Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to tungara frog calls

Mating signals that increase attractiveness of males to femalescan also increase conspicuousness of the signaler to predatorsand parasites. We investigated the acoustic preference of speciesof blood-sucking flies of the genus Corethrella (Diptera: Corethrellidae),which eavesdrop on the sexual advertisement signals of túngarafrogs (Physalaemus pustulosus). Male frogs of this species facultativelyproduce 2 types of mating calls: simple (whines alone) and complex(whines and chucks). We tested the acoustic preference of theflies and their ability to locate their host when the frogsproduce simple or complex calls. The flies exhibited phonotaxisto both types of calls but were preferentially attracted tocomplex calls. We show that acoustic information alone is sufficientfor the flies' accurate localization of calling frogs. Complexcalls, however, were not approached at closer distance or withdecreased landing error (i.e., proportion of landings outsidethe target) than simple calls, suggesting that call structuredoes not influence localization performance. Female túngarafrogs and frog-eating bats (Trachops cirrhosus) also prefercomplex to simple túngara frog calls. Thus, intendedand unintended receivers with different ear morphologies exhibitthe same preference for a specific túngara frog calltype. This result is discussed in the context of the evolutionof call attractiveness in a communication network.     

The mixed-species chorus as public information: tungara frogs eavesdrop on a heterospecific

Multispecies choruses represent a promising but uninvestigatedforum for public information. Although frogs exposed to a potentialpredator call more readily in the presence of conspecific callsthan in their absence, none are known to make comparable useof heterospecific calls. To test for heterospecific eavesdropping,we isolated calling male túngara frogs (Physalaemus pustulosus),presented them with a potential predator, and recorded theirresponses to playbacks of 1 of 4 stimuli: calls of a conspecific,a sympatric heterospecific (Leptodactylus labialis), an allopatriccongener (Physalaemus enesefae), or silence. We found that malescalled more in response to the L. labialis call than to eitherthe silent stimulus or the P. enesefae call. In contrast, theP. enesefae call did not result in significantly more callingthan the silent stimulus. The conspecific call was the mosteffective at promoting calling. The data indicate that túngarafrogs selectively attend to the call of a heterospecific. Wehypothesize that such heterospecific eavesdropping contributesto the emergent behavior of mixed-species choruses.     

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.     

Geographic variation of genetic and behavioral traits in northern and southern tüngara frogs

We use a combination of microsatellite marker analysis and mate-choice behavior experiments to assess patterns of reproductive isolation of the túngara frog Physalaemus pustulosus along a 550-km transect of 25 populations in Costa Rica and Panama. Earlier studies using allozymes and mitochondrial DNA defined two genetic groups of túngara frogs, one ranging from Mexico to northern Costa Rica (northern group), the second ranging from Panama to northern South America (southern group). Our more fine-scale survey also shows that the northern and southern túngara frogs are genetically different and geographically separated by a gap in the distribution in central Pacific Costa Rica. Genetic differences among populations are highly correlated with geographic distances. Temporal call parameters differed among populations as well as between genetic groups. Differences in calls were explained better by geographic distance than by genetic distance. Phonotaxis experiments showed that females preferred calls of males from their own populations over calls of males from other populations in about two-thirds to three-fourths of the contrasts tested. In mating experiments, females and males from the same group and females from the north with males from the south produced nests and tadpoles. In contrast, females from the south did not produce nests or tadpoles with males from the north. Thus, northern and southern túngara frogs have diverged both genetically and bioacoustically. There is evidence for some prezygotic isolation due to differences in mate recognition and fertilization success, but such isolation is hardly complete. Our results support the general observation that significant differences in sexual signals are often not correlated with strong genetic differentiation.     

Estradiol induces sexual behavior in female túngara frogs

Steroid hormones play an important role in regulating vertebrate sexual behavior. In frogs and toads, injections of exogenous gonadotropins, which stimulate steroid hormone production, are often used to induce reproductive behavior, but steroid hormones alone are not always sufficient. To determine which hormonal conditions promote sexual behavior in female túngara frogs, we assessed the effect of hormone manipulation on the probability of phonotaxis behavior toward conspecific calls in post-reproductive females. We injected females with human chorionic gonadotropin (HCG), estradiol, estradiol plus progesterone, saline, or HCG plus fadrozole (an aromatase blocker) and tested their responses to mating calls. We found that injections of HCG, estradiol, and estradiol plus progesterone all increased phonotaxis behavior, whereas injections of saline or HCG plus fadrozole did not. Since injections of estradiol alone were effective at increasing phonotaxis behavior, we concluded that estradiol is sufficient for the expression of phonotaxis behavior. Next, to determine if estradiol-injected females display the same behavioral preferences as naturally breeding females, we compared mating call preferences of naturally breeding females to those of post-reproductive females injected with estradiol. We found that, when injected with estradiol, females show similar call preferences as naturally breeding females, although they were less likely to respond across multiple phonotaxis tests. Overall, our results suggest that estradiol is sufficient for the expression of sexual responses to mating calls in túngara frogs. To our knowledge, ours is the only study to find that estradiol alone is capable of promoting phonotaxis behavior in a frog.     

Fluctuating asymmetries and advertisement call variation in the cricket frog, Acris crepitans

We used an anuran acoustic communication system to test a predictionof the "fluctuating asymmetries/good genes" hypothesis thatfemales prefer more symmetric mates because symmetry indicatesgenetic quality. Mate preferences of female cricket frogs (Acriscrepitans) can be influenced by three call characters: dominantfrequency, numbers of pulses per call, and number of pulse groupsper call. We tested the hypothesis that these preferences resultin females preferring more symmetric males. We measured fluctuatingasymmetries of characters not involved with the communicationsystem (head and tibia), and those involved in signal production(laryngeal characters) and signal reception (aural characters).We determined whether the asymmetries in these characters wererelated to the three variables that enhance call attractiveness.Most of the multiple regression models showed no significantassociation between the fluctuating asymmetries of charactersand any of the calls. The regression of head and tibia fluctuatingasymmetry on pulse number was significant, but partial regressioncoefficients revealed that more pulses were associated witha more symmetric head length and a less symmetric tibia length.Our findings provide little or no support for the fluctuatingasymmetries/good genes hypothesis. We emphasize, however, thatthis hypothesis should not be abandoned based on negative resultsof a single study, but deserves further scrutiny.     

Female preference functions based on call duration in the gray tree frog (Hyla versicolor)

Preference functions, which quantify preference strength relativeto variation in male traits or signals, are central to understandingmechanisms and consequences of female choice. Female tree frogs(Hyla versicolor) choose mates on the basis of advertisementcalls and prefer long calls to short calls. Here we show, intwo experimental designs, that preference strength increasedsignificantly as the difference in call duration was increasedonly if the absolute durations of alternative stimuli were below average. Hence preference strength was a non-linear functionof duration, and females did not base preferences solely onthe percentage difference in duration. In experiments simulatingcostly choice (unequal playback levels), non-linear effectswere more pronounced than in the conventional design (equal playback levels). Repeated estimates of preference strengthusing the unequal-playback design revealed significant among-femalevariation. These patterns of preference suggest that selectionby female choice for males producing calls of average durationover males producing very short calls is stronger than selectionfor males producing very long calls over males producing callsof average duration. Female preferences, especially in tests simulating a potentially costly choice, could reflect differencesin the net benefits to females of mating with males producingcalls of different duration.     

Acoustic Preference of Frog‐Biting Midges (Corethrella spp) Attacking Túngara Frogs in their Natural Habitat

In many animals, males aggregate to produce mating signals that attract conspecific females. These leks, however, also attract eavesdropping predators and parasites lured by the mating signal. This study investigates the acoustic preferences of eavesdroppers attracted to natural choruses in a Neotropical frog, the túngara frog (Engystomops pustulosus). In particular, we examined the responses of frog‐biting midges to natural variation in call properties and signaling rates of males in the chorus. These midges use the mating calls of the frogs to localize them and obtain a blood meal. Although it is known that the midges prefer complex over simple túngara frog calls, it is unclear how these eavesdroppers respond to natural call variation when confronted with multiple males in a chorus. We investigated the acoustic preference of the midges using calling frogs in their natural environment and thus accounted for natural variation in their call properties. We performed field recordings using a sound imaging system to quantify the temporal call properties of males in small choruses. During these recordings, we also collected frog‐biting midges attacking calling males. Our results revealed that, in a given chorus, male frogs calling at higher rates and with higher call complexity attracted a larger number of frog‐biting midges. Call rate was particularly important at increasing the number of midges attracted when males produced calls of lower complexity. Similarly, call complexity increased attractiveness to the midges especially when males produced calls at a low repetition rate. Given that female túngara frogs prefer calls produced at higher repetition rates and higher complexity, this study highlights the challenge faced by signalers when increasing attractiveness of the signal to their intended receivers.     

Simulated Predation Risk Influences Female Choice in Túngara Frogs,Physalaemus pustulosus

While the presence of predators can influence female mate choice, few studies have investigated how females respond to quantitative variation in predation risk. In addition, we know little of how females respond to multiple, independent cues of risk. In this study, we investigated the effects of simulated predation risk on mate choice in túngara frogs, Physalaemus pustulosus, using the advertisement calls of predatory frogs, variation in ambient light, and simulated distance. Females showed aversion to conspecific calls associated with the calls of predators, and females were significantly less likely to travel perceived longer distances while the calls of predatory frogs were broadcast. In both the laboratory and field, females chose among potential mates significantly faster under higher light levels. Female responses to acoustic cues of predation risk were significantly influenced by light level, but decisions about travel distances were not. These results demonstrate that female choice is strongly influenced by perceived predation risk and that females can simultaneously evaluate quantitative variation in different cues of predation risk. The changes in search behavior and mate evaluation we demonstrate indicate that predation plays a strong role in limiting signal evolution and possibly reproductive isolation.     

Neural Activity Patterns in Response to Interspecific and Intraspecific Variation in Mating Calls in the Túngara Frog

Background

During mate choice, individuals must classify potential mates according to species identity and relative attractiveness. In many species, females do so by evaluating variation in the signals produced by males. Male túngara frogs (Physalaemus pustulosus) can produce single note calls (whines) and multi-note calls (whine-chucks). While the whine alone is sufficient for species recognition, females greatly prefer the whine-chuck when given a choice.

Methodology/Principal Findings

To better understand how the brain responds to variation in male mating signals, we mapped neural activity patterns evoked by interspecific and intraspecific variation in mating calls in túngara frogs by measuring expression of egr-1. We predicted that egr-1 responses to conspecific calls would identify brain regions that are potentially important for species recognition and that at least some of those brain regions would vary in their egr-1 responses to mating calls that vary in attractiveness. We measured egr-1 in the auditory brainstem and its forebrain targets and found that conspecific whine-chucks elicited greater egr-1 expression than heterospecific whines in all but three regions. We found no evidence that preferred whine-chuck calls elicited greater egr-1 expression than conspecific whines in any of eleven brain regions examined, in contrast to predictions that mating preferences in túngara frogs emerge from greater responses in the auditory system.

Conclusions

Although selectivity for species-specific signals is apparent throughout the túngara frog brain, further studies are necessary to elucidate how neural activity patterns vary with the attractiveness of conspecific mating calls.     

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.     

How cricket frog females deal with a noisy world: habitat-related differences in auditory tuning

Cricket frogs (Acris crepitans) occupy a variety of acousticallydifferent habitats ranging from pine forest to open grassland.There is geographic variation in their calls and the tuningof their basilar papilla (BP) correlated with habitat. Here,we characterize the spectral content of environmental noisefrom two habitats, one a pine forest (Stengl) and one a grassland(Gill) habitat. We then used rounded exponential filter functionsbased on the mean tuning of auditory fibers in Stengl and Gillfemales to model the BP tuning characteristics of an averagefemale from the two cricket frog populations occupying thosehabitats to compare their ability to filter out environmentalnoise. Noise recordings were made at both sites from 1800 to2400 h on multiple nights throughout a breeding season (Marchthrough early August). Noise spectra were similar at both sites.Cross-correlation analyses of the sampled noise indicated thatnoise spectra were consistent throughout the night and variedlittle over the season other than during the month of May. Themodel auditory filter simulating an average Stengl female wassignificantly better than one simulating an average Gill femaleat filtering environmental noise at both sites. Previous workhad shown that cricket frog calls suffered greater attenuationand degradation in the Stengl site than the Gill site but thatthe male calls from Stengl frogs suffered less attenuation andless degradation than Gill calls during transmission throughboth habitats. These new results demonstrate that frogs fromthe more acoustically challenging Stengl habitat have enhancedboth the sender and receiver portions of their communicationsystem, evolving calls that transmit better and auditory filtersthat better eliminate noise.     

THE SENSORY BASIS OF SEXUAL SELECTION FOR COMPLEX CALLS IN THE TÚNGARA FROG,PHYSALAEMUS PUSTULOSUS (SEXUAL SELECTION FOR SENSORY EXPLOITATION)

Male túngara frogs (Physalaemus pustulosus) vocalize to attract females, and enhance the attractiveness of their simple, whine-only call by adding chucks to produce complex calls. Complex calls contain more total energy and are of longer duration. By virtue of the greater frequency range of the chuck, complex calls also simultaneously stimulate both the amphibian papilla and the basilar papilla of the frog's inner ear. Female phonotaxis experiments using synthetic stimuli demonstrate that an increase in the call's acoustic energy is not sufficient to account for the enhanced attractiveness of the complex call. However, the stimulation of either or both of the female's sound-sensitive inner-ear organs is sufficient to elicit her preference. We suggest that the female's sensory system generates selection that equally favors at least three evolutionary alternatives for enhancing call attractiveness and that historical constraints imposed by the male's morphology determined which of the alternatives was more likely to evolve. These data are consistent with our hypothesis of sensory exploitation, which states that selection favors those traits that elicit greater stimulation from the female's sensory system and which emphasizes the nonadaptive nature of female preference.     

Sound Pattern Recognition in Some North American Treefrogs (Anura: Hylidae): Implications for Mate Choice

SYNOPSIS. Playback experiments using synthetic sounds indicatethat gravid females of the gray treefrogs (Hyla versicolor andH. chrysoscelis) and the green treefrog (H. cinerea) selectivelyrespond to sounds on the basis of physical properties that showinter-individual variation in the calls of conspecific males.Although the specificity is adequate to differentiate amongthe signals of many males, this potential for mate choice maynot be fully realized in acoustically complex situations suchas natural breeding aggregations. Female selectivity in H. cinereawas less precise in four-speaker experiments than in two-speakerexperiments. An analysis of female preferences with respectto a call property correlated with body size was only partiallysuccessful in predicting the size distribution of successfulmales in a natural population. Finally, the existence of othersynchronously breeding species of frogs with similar calls mayimpose significant constraints on intraspecific mate choice,and female specificity with respect to some acoustic propertiesof mating calls is difficult to explain otherwise.     

The vocal sac as a visual cue in anuran communication: an experimental analysis using video playback

Acoustic signals produced by most anurans are accompanied by inflation of a conspicuous vocal sac. We presented female túngara frogs, Physalaemus pustulosus, with acoustic playback of the male advertisement call, synchronized with a video playback of vocal sac inflation. Females significantly preferred a stimulus combination including vocal sac inflation over an identical set of stimuli with the vocal sac inflation removed. Neither a moving rectangle bearing the gross contrast and spatiotemporal properties of the vocal sac inflation sequence, nor the image of a noncalling male significantly enhanced the attractiveness of the acoustic stimulus. Both the form and spatiotemporal properties of the vocal sac thus appear to be salient to females. The results indicate that the vocal sac can serve as a visual cue, which may account for the conspicuous pigmentation found on the vocal sacs of males in many species. Gular inflation in synchrony with a call may function to facilitate female localization of individual males in an aggregation.     

Collective detection in escape responses of temporary groups of Iberian green frogs

When confronted with a predator, prey are often in close proximityto conspecifics. This situation has generated several hypothesesregarding antipredator strategies adopted by individuals withingroups of gregarious species, such as the "risk dilution," "earlydetection," or "collective detection" effects. However, whethershort-term temporary aggregations of nongregarious animals arealso influenced in their escape decisions by nearby conspecificsremains little explored. We simulated predator approaches togreen frogs (Rana perezi) in the field while they were foragingat the edge of water, either alone or spatially aggregated intemporary clusters. "Flight initiation distances" of frogs (i.e.,the distance between the simulated predator and the frog atthe time it jumped) that escaped by jumping into the water wereinfluenced by microhabitat variables (vegetation at the edgeand in water and the initial distance of the frog to the closestwater edge) and also by the responses of nearby individuals.In clusters, risk dilution did not influence the first individualto respond to the predator simulation or the average responseof all frogs in the cluster as the frog's responses were independentof group size. Also, flight initiation distances of individualsthat first responded to the predator within clusters did notdiffer from those of solitary individuals, which is contraryto the predictions of the early detection hypothesis. However,the remaining frogs in the cluster had longer flight initiationdistances than expected from the comparison with solitary individuals.We suggest that this pattern originated because the responseof the first frog within a cluster triggered the sequentialresponse of the remaining frogs in the cluster, which agreeswith the expectations from the collective detection hypothesis.Our findings give insight into an early stage in the evolutionof grouping as they suggest that individual frogs may benefitfrom being part of a cluster, even for short periods of time.     

Arginine Vasotocin Injection Increases Probability of Calling in Cricket Frogs, but Causes Call Changes Characteristic of Less Aggressive Males

Male cricket frogs,Acris crepitanscommunicate to males and females using advertisement calls, which are arranged into call groups. Calls at the middle and end, but not beginning of the call group, are modified in response to male–male aggressive interactions. We found in this field study of male cricket frogs in natural breeding choruses that the peptide hormone arginine vasotocin (AVT) not only increased the probability that males called after injections, but also caused modifications in middle and end calls to produce calls characteristic of less aggressive males. Moreover, AVT-injected males showed significantly greater increases in call dominant frequency than saline-injected males, again, a characteristic of less aggressive males. Cricket frog calls are used to both repel males and attract females, thus call changes may relate to male–male and/or male–female interactions. Saline-injected males also demonstrated significant changes in several call traits, including changes that occurred in the beginning and middle calls of the call groups, but not the end calls. AVT appeared to block some call changes produced through handling. These data suggest that AVT can influence acoustic communication in frogs in several ways, including effects on call characteristics and dominant frequency, as well as potentially blocking some handling effects.     

Acoustical Aspects of the Propagation of Long Calls of Wild <Emphasis Type="Italic">Leontopithecus rosalia</Emphasis>

Golden lion tamarins emit conspicuous and complex long calls. Little is known about the propagation distance of the calls, and the knowledge is important to understand the function of long calls. The high-frequency spectrum of the calls renders them susceptible to substantial degradation inside forest habitats. We investigated 1) the propagation distance of the long call and if the height from the ground affects the degree of degradation and 2) whether long-call acoustic variation affects the propagation distance. We conducted a playback study of 7 2-phrase long calls recorded at different distances (20, 40, 80, 120 m) and heights above ground (2 m and 7.5 m) in 3 transects of Brazilian Atlantic Forest. We quantified the degradation by measuring differences in the number of syllables and frequency measures of the calls at each distance. Degradation became significant at 80 m; the calls degraded below background noise at 120 m. The degradation of syllables was lower for recordings at 7.5 m above ground. The frequency spectra of the calls influenced significantly the propagation distance of the call. Because of the short propagation distance of long calls relative to territory size, we hypothesize that long calls may be adapted to avoiding ambient noise and that they evolved first for intragroup communication and then for territorial defense.     

SPECIES RECOGNITION AND SEXUAL SELECTION AS A UNITARY PROBLEM IN ANIMAL COMMUNICATION

We investigated patterns of mating call preference and mating call recognition by examining phonotaxis of female túngara frogs, Physalaemus pustulosus, in response to conspecific and heterospecific calls. There are four results: females always prefer conspecific calls; most heterospecific calls do not elicit phonotaxis; some heterospecific calls do elicit phonotaxis and thus are effective mate recognition signals; and females prefer conspecific calls to which a component of a heterospecific call has been added to a normal conspecific call. We use these data to illustrate how concepts of species recognition and sexual selection can be understood in a unitary framework by comparing the distribution of signal traits to female preference functions.     

Proximity‐dependent Response to Variably Complex Mating Signals in Túngara Frogs (Physalaemus pustulosus)

The plasticity of animal behavior allows individuals to maximize fitness in a wide range of contexts. Both production of and preference for mating signals are context‐dependent according to internal factors such as hormonal state, and external factors such as predation risk. In many species, male‐to‐female proximity also defines an important context for mating communication. Males often possess short‐distance courtship signals, and females often exhibit distance‐related variation in signal response. Such variation in response may occur when a signal’s relevance changes with male‐to‐female distance, but it may also result from perceptual constraints that are unrelated to fitness. Túngara frogs produce variably complex advertisement calls, and sexual selection theory predicts that females should prefer calls of greater complexity. Preference tests, however, have not demonstrated consistent trends for preference between calls of variable complexity. We tested whether proximity to males influences female response to variable signal complexity and found that both preference and memory for signal complexity are proximity‐dependent.