Talking Back: Sending Soil Vibration Signals to Lekking Prairie Mole Cricket Males

The male prairie mole cricket, Gryllotalpa major, native ofthe tallgrass prairie of the south central U.S., constructsa specialized acoustical burrow in the spring in the prairiesoil from which he generates an airborne calling song that attractsflying females for mating. Males do not phonorespond to manipulationsinvolving playbacks of airborne sounds. At the same time, vibrationswith the same temporal scale and pattern as the airborne signalare produced in the substrate through an unknown mechanism.These ground vibrations can be distinguished from backgroundvibrations in the soil at distances up to 3 m depending on soilconditions and conditions that control the background vibrationenvironment (e.g., wind, highway traffic). We hypothesize thatmales use the vibration component of the call as informationfor spacing as they form display arenas, or leks. We used modifiedfield recordings of soil vibrations from singing males withan electromechanical vibration exciter to simulate the vibrationcomponent of a calling song in playback experiments. Airbornesounds of males were monitored for two minutes before and twominutes after the introduction of the ground vibration stimuluswith a tape recorder microphone placed 20 cm from the burrowopening. Males did respond to the manipulation experiment; although,we observed individual variation in the level of response.     

Reduced reproductive effort in male field crickets infested with parasitoid fly larvae

Some populations of the field cricket Teleogryllus oceanicusare parasitized by the phonotactic fly Ormia ochracea. Flieslocate crickets by their song and deposit larvae onto them.The larvae develop inside the cricket for 1 week before killingthe host upon emergence. The reproductive compensation hypothesispredicts that parasitized crickets should increase their reproductiveeffort during the initial stages of infestation to offset theloss of fitness resulting from their shortened life span. An alternative hypothesis predicts that parasitized crickets willdecrease reproduction, either because they are unable to reproduceor because selection acting on the parasitoid favors decreasedhost reproduction. In laboratory experiments, parasitized malecrickets had reduced reproductive effort (spermatophore production,calling, mating activity, and mass allocated to reproductivetissue) compared to unparasitized males. Parasitized males fedad libitum showed no evidence of allocating a greater proportionof their resources to reproduction. Parasitized and healthymales did not differ significantly in resting or maximal metabolicrates, although this may have been due to the substantial contributionof larval respiration to the metabolic rate of the host—parasitoidcomplex. These results are consistent with previous studiesand suggest that T. oceanicus males parasitized by O. ochraceado not increase their reproductive effort. We discuss potentialreasons that crickets do not increase reproductive effort inresponse to fly larvae and address difficulties in demonstratingaltered life-history patterns in response to parasitism.     

Are Centrally Displaying Males Always the Centre of Female Attention? Acoustic Display Position and Female Choice in a Lek Mating Subterranean Insect

Several conceptual models seek to explain patterns of male display and factors that influence female mate choice in lek mating systems. The central advantage model predicts that males displaying at or near the lek centre should be more attractive to females than are males positioned along the lek periphery. Females may exhibit biases toward these centrally displaying males based on either spatial or display‐related cues. We tested the prediction of the central advantage model in investigating the importance of male display position in the subterranean and lek mating prairie mole cricket (Gryllotalpa major). Gryllotalpa major males form mating aggregations in the early spring and produce an acoustic advertisement signal from a constructed calling chamber at the soil surface. Pair formation occurs in the calling chamber, and males typically maintain these structures for the duration of the reproductive season. To assess whether G. major females exhibit a preference for males calling from centrally located acoustic burrows, we documented the spatial position and number of female attractions for all advertising males across the focal lek. Six spatial attributes related to display position were reduced using principal component analysis and examined for an association with male attractiveness. We found that in general, female attractions were distributed randomly across the lek; male attractiveness was not related to proximity to the lek centre nor to any factor associated with display position. The most highly attractive males, however, were located further from the lek centre and from nearest calling neighbours than other attractive males. Advertising males that segregate themselves within the aggregation and locate nearer the lek margin may gain a geometric advantage resulting in the increased probability of attracting a searching female.     

Lekking in Gryllotalpa major, the Prairie Mole Cricket (Insecta: Gryllotalpidae)

Gryllotalpa major is a rare, burrowing insect native to the tallgrass prairie of the south-central United States and is known to exhibit 'lek-like' behavior during mating. Here I report on a study carried out in the field that demonstrates that the prairie mole cricket meets all criteria defining a classical lekking species. Males construct specialized acoustic burrows from which they call to attract females for mating. I show that these burrows, which seem to serve no purpose other than for sexual advertisement and mating, are aggregated spatially on at least three scalar levels. Females fly through the aggregation of burrows and drop to the ground in the vicinity of calling males, and are, thus, not constrained in choosing a mate. Females enter the males' acoustic burrows, but I argue that the burrows are not used as oviposition sites, and that the males do not otherwise sequester resources important to females. Although the term 'lek' is useful for the discussion of mating systems, its definition remains ambiguous. I discuss the current usage of the term and suggest extensions.     

Sexual signaling and immune function in the black field cricket Teleogryllus commodus

The immunocompetence handicap hypothesis predicts that male sexual trait expression should be positively correlated with immunocompetence. Here we investigate if immune function in the cricket, Teleogryllus commodus, is related to specific individual components of male sexual signals, as well as to certain multivariate combinations of these components that females most strongly prefer. Male T. commodus produce both advertisement and courtship calls prior to mating. We measured fine-scale structural parameters of both call types and also recorded nightly advertisement calling effort. We then measured two standard indices of immune function: lysozyme-like activity of the haemolymph and haemocyte counts. We found a weak, positive relationship between advertisement calling effort and lysozyme-like activity. There was, however, little evidence that individual structural call components or the net multivariate attractiveness of either call type signalled immune function. The relationships between immunity and sexual signaling did not differ between inbred and outbred males. Our data suggest that it is unlikely that females assess overall male immune function using male calls.     

Spatio-Temporal Dynamics of Field Cricket Calling Behaviour: Implications for Female Mate Search and Mate Choice

Amount of calling activity (calling effort) is a strong determinant of male mating success in species such as orthopterans and anurans that use acoustic communication in the context of mating behaviour. While many studies in crickets have investigated the determinants of calling effort, patterns of variability in male calling effort in natural choruses remain largely unexplored. Within-individual variability in calling activity across multiple nights of calling can influence female mate search and mate choice strategies. Moreover, calling site fidelity across multiple nights of calling can also affect the female mate sampling strategy. We therefore investigated the spatio-temporal dynamics of acoustic signaling behaviour in a wild population of the field cricket species Plebeiogryllus guttiventris. We first studied the consistency of calling activity by quantifying variation in male calling effort across multiple nights of calling using repeatability analysis. Callers were inconsistent in their calling effort across nights and did not optimize nightly calling effort to increase their total number of nights spent calling. We also estimated calling site fidelity of males across multiple nights by quantifying movement of callers. Callers frequently changed their calling sites across calling nights with substantial displacement but without any significant directionality. Finally, we investigated trade-offs between within-night calling effort and energetically expensive calling song features such as call intensity and chirp rate. Calling effort was not correlated with any of the calling song features, suggesting that energetically expensive song features do not constrain male calling effort. The two key features of signaling behaviour, calling effort and call intensity, which determine the duration and spatial coverage of the sexual signal, are therefore uncorrelated and function independently.     

In situ measurement of calling metabolic rate in an Australian mole cricket, Gryllotalpa monanka

Examination of the energetics of sound production usually requires measurement of species that will produce normal calls under unnatural circumstances. Such measurements are potentially compromised by stress-related changes in calling input (through a reduction in calling effort) or output (through forced use of sub-optimal singing burrows). To determine if such measurements are indeed affected by abstraction from a natural setting, we measured the energetics of song production in undisturbed mole crickets Gryllotalpa monanka and employed a new approach where the animal's singing chamber replaces the respirometry chamber normally used in studies of this type. It was therefore possible to measure metabolic rate (MR) of calling crickets in situ for animals within self-constructed burrows under natural conditions. Calling MR measured under these conditions averaged 13.5-fold higher than standard MR and 2.2-fold higher than MR measured during burrowing in the lab. The calling MR of G. monanka was similar to that measured for other calling insects, and to endothermic insects, but was only 10% of that allometrically predicted for a similarly sized insect (0.89 g) during flight. A male mole cricket is estimated to consume 5.9 ml of oxygen during construction of a calling burrow and a 1-h calling bout; by comparison, a flying female would consume a similar volume in less than 6 min.     

In situ measurement of calling metabolic rate in an Australian mole cricket, Gryllotalpa monanka.

Examination of the energetics of sound production usually requires measurement of species that will produce normal calls under unnatural circumstances. Such measurements are potentially compromised by stress-related changes in calling input (through a reduction in calling effort) or output (through forced use of sub-optimal singing burrows). To determine if such measurements are indeed affected by abstraction from a natural setting, we measured the energetics of song production in undisturbed mole crickets Gryllotalpa monanka and employed a new approach where the animal's singing chamber replaces the respirometry chamber normally used in studies of this type. It was therefore possible to measure metabolic rate (MR) of calling crickets in situ for animals within self-constructed burrows under natural conditions. Calling MR measured under these conditions averaged 13.5-fold higher than standard MR and 2.2-fold higher than MR measured during burrowing in the lab. The calling MR of G. monanka was similar to that measured for other calling insects, and to endothermic insects, but was only 10% of that allometrically predicted for a similarly sized insect (0.89 g) during flight. A male mole cricket is estimated to consume 5.9 ml of oxygen during construction of a calling burrow and a 1-h calling bout; by comparison, a flying female would consume a similar volume in less than 6 min.     

Death comes suddenly to the unprepared: singing crickets, call fragmentation, and parasitoid flies

Male field crickets are subject to a delicate dilemma becausetheir songs simultaneously attract mates and acoustic predators.It has been suggested that in response, crickets have modifiedvarious temporal song parameters to become less attractiveto acoustic predators. We investigated whether crickets withchirping (versus trilling) song structures are less likely toattract acoustically orienting parasitoid flies. Experimentally,we evaluated the phonotactic quest of the parasitoid fly Ormiaochracea in response to broadcast cricket calls, presentedboth simultaneously (choice paradigm) and sequentially (no-choiceparadigm). Flight trajectories were recorded in darkness usingthree-dimensional active infrared video tracking. The flies showed remarkable phonotactic accuracy by landing directly onthe loudspeaker. The introduction of acoustic fragmentationthat resembles calls of many chirping crickets altered theflies' phonotactic accuracy only slightly. Our results documentdifferential attraction between trilling and chirping cricket songs and quantitatively demonstrate that chirping songs, ifpresented alone, do not impair the efficiency (temporal investmentand landing accuracy) of the flies' phonotactic quest. Thisstudy shows that song fragmentation is no safeguard againstacoustic parasitism. We conclude that, in general, a cricket may reduce predation only if its neighbors are acousticallymore conspicuous, chiefly by amplitude.     

Responses of male cricket frogs (Acris crepitans) to attenuated and degraded advertisement calls

We examined the vocal and non‐vocal responses of male cricket frogs (Acris crepitans) to conspecific advertisement calls that had been attenuated or degraded by reducing the depth of amplitude modulation (AM). Both are characteristic of changes to the call as it is transmitted through natural habitats. As stimulus calls became more intense or less degraded, male cricket frogs gradually decreased their call rate and increased the number of call groups and pulse groups in their calls, changes indicative of increased aggressive interactions. At the higher intensities and lower degradation levels, the probability that males would shift to one of two non‐vocal behavioral responses, attacking the perceived intruder or ceasing calling and abandoning the call site, gradually increased. The results show that differences in signal attenuation and AM degradation levels are perceived by males and trigger both vocal and non‐vocal behavioral responses consistent with their use in evaluating the distance to a challenging male. Furthermore, the results indicate that the male responses are graded, increasing as intensity rises and degradation falls, and hierarchical, with vocal responses preceding behavioral responses over the range of intensities and degradation levels presented.     

Entomopathogenic fungi detection and avoidance by mole crickets (Orthoptera: Gryllotalpidae)

A chamber to monitor mole cricket behavior was designed using two different soil-filled containers and photosensors constructed from infrared emitters and detectors. Mole crickets (Scapteriscus spp.) were introduced into a center tube that allowed them to choose whether to enter and tunnel in untreated soil or soil treated with Beauveria bassiana (Balsamo) Vuillemin. Each time the cricket passed through the photosensor located near the entrance of soil-filled containers, the infrared light was blocked and the exact moment that this occurred was logged onto a computer using custom-written software. Data examined included the first photosensor trigger, total number of sensor triggers, presence of tunneling, and final location of the cricket after 18 h. These behaviors were analyzed to discern differences in mole cricket behavior in the presence of different treatments and to elucidate the mechanism that mole crickets use to detect fungal pathogens. The first study examined substrate selection and tunneling behavior of the southern mole cricket, Scapteriscus borellii Giglio-Tos, to the presence of five strains of B. bassiana relative to a control. There were no differences between the first sensor trigger and total number of triggers, indicating the mole crickets are not capable of detecting B. bassiana at a distance of 8 cm. Changes in mole cricket tunneling and residence time in treated soil occurred for some strains of B. bassiana but not others. One of the strains associated with behavioral changes in the southern mole cricket was used in a second experiment testing behavioral responses of the tawny mole cricket, S. vicinus Scudder. In addition to the formulated product of this strain, the two separate components of that product (conidia and carrier) and bifenthrin, an insecticide commonly used to control mole crickets, were tested. There were no differences in mole cricket behavior between treatments in this study. The differences in behavioral responses between the two species could suggest a more sensitive chemosensory recognition system for southern mole crickets.     

Do Male White-Lipped Frogs Use Seismic Signals for Intraspecific Communication?

Modern frogs and toads possess a structurally unique saccule,endowing them with seismic sensitivity greater than that observedso far in any other group of terrestrial vertebrates. In synchronywith their advertisement calls, approximately half of the callingmales of one frog species, the Puerto-Rican white-lipped frog(Leptodactylus albilabris), produce impulsive seismic signals(thumps). The spectral distribution of power in these seismicsignals matches precisely the spectral sensitivity of the frog'ssaccule. The signals have sufficient amplitude to be sensedeasily by the frog's saccule up to several meters from the source—wellbeyond the typical spacing when these frogs are calling in agroup. This circumstantial evidence suggests that white-lippedfrogs may use the seismic channel in intraspecific communication,possibly as an alternative to the airborne channel, which oftenis cluttered with noise and interference. Using the frog's vocalizationsas our assay, we set out to test that proposition. In responseto playback calls, the male white-lipped frog adjusts severalof its own calling parameters. The most conspicuous of theseinvolves call timing—specifically the tendency for a gapin the distribution of call onsets, precisely timed with respectto the onsets of the playback calls. When the airborne componentis unavailable (e.g., masked by noise), approximately one infive animals produces the calling gap in response to the seismicsignals alone.     

Temporal and spatial dynamics in a northern tallgrass prairie

It is well established that plants and soil properties are interdependent. What is less known is the degree to which the distribution of plant and soil properties, in both space and time, match one another. We assessed plant community and soil conditions in permanent sample plots in a tallgrass prairie community from 2002 to 2008. Redundancy analysis showed that the dominant grass species were associated with changes in elevation, soil pH, and gravimetric water content, but not nitrogen or phosphate. Indicator species analysis suggested the community is best described by four cluster types, with half of the plots changing community type over the 6-year sampling period. These cluster types were generally spatially aggregated, with semivariograms showing a range from 80 to 346 m. This degree of spatial structuring was observed in the elevation and soil water content data, but not in measures of soil inorganic N or P. This suggests that natural plant communities do not necessarily show a strong correspondence to all soil variables, especially those that vary rapidly in time and space. The dynamic nature of vegetation patch distribution, combined with their size, may contribute to the loss of species from small tallgrass prairie reserves.     

Variation in plant responses to neighbors at local and regional scales

Differences in the responses of plant species to neighbors may determine their distribution among contrasting environments, but no studies have compared variation in competitive or facilitative abilities both within and among environments. We determined whether the responses of plants to interspecific interactions varied at large scales (between environments) and small scales (among sites within an environment) across a tree line. We separated the effects of above- and belowground interactions on seedlings of grasses and trees grown in prairie or forest using vegetation removals at several sites. Species interactions generally had no significant effect on transplant survival. Competition reduced seedling growth by about 33%-89% in both prairie and forest environments. Despite the strong suppression of growth by neighbors, environment and species effects contributed more to variation in transplant performance than did neighbor removals. Responses to neighbors varied among transplant species but generally did not vary significantly between environments or among sites. With vegetation removed, grasses grew significantly faster in prairie and trees grew faster in forest. Thus, in the absence of neighbors, species showed distinct preferences for the environment in which they are most abundant. In summary, the responses of grasses and woody species to neighbors did not vary significantly at either large (between environments) or small (among sites) scales. These results suggest that species responses to interspecific interactions do not vary strongly with environment or smaller-scale site effects.     

Baffling: a condition-dependent alternative mate attraction strategy using self-made tools in tree crickets

Intense sexual selection in the form of mate choice can facilitate the evolution of different alternative reproductive strategies, which can be condition-dependent. Tree cricket males produce long-distance acoustic signals which are used by conspecific females for mate localization and mate choice. Our study shows that baffling, an acoustic call amplification strategy employed by male tree crickets using self-made tools, is a classic example of a condition-dependent alternative strategy. We show that though most males can baffle, less preferred males, such as smaller and lower-amplitude callers, predominantly use this alternative strategy. Baffling allows these males to increase their call amplitude and advertisement range, which attracts a higher number of females. Baffling also gives these males a mating benefit because females mate for longer durations with them. Our results suggest that the advantage of baffling in terms of gain in the number of sperm cells transferred while mating is primarily limited to less preferred males, thus maintaining the polymorphism of calling strategies in the population. We summarize that baffling is a condition-dependent strategy used by less preferred tree cricket males to obtain mating benefits.     

Individual, nightly, and seasonal variation in calling behavior of the gray tree frog, Hyla versicolor: implications for energy expenditure

We investigated individual, nightly, and seasonal variationin calling behavior of a population of gray tree frogs (Hylaversicolor) from Connecticut, USA. Repeated recordings of individualmales on seven nights revealed significant differences amongmales in calling rate on all but one night and differences innumber of pulses per call and number of pulses produced perhour (pulse effort) on four nights. Most males reduced callingactivity late at night (after 2230 h), but some maintained arelatively steady rate of call production before dropping outof the chorus. Data collected for 26 individuals recorded onthree or more nights throughout the breeding season revealedsignificant differences among males in calling rate, numberof pulses per call, and pulse effort, but repeatabilities forall three variables were low (0.17, 0.35, and 0.12, respectively).The highest repeatability was for number of pulses per call,a variable strongly influenced by proximity to calling neighbors,probably because males often interacted with neighbors at similardistances on several successive nights. Males tended to reducethe number of pulses per call as the season progressed and thedistance between neighbors decreased, but they showed no clearseasonal change in calling rate or pulse effort. There was asubstantial seasonal decline in the number of hours of chorusactivity, resulting in a median decrease of 43% in nightly energyexpenditure by calling males.     

Temporal call changes and prior experience affect graded signalling in the cricket frog

We investigated how male cricket frogs Acris crepitans, alter their advertisement calls in response to broadcasts of synthetic calls that were either 'attractive' or 'aggressive'. The stimulus calls differed in temporal but not spectral characteristics. Male cricket frogs produced a more aggressive call when presented with the aggressive stimulus, indicating that they perceived the temporal differences between the two call categories. The direction and degree of temporal and spectral changes depended on the relative dominant frequency of the resident and opponent. If the resident's dominant frequency was initially higher than the stimulus frequency, the pattern of change in dominant frequency mirrored that seen for the temporal call characters. In contrast, if the resident's initial dominant frequency was below that of the stimulus, then the temporal and spectral changes were in opposite directions. Furthermore, stimulus order influenced whether males responded differently to playbacks of aggressive and attractive calls; males that received the aggressive call first produced more aggressive calls during the aggressive stimulus, while males that received the attractive call first produced similar calls in response to the two stimuli. This suggests that experience with different types of signals influences the subsequent calling behaviour of male cricket frogs. Copyright 1999 The Association for the Study of Animal Behaviour.     

Trade-off in short- and long-distance communication in tungara (Physalaemus pustulosus) and cricket (Acris crepitans) frogs

Female phonotaxis in túngara (Physalaemus pustulosus)and cricket (Acris crepitans) frogs is biased toward male advertisementcalls or call components of lower frequency. This behavioralbias might result in part from a mismatch between the spectralcharacteristics of the advertisement call and the most sensitive frequencyof the peripheral end organ implicated in reception of thesesounds. In both species, females are tuned to frequencies lowerthan average for the calls in their population. This mismatch,however, represents the situation during short-distance communication.Female frogs can also use the call to detect choruses at longdistances, and the spectral distribution of call energy canvary with transmission distance. We used computer simulationsto test the hypothesis that there is a better match betweentuning and call spectral energy at long distances from the callingmale than at short distances by comparing the performance (soundenergy received) of the natural tuning curve relative to anoptimal tuning curve (i.e., one centered at the call's dominantfrequency). The relative performance of the natural tuning curveincreased with distance in túngara frogs. For the twosubspecies of cricket frogs, however, the relative performancedecreased at longer distances. The performance did not equalthe optimal tuning curve at the distances tested. The resultsindicate that the relationship between calls and auditory tuningcannot be optimal for both long and short distance reception.The relationship between female tuning and call dominant frequencymay represent a compromise between short and long distance communication,and the bias toward short or long distances may vary among species.     

The juvenile social environment introduces variation in the choice and expression of sexually selected traits

The juvenile environment provides numerous cues of the intensity of competition and the availability of mates in the near environment. As research demonstrates that the developing individuals can use these cues to alter their developmental trajectories, and therefore, adult phenotypes, we examined whether social cues available during development can affect the expression and the preference of sexually selected traits. To examine this, we used the Australian black field cricket (Telogryllus commodus), a species where condition at maturity is known to affect both male calling effort and female choice. We mimicked different social environments by rearing juveniles in two different densities crossed with three different calling environments. We demonstrate that the social environment affected female response speed but not preference, and male age-specific calling effort (especially the rate of senescence in calling effort) but not the structural/temporal parameters of calls. These results demonstrate that the social environment can introduce variation in sexually selected traits by modifying the behavioral components of male production and female choice, suggesting that the social environment may be an overlooked source of phenotypic variation. We discuss the plasticity of trait expression and preference in reference to estimations of male quality and the concept of condition dependence.     

Landscape and weather determinants of prey availability: implications for the Lesser Kestrel Falco naumanni

Spatial and temporal variation in prey abundance have been shown to impact the time of breeding and breeding success of birds. Understanding the ecological requirements of preferred prey can help develop management measures to improve food supply for target species. For the colonial Lesser Kestrel Falco naumanni, mole crickets Gryllotalpa spp. are one of the most important prey items during the mate‐feeding period. Lesser Kestrel colonies with higher mole cricket consumption had earlier egg‐laying dates, suggesting that differences between individuals in the time of breeding could be caused by differences in the diet. Moreover, the mean number of mole crickets in pellets was significantly correlated with clutch size (in one of the studied years) and egg volume. Thus, the impact of environmental variables and land use on mole crickets is likely to be relevant to Lesser Kestrel conservation. Weekly consumption of mole crickets was higher following an increase in either precipitation or minimum temperature values. Furthermore, mole cricket consumption was higher in colonies surrounded by higher quality soils and in wetter areas and years. Predicted probability of mole cricket occurrence in surveyed watercourse margins suggested a positive relationship between soil penetrability and mole cricket occurrence. Among variables that might be the target of management, the presence of riparian vegetation positively influenced the occurrence of mole crickets, whilst tillage and sowing of streambeds were revealed as the most important threats. We suggest that the maintenance of native vegetation in the margins of watercourses could improve soil resilience to erosion, increase water retention, soil penetrability and fertility, and provide a food supply and shelter for mole crickets. Overall, the implementation of such recommendations is likely to benefit other farmland species known to consume mole crickets, including several endangered species.