation with a repetition period of 30 ms led to unexpectedly low phonotactic and exploratory activity. Initial stimulation with trills of 30- ms repetition period drastically reduced the responsiveness of inexperienced animals to conspecific calling song and other attractive stimuli. Effects of visual stimulation on the phonotactic behavior of female crickets are demonstrated. Threatening visual stimuli changed the behavior of experienced animals to a state that resembles that of inexperienced animals. The relevance of these observations is discussed with respect to the development of the auditory pattern recognition mechanism in crickets.     

Calling behavior of the female german cockroach,Blattella germanica (Dictyoptera: Blattellidae)

Virgin German cockroach females, Blattella germanica(L.), were observed, for the first time, to exhibit a characteristic calling behavior during which females emit a volatile sex pheromone. Under a photoperiod of 12L12D, the percentage of 7-day-old virgin females that exhibited this behavior peaked before the end of the scotophase in a similar pattern to the diel periodicity of mating. A clear relationship was evident between calling and stages of sexual receptivity during successive gonotrophic cycles. Females initiated calling 5–6 days after the imaginal molt, when their basal oocytes were 1.6 mm long. If not mated, females continued to exhibit bouts of calling during the next 3–4 days until 24 h before ovulation. Calling was completely suppressed by mating as well as the presence of an egg case in the genital atrium in both virgin and mated gravid females. We suggest that calling and the emission of a volatile sex pheromone serve to attract males from a distance as well as to potentiate responses to contact sex pheromone in aggregations.     

Seasonal Variation in Female Response to Male Calling Song in the Field Cricket, Gryllus rubens

Conspicuous traits that make males attractive to females may make them vulnerable to predators. Females that approach conspicuous males may increase their risk of predation. This means that selection for reduced male conspicuousness in the presence of predators may be due to sexual selection resulting from altered female behavior in the face of increased predator risk. We examine this hypothesis in the field cricket, Gryllus rubens, in which male calling song attracts both conspecific females for mating and parasitoid flies (Ormia ochracea) which kill their hosts within a week. Female crickets are also parasitized by these flies as a result of associating with calling males. In northern Florida crickets that emerge in the spring are not subject to fly parasitism whereas autumn crickets encounter large numbers of flies. We predicted that autumn females should be less attracted to male song than spring females. We tested female response to male calls in a rectangular arena in which male calling song was broadcast from a speaker. Spring females readily approached the speaker but autumn females were less likely to approach and remain in the vicinity of the speaker. These results emphasize the importance of considering how risk affects the evolution of conspicuous male behavior both directly through its effect on the male and indirectly through its effect on female responses to males.     

Temperature Effects on the Temporal Properties of Calling Songs in the Crickets <Emphasis Type="Italic">Gryllus fultoni</Emphasis> and <Emphasis Type="Italic">G. vernalis</Emphasis>: Implications for Reproductive Isolation in Sympatric Populations

Two closely related wood-cricket species, Gryllus fultoni (Orthoptera: Gryllidae) and G. vernalis, produce similar calling songs, consisting of 3-pulse chirps. Analysis of field and laboratory recordings of calling songs showed that, after correction to a common temperature, there was a divergence in chirp and pulse rates between far allopatric populations of G. fultoni and populations sympatric with G. vernalis. To determine whether the divergence in calling songs potentially provides reproductive isolation between G. fultoni and G. vernalis throughout the temperature range over which these insects sing, we recorded calling songs of lab-reared G. fultoni and G. vernalis populations between 18 and 28°C. Mean chirp rate significantly differed between sympatric and far allopatric G. fultoni populations as well as between sympatric G. fultoni and G. vernalis populations. Although there was a significant difference in mean pulse rate between sympatric G. fultoni and G. vernalis populations, pulse rate did not differ between sympatric and far allopatric G. fultoni populations in the laboratory study. Considering the magnitudes of differences in calling song characters discriminated by females of G. fultoni and the mean differences and the variability in calling song characters between the two species, the joint difference in chirp and pulse rates may be adequate for species discrimination over most of the range at which these crickets breed.     

Inter- and intraspecific variation in nightly calling duration in field crickets,Gryllus integer andG. rubens (Orthoptera: Gryllidae)

The time that male field crickets spend calling was measured electronically in the laboratory to examine nightly calling duration from different species and populations. Male Gryllus integerfrom Davis, CA, and Las Cruces, NM, called approximately 7 h per 24 h, whereas male G. integerfrom San Antonio and Austin, TX, and Norman, OK, and male G. rubensfrom McAlester, OK, and Arkadelphia, AR, called approximately 3 h per 24 h. Variation in duration of calling is discussed in terms of the energetic costs of producing song and selection against calling by acoustically orienting parasites and predators. Duration of calling was also studied infield-collected male G. integer.Males were first observed in field populations and then collected. Those males observed calling in the field later called significantly more in the laboratory than males observed showing non-calling, satellite behavior. Flying G. integercollected under lights were intermediate in their calling duration to calling and satellite males. These data are discussed in terms of the heritability of nightly calling song duration infield crickets.     

Cricket phonotaxis: localization depends on recognition of the calling song pattern

Summary Calling song with a carrier frequency of 5 kHz evokes positive phonotaxis in female crickets,Gryllus bimaculatus, when presented at an azimuth. In contrast, a continuous tone of 4.7 kHz in the same position when paired with calling song from above leads to negative phonotaxis. Under open-loop conditions, when a tethered animal runs on a paired tread wheel, characteristic curves are produced with the stable equilibrium point towards or away from the stimulus, respectively (Fig. 3).In order to understand this sign reversal at the neuronal level, directional characteristics of the ascending acoustic inter neurons AN1 and AN2 were measured using extracellular recordings from the cervical connectives.Taking the mean spike rate of the interneurons as a measure for their excitation, the function relating response magnitude to stimulus direction for calling song corresponds well to the behavioural characteristic curve (Fig. 5). The response function obtained using a continuous tone with simultaneous presentation of calling song from above is similar (Fig. 5) and hence does not correspond to the inverse behavioural characteristic curve.However, consideration of the extent to which the temporal parameters of the calling song (syllables and chirps) are reflected in the neuronal response (amplitudes of the Fourier components) leads to characteristic curves for AN1 and AN2 which are in good agreement with the behaviour for stimulation with calling song as well as for the continuous tone experiment (Fig. 8). In addition, the neural response curves correspond to the behaviour in showing smaller amplitudes when a continuous tone rather than the calling song is presented on the horizon (Fig. 8).From these data we conclude that the activity in interneurons AN1 and AN2 does not directly guide orientation in mating behaviour but first is filtered by a mechanism tuned to the frequency of syllables and/or chirps. According to this hypothesis recognition of conspecific song and localization proceed sequentially inGryllus.     

The Introduction, Establishment, and Spread ofOrmia depletain Florida

Ormia depleta(Wiedemann) (Diptera: Tachinidae), native to Brazil, is a parasitoid of someScapteriscusspecies (Orthoptera: Gryllotalpidae). It was first cultured in a laboratory in Florida in 1987. Releases ofO. depletawere made againstScapteriscusmole crickets in all regions of Florida beginning in 1988. Establishment of populations was achieved at some, but not all, of the release sites. The two earliest-established populations were monitored using traps employing synthetic calling song of maleScapteriscusmole crickets, to which gravid female flies are attracted. Additionally, progeny of the released flies were trapped between 1988 and 1993 in 32 peninsular counties, including 15 counties in which no releases had been made. The most parsimonious explanation of the pathways of spread of the current population was inferred from trapping surveys, and this yielded the probable year of colonization for peninsular counties. Reports in successive years by golf course superintendents of damage by mole crickets showed that counties withO. depletapopulations had significantly less damage than did yet-uncolonized counties.     

CALLING SONGS OF FIELD CRICKETS (TELEOGRYLLUS OCEANICUS) WITH AND WITHOUT PHONOTACTIC PARASITOID INFECTION

The field cricket Teleogryllus oceanicus has been introduced to Hawaii, where it is parasitized by an acoustically orienting parasitoid fly, Ormia ochracea. Previous work showed that call parameters from parasitized populations differ from those in unparasitized populations in a direction expected if selection by flies is occurring. Here we examined songs of males collected in the field and compare calling song characters of crickets later found to harbor parasitoid larvae with those of males free of parasitoids. The two groups differ significantly in several song characteristics, particularly the trill-like long chirp given at the beginning of each song. Males with longer long chirps containing shorter interpulse intervals are more likely to be parasitized, suggesting that the flies find such males more attractive. Depending on the traits females prefer, sexual selection may oppose natural selection in altering T. oceanicus song in parasitized populations.     

Auditory pattern recognition and steering in the cricket Teleogryllus oceanicus

Male crickets Teleogryllus oceanicus (Le Guillou) produce a complex species‐specific calling song with phrases combining groups of single pulses (chirps) and groups of double‐pulses (trills) to attract females, which fly or walk towards singing males. In open‐loop trackball experiments, phonotactic steering responses to normal calling song phrases consisting of chirps and trills are strongest, suggesting that both components are necessary for maximal attractiveness. Sequences of just chirps or trills are less effective in eliciting phonotactic walking and steering. Split‐song paradigms are used to analyze the steering behaviour underlying orientation in more detail. The females' phonotactic steering reflects the alternating acoustic pattern of the split‐song paradigm. Analysis with high temporal resolution demonstrate, that even when the calling song is presented only from one side, the steering velocity and lateral deviation towards the song is modulated by steering events to single‐sound pulses. Therefore, pattern recognition, which integrates the structure of the song, appears not to be directly involved in the rapid steering response. This organization of phonotactic behaviour with a parallel processing of pattern recognition and steering is similar to other cricket species and may allow T. oceanicus females to steer transiently towards distorted song patterns as they occur in natural habitats.     

Nocturnal behaviour of female Mythimna convecta

Nocturnal behaviour of Mythimna convecta (Walker) (Lepidoptera: Noctuidae) virgin females was studied in the laboratory under 20 °C and 16:8 LD conditions. The periodicity of activity, feeding, calling, pre-oviposition extrusion and oviposition varied with female age and hour of the scotophase. Females called for the first time between the 2nd and 11th scotophases with the peak in the 4th scotophase. Maximum calling occurred on the 7th hour of the scotophase. Young moths called more frequently with shorter bouts while old moths called less often but with longer bouts. In the presence of older females, moths spent significantly more time in pre-oviposition extrusion and resting and less in activity and feeding than they did when only females of the same age or younger were present. There were no significant differences for calling suggesting that pheromones of older calling females did not affect calling of younger females.     

Divergent Preferences for Song Structure between a Field Cricket and its Phonotactic Parasitoid

In many animals, males produce signals to attract females for mating. However, eavesdropping parasites may exploit these conspicuous signals to find their hosts. In these instances, the strength and direction of natural and sexual selection substantially influence song evolution. Male variable field crickets, Gryllus lineaticeps, produce chirped songs to attract mates. The eavesdropping parasitoid fly Ormia ochracea uses cricket songs to find its hosts. We tested female preferences for song structure (i.e., chirped song vs. trilled song) in crickets and flies using choice experiments. Female crickets from a parasitized and a non-parasitized population significantly preferred the species-typical chirped song, whereas flies significantly preferred a trilled song, which is expressed by other hosts in different regions. Sexual selection due to female choice and natural selection due to fly predation both appear to favor the chirped song structure of G. lineaticeps in the parasitized population, whereas sexual selection favors the chirped structure in the non-parasitized population.     

Circadian calling behavior of the adult female brown-banded cockroach,Supella longipalpa (F.) (Dictyoptera: Blattellidae)

The diel pattern of pheromone-releasing behavior (calling) of the adult female brown-banded cockroach, Supella longipalpa (F.),was examined. Calling occurs discontinuously throughout most of the scotophase in a 12L: 12D photoperiodic regime. Females exhibited a free-running calling rhythm after transfer to continuous light or dark conditions. Shifts in the temporal pattern of calling following changes in the timing of the photoperiodic cues indicated that lights-off is the Zeitgeber. Studies of insects under long- and short-day conditions suggest that, although insects within a population may call synchronously or asynchronously, respectively, the duration of an individual's calling bout is innately limited.     

the effect of pair formation on diel calling patterns in two cricket species,Gryllus veletis andGryllodes sigillatus (Orthoptera: Gryllidae)

After pair formation, male crickets should reduce calling to minimize the risks to males of attracting predators and/or rivals. We tested this hypothesis in two cricket species, one in which males exhibit a high mating propensity (Gryllus veletis)and another in which the mating propensity of males is constrained by the manufacture of elaborate, bipartite spermatophores (Gryllodes sigillatus).Calling durations of male G. veletisdeclined precipitously after the introduction of females but remained unchanged in G. sigillatus.We attribute the asymmetric effect of female proximity on male calling to differences in the mating propensity of males of the two species. Male G. veletisabstain from further calling in favor of repeated matings with the same female. Male G. sigillatusprobably lack the opportunity to mate repeatedly with the same female and, thus, resume calling shortly after mating to increase their probability of attracting additional mates.     

Limited flexibility in female Pacific field cricket (Teleogryllus oceanicus) exploratory behaviors in response to perceived social environment

How populations adapt, or not, to rapid evolution of sexual signals has important implications for population viability, but is difficult to assess due to the paucity of examples of sexual signals evolving in real time. In Hawaiian populations of the Pacific field cricket (Teleogryllus oceanicus), selection from a deadly parasitoid fly has driven the rapid loss of a male acoustic signal, calling song, that females use to locate and evaluate potential mates. In this newly quiet environment where many males are obligately silent, how do phonotactic females find mates? Previous work has shown that the acoustic rearing environment (presence or absence of male calling song) during late juvenile stages and early adulthood exposes adaptive flexibility in locomotor behaviors of males, as well as mating behaviors in both sexes that helps facilitate the spread of silent (flatwing) males. Here, we tested whether females also show acoustically induced plasticity in walking behaviors using laboratory‐reared populations of T. oceanicus from Kauai (HI; >90% flatwings), Oahu (HI; ~50% flatwings), and Mangaia (Cook Islands; no flatwings or parasitoid fly). Though we predicted that females reared without song exposure would increase walking behaviors to facilitate mate localization when song is rare, we discovered that, unlike males, female T. oceanicus showed relatively little plasticity in exploratory behaviors in response to an acoustic rearing environment. Across all three populations, exposure to male calling song during development did not affect latency to begin walking, distance walked, or general activity of female crickets. However, females reared in the absence of song walked slower and showed a marginally non‐significant tendency to walk for longer durations of time in a novel environment than those reared in the presence of song. Overall, plasticity in female walking behaviors appears unlikely to have facilitated sexual signal loss in this species.     

Nocturnal Calling Behavior in Mantids

Females of Mantis religiosa and Empusa pennata were video taped for several 24 h periods to determine if they showed behaviors associated with pheromone release. In the photophase the abdomen of both species was motionless and rested in continuous contact with the wings. However, at the beginning of the scotophase the females bent the abdomen ventrally so that the space between the abdomen and the wings increased significantly with respect to the daytime posture. Calling behavior (abdominal bending) was maintained throughout the 8 h scotophase and ended abruptly at lights on. Females of M. religiosa did not start calling until they were 30 days of age. Calling disappeared in mated females, but it reappeared two weeks later. Males stayed motionless in response to the odors emitted by other males or by noncalling females, but walked when a calling female was placed in the air flow. These observations suggest that female mantids bend their abdomens at night to release a sex pheromone. The adaptive function of nocturnal sex pheromone release in sexually cannibalistic species that rely strongly on visual cues for mating is discussed.     

CALLING SONG DISPLACEMENT IN A ZONE OF OVERLAP AND HYBRIDIZATION

The ground crickets Allonemobius fasciatus and A. socius meet in a mosaic zone of overlap and hybridization stretching from the East Coast to at least Illinois. To test whether male calling song differences were enhanced in sympatry, we analyzed the songs of crickets from inside and outside the zone of overlap along two transects. No evidence of calling song displacement was found in A. socius males from populations within the zone of overlap. On the other hand, A. fasciatus displayed calling song displacement in three populations. Our results are consistent with the hypothesis that the selective pressure exerted by the challenge from a related species is frequency dependent. While not a conclusive demonstration, the observed shifts in calling song are strongly suggestive of reproductive character displacement.     

Acoustic communication in the trilling field cricket,Gryllus rubens (Orthoptera: Gryllidae)

Male field crickets produce calling songs that are used for attracting conspecific females for mating. Acoustic communication was studied in the trilling field cricket, Gryllus rubens.A trilled calling song consists of a continuous train of sound pulses, each of which was repeated at a stereotyped rate. Singing males were recorded at different temperatures. The pulse period of the calling song decreased with increasing temperature; there was less effect of temperature on pulse duration. Female phonotaxis was studied on a noncompensating, spherical treadmill. In two-stimulus (choice) playback experiments, females preferred the conspecific trilled song over the chirped calling song of a sympatric species, Gryllus fultoni.This preference persisted even when the song of G. fultoniwas 6 dB louder. Females also discriminated between synthetic trills having different pulse periods; females chose trills with the conspecific pulse period over trills having lower and higher pulse periods.     

Rearing phonotactic parasitoid flies [Diptera: Tachinidae,ormiini, ormia spp.]

Females of ormiine tachinids fly to their hosts' calling songs and deposit larvae on the host or nearby. Two species,Ormia ochracea (Bigot) andO. depleta (Wiedemann), were reared for at least 8 generations, making them the first ormiines to be laboratory-propagated. Both were reared on natural hosts:Gryllus spp. field crickets (principallyG. rubens) forO. ochracea, andScapteriscus spp. mole crickets forO. depleta. Commercially rearedAcheta domesticus tested as hosts were less satisfactory. Hosts were parasitized manually or by confinement with flies or planidia (infective larvae). Transparent, cylindrical, sleeved cages were designed to accommodate parasitized hosts and pupae and adults ofO. ochracea. Cages were joined to allowO. ochracea to cycle through its stages with minimum handling and care. Parasitized hosts and pupae ofO. depleta were held in containers of damp sand; adults were held in cages developed forO. ochracea. Adults of both species were maintained on applesauce, sugar cubes, powdered milk, and water. The life cycle ofO. ochracea was about 31 days and ofO. depleta about 36 days, with the principal difference being the time required for planidia to complete development. InO. ochracea the adults emerged synchronously but inO. depleta males preceded females. In both species sex ratio was generally I: 1 and females lived slightly longer than males.O. depleta from our laboratory colony have been released for biological control of mole crickets.