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 Sounds of Silence as an Alarm Cue in Túngara Frogs,Physalaemus pustulosus

In many species males vocally advertise for mates in choruses and these choruses serve as acoustic beacons to conspecific females as well as to eavesdropping predators and parasites. Chorusing will often cease in response to disturbances, such as the presence of predators. In some cases the cessation is so rapid and over such a large area that it seems improbable that males are all responding directly to the same local disturbance. Here, we demonstrate experimentally in Neotropical túngara frogs, Physalaemus pustulosus, that the cessation of calling by males spreads rapidly through the chorus. The cessation of chorusing in response to the cessation of playbacks of three calling males is more effective in inducing chorus cessation than is the cessation of one male calling. When three males are calling, the cessation of complex calls is more effective in inducing chorus cessation than simple calls. There is no main effect on whether the final call of the male is complete or is interrupted. We thus conclude that the sudden lack of signals—the ‘sounds of silence’—becomes an alarm cue that can explain the rapid cessation of choruses that are common in many chorusing species.     

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.     

Flexibility as a Strategy for Avoiding Call Overlap in Male Anhui Treefrogs

Male-male vocal competition is critical for mating success in anuran species; however, it remains unknown that how males regulate their competitive strategies dynamically during competition because calling is highly time-consuming, energetically demanding and likely to increase predation risks. Since different parts of calls will encode different information for vocal communication, we hypothesized that competitive strategies of male frogs may be modulated by the temporal and spectral features of different call notes. To test this hypothesis, the natural advertisement calls(OC), its modified versions with the first call note replaced by white noise(WN) or other notes and with the fifth call note replaced by WN, were played back to the Anhui tree frogs(Rhacophorus zhoukaiyae). Results showed that 1) males produced more competitive calls in response to acoustic stimuli compared to their baseline calling during silence; and 2) males emitted more non-overlapping calls compared to overlapping calls in response to the acoustic stimuli. These results are consistent with the idea that males are flexible to acoustic signals and their competition strategies are modulated dynamically by social contexts.     

A continental assessment of diurnality in frog calling behaviour

Acoustic signalling is evolutionarily important, influencing sexual selection and serving as a premating isolation mechanism. There is a strong evolutionary basis for acoustic signalling to occur nocturnally across many terrestrial vertebrate groups including mammals, reptiles and amphibians. Within some of these groups, there is a general assumption that ‘most taxa are nocturnal’ in their acoustic signalling, and this is a particularly strongly held view for most frogs. Here we challenge this well-accepted notion by quantifying diurnal calling behaviour in Australian frogs, leveraging a continental-wide citizen science dataset. Of 196 species present in the citizen science dataset, 140 (71%) were recorded at least once during the day. Of the most commonly observed species (i.e. species with at least 150 calls recorded in the database), there were surprisingly high rates of diurnal calling: 14 species had >25% of their calls recorded during the day. We also found that the relative rate of diurnal calling in frogs showed a strong phylogenetic signal, suggesting that the plasticity in calling behaviour as it relates to time of the day is strongly evolutionarily conserved. Our results highlight a suite of ecological and evolutionary questions that are worthy of further investigation.     

Multimodal cues improve prey localization under complex environmental conditions

Predators often eavesdrop on sexual displays of their prey. These displays can provide multimodal cues that aid predators, but the benefits in attending to them should depend on the environmental sensory conditions under which they forage. We assessed whether bats hunting for frogs use multimodal cues to locate their prey and whether their use varies with ambient conditions. We used a robotic set-up mimicking the sexual display of a male túngara frog (Physalaemus pustulosus) to test prey assessment by fringe-lipped bats (Trachops cirrhosus). These predatory bats primarily use sound of the frog''s call to find their prey, but the bats also use echolocation cues returning from the frog''s dynamically moving vocal sac. In the first experiment, we show that multimodal cues affect attack behaviour: bats made narrower flank attack angles on multimodal trials compared with unimodal trials during which they could only rely on the sound of the frog. In the second experiment, we explored the bat''s use of prey cues in an acoustically more complex environment. Túngara frogs often form mixed-species choruses with other frogs, including the hourglass frog (Dendropsophus ebraccatus). Using a multi-speaker set-up, we tested bat approaches and attacks on the robofrog under three different levels of acoustic complexity: no calling D. ebraccatus males, two calling D. ebraccatus males and five D. ebraccatus males. We found that bats are more directional in their approach to the robofrog when more D. ebraccatus males were calling. Thus, bats seemed to benefit more from multimodal cues when confronted with increased levels of acoustic complexity in their foraging environments. Our data have important consequences for our understanding of the evolution of multimodal sexual displays as they reveal how environmental conditions can alter the natural selection pressures acting on them.     

Vocal communication in frogs

The robust nature of vocal communication in frogs has long attracted the attention of natural philosophers and their biologically inclined successors. Each frog species produces distinctive calls that facilitate pre-mating reproductive isolation and thus speciation. In many terrestrial species, a chorus of simultaneously calling males attracts females to breeding sites; reproductive females then choose and locate one male, using distinctive acoustic cues. Males compete with each other vocally and sometimes physically as well. Anuran acoustic signaling systems are thus subject to the strong pressures of sexual selection. We are beginning to understand the ways in which vocal signals are produced and decoded by the nervous system and the roles of neurally active hormones in both processes.     

Parasites and Mate Choice in Gray Treefrogs, Hyla versicolor

A fundamental assumption of the Hamilton and Zuk (1982) modelof sexual selection is that parasite-free males should producemate attracting displays that are substantially more vigorousand effective than those of their parasitized counterparts.Further, the model predicts that parasite-free males shouldbe preferred as mating partners by females and, as a consequence,should have higher reproductive success than their parasitizedcompetitors. Gray treefrogs (Hyla versicolor) constitute anideal species for testing both assumptions and predictions ofthe Hamilton-Zuk model in that: (i) mate attraction by malesrequires the production of energetically costly calls and (ii)males of this species have been shown to harbor a wide rangeof helminth parasites. The present paper summarizes resultsof analyses of calling and mating behavior by male gray treefrogsin relation to their parasite infection levels. In general,these analyses revealed no consistent relationship between thenumber and kinds of parasites harbored by males and either theduration or duty-cycle (a direct measure of energetic cost)of their calls. Furthermore, males found in amplexus (i.e.,males actually selected as mating partners by females) showeda slightly higher prevalence of parasite infection (but a slightlylower intensity of infection) than did a comparable sample ofunmated males. In sum, the present study failed to support themajor within-species prediction of the Hamilton-Zuk model ofsexual selection and also calls into question one of the fundamentalassumptions of the model.     

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.     

Ultra-violet reflectance of male and female red grouse, Lagopus lagopus scoticus, sexual ornaments reflect nematode parasite intensity

In many birds, females prefer males with the biggest or brightest sexual ornaments, which might reflect a higher phenotypic quality, such as fewer parasites. Unlike humans, most birds detect near-ultraviolet (UV) light, and UV signals can play an important role in sexual signalling and mate choice. Using a spectrophotometer, we analysed the colour of red grouse Lagopus lagopus scoticus sexual ornaments (their combs). We first show that combs reflect both in the red (600–700 nm) and UV (300–400 nm) part of the spectrum. Second, we investigated whether comb size and colour, and UV reflectance in particular, reflected an aspect of individual quality: the intensity of infection by a main nematode parasite, the caecal threadworm Trichostrongylus tenuis . We first analysed comb size and colour variation, and parasite intensity variation, in relation to sex and age. Males had bigger and redder combs than females, but UV brightness was greater for female than for male combs. Comb colour also differed between age groups, with young birds of both sexes showing brighter UV than old birds. Young grouse also had fewer T. tenuis worms than old grouse. We further tested whether intensity of infection could be predicted from comb characteristics (size and colour) in male and female red grouse. We found that parasite intensity was not significantly related to comb size or red brightness, but fewer worms were predicted from brighter UV in combs, in both males and females. The results indicate that UV reflectance of combs have a quality revealing function and might play an important role in grouse mate choice: UV brightness of combs could enable both male and female red grouse to assess the parasite loads of a potential mate.     

Sexual Differences in the Behavioral Response of Túngara Frogs, Physalaemus pustulosus, to Cues Associated with Increased Predation Risk

Engaging in mating behaviors usually increases exposure to predators for both males and females. Anti‐predator strategies during reproduction may have important fitness consequences for prey. Previous studies have shown that individuals of several species adjust their reproductive behavior according to their assessment of predation risk, but few studies have explored potential sexual differences in these strategies. In this study, we investigate whether the acoustic cues associated with predatory attacks or those associated with predators themselves affect the mating behavior of female and male túngara frogs, Physalaemus pustulosus. We compared the responses of females approaching a mate and those of calling males when exposed to mating calls associated with sounds representing increased hazard. When presented with mating calls that differed only in whether or not they were followed by a predation‐related sound, females preferentially approached the call without predation‐related sounds. In contrast to females, calling males showed greater vocal response to calls associated with increased risk than to a call by itself. We found significant differences in the responses of females and males to several sounds associated with increased hazard. Females behaved more cautiously than males, suggesting that the sexes balance the risk of predation and the cost of cautious mating strategies differently.     

Males of <Emphasis Type="Italic">Hypsiboas goianus</Emphasis> (Anura; Hylidae) do not assess neighbor fighting ability through acoustic interactions

In frogs, acoustic signals are the most important communication mechanism, since they may be used in several social contexts. In many anurans, the dominant frequency of calls is negatively related to body size, and in such species, this spectral parameter may be considered a good predictor of fighting ability. We experimentally investigated the vocal behavior of 30 male Hypsiboas goianus in central Brazil to answer the following questions: (1) Do males change the acoustic parameters of their calls in response to conspecific intruders? and (2) Does the acoustic behavior of H. goianus depend on the simulated body size of their opponent? We used playback of synthesized calls with high (3573 Hz) and low (3123 Hz) dominant frequency to simulate small and large males, respectively. Males reduced the rate of advertisement calling in response to playback but did not change vocal behavior in response to low-frequency and high-frequency playback. So, while males adjust their calling activity in response to simulated conspecifics, there was no evidence that they assess the fighting ability of their opponents through acoustic interactions.     

Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula)

Many parasites depress the expression of the carotenoid-based colour displays of their hosts, and it has been hypothesized that animals face a trade-off in carotenoid allocation between immune functions and 'degree of ornamentation'. While numerous correlative studies suggest that parasite infection decreases the intensity of carotenoid-based colour displays, the existence of this trade-off has never been demonstrated experimentally in a host-parasite model. In this study, we used the blackbird (Turdus merula) and Isospora (an intestinal parasite) to assess whether this trade-off does indeed exist. Blackbirds were supplemented with carotenoids while simultaneously being exposed to parasites. Supplemented males circulated more carotenoids in the blood and developed more brightly coloured bills than unsupplemented males. In addition, supplementation slowed down the replication rate of parasites. Supplementation with carotenoids enabled infected birds to maintain their bill coloration, whereas birds that were infected but not supplemented showed reduced bill coloration. At the same time, infection slowed carotenoid assimilation in the blood. Overall, we demonstrated that bill colour reflects a bird's health, and that only males with a carotenoid-rich diet are capable of coping with costs associated with parasitic infection. Carotenoids are thus traded off between host physiological response to parasites and secondary sexual traits. Further investigations are required to determine the physiological mechanisms that govern this trade-off.     

Female call preferences in tree-hole frogs: why are there so many unattractive males?

In tree-hole frogs, Metaphrynella sundana, the fundamental call frequency varies widely between males. In field playback experiments, females strongly preferred calls from the lower range of frequencies found in the population. There was no correlation, however, between male size and call frequency, as is normally the case for anurans, so large males were not necessarily more attractive to females. Presence or absence of upper harmonics in the call had no effect on female choice. Tree holes with shallow air columns were more often used by calling frogs, and were presumably more common, than deep holes. Since male M. sundana actively exploit the resonant properties of tree holes for mate attraction, and high frequencies match comparatively shallow holes, the benefits of attaining acoustic matching probably select for high-frequency calls. In addition, males with high-frequency calls may be heard from a greater distance in the vicinity of torrent streams. Since the level of such noise in the forest varies in time and space, different frequencies may prove optimal in different contexts, thereby preserving the observed variation within the population. Having an ‘unattractive’ high-frequency call should be potentially beneficial only when calling males do not congregate, a condition that our data suggest is fulfilled in this system.     

Female Mate Choice Can Drive the Evolution of High Frequency Echolocation in Bats: A Case Study with Rhinolophus mehelyi

Animals employ an array of signals (i.e. visual, acoustic, olfactory) for communication. Natural selection favours signals, receptors, and signalling behaviour that optimise the received signal relative to background noise. When the signal is used for more than one function, antagonisms amongst the different signalling functions may constrain the optimisation of the signal for any one function. Sexual selection through mate choice can strongly modify the effects of natural selection on signalling systems ultimately causing maladaptive signals to evolve. Echolocating bats represent a fascinating group in which to study the evolution of signalling systems as unlike bird songs or frog calls, echolocation has a dual role in foraging and communication. The function of bat echolocation is to generate echoes that the calling bat uses for orientation and food detection with call characteristics being directly related to the exploitation of particular ecological niches. Therefore, it is commonly assumed that echolocation has been shaped by ecology via natural selection. Here we demonstrate for the first time using a novel combined behavioural, ecological and genetic approach that in a bat species, Rhinolophus mehelyi: (1) echolocation peak frequency is an honest signal of body size; (2) females preferentially select males with high frequency calls during the mating season; (3) high frequency males sire more off-spring, providing evidence that echolocation calls may play a role in female mate choice. Our data refute the sole role of ecology in the evolution of echolocation and highlight the antagonistic interplay between natural and sexual selection in shaping acoustic signals.     

Frogs Have Rules: Selective Attention Algorithms Regulate Chorusing in Physalaemus pustulosus (Leptodactylidae)

In various acoustic insects and frogs, females preferentially orient towards the leading of two or more males' advertisement signals that occur closely in time. Such preferences in receivers have apparently selected for timing mechanisms whereby male signallers actively refrain from calling immediately following the onset of a neighbour's call and thereby increase their production of leading calls. However, indiscriminate application of this inhibitory mechanism to all neighbours might severely reduce a male's calling rate, particularly in high density. Consequently, mechanisms of selective attention to only a subset of signalling neighbours are expected.
Female Túngara frogs ( Physalaemus pustulosus ) exhibit strong preferences for leading male calls, and males refrain from calling immediately following a neighbour. Four-loudspeaker playback experiments demonstrated that males do selectively apply this inhibitory mechanism to only a subset of close signalling neighbours. Selective attention is regulated by a combination of sliding threshold and fixed number rules: (i) Attend to the loudest (nearest) conspecific neighbour and those additional ones whose calls are within 6–8 dB of the loudest one; (ii) attend to only two neighbours in total when the calls are weak or the second one is much farther than the first; (iii) attend to three neighbours when the calls are loud or all neighbours are approximately equidistant. The means by which such plasticity may be achieved and its potential adaptiveness are discussed.     

Social Context Influences Androgenic Effects on Calling in the Green Treefrog (Hyla cinerea)

Courtship behavior in frogs is an ideal model for investigating the relationships among social experience, gonadal steroids, and behavior. Reception of mating calls causes an increase in androgen levels in listening males, and calling, in turn, depends on the presence of androgens. However, previous studies found that androgen replacement does not always restore calling to intact levels, and the relationship between androgens and calling may be context dependent. We examined the influence of androgens on calling behavior in the presence and the absence of social signals in male green treefrogs (Hyla cinerea). We categorized calling during an acoustic stimulus (mating chorus or tones) as evoked and calling in the absence of a stimulus as spontaneous. Intact males received a cholesterol implant, castrated males were castrated and received a cholesterol implant, and T-implanted males were castrated and received a testosterone implant. The androgen levels (mean +/- SE ng/ml of plasma) achieved by the implants were as follows: castrated males, 1.2 +/- 0.2; intact males 21.9 +/- 7.0; T-implanted males, 254.6 +/- 39.5. As in other frogs, calling depends on the presence of androgens, as castration abolished and T replacement maintained calling. However, among intact and T-implanted males, the influence of androgens on calling differed between spontaneous and evoked calling. There was a positive effect of androgen treatment on spontaneous call rate and a positive correlation between spontaneous call rate and androgen levels. The influence of androgen levels on evoked call rate was more complex and interacted with acoustic treatment. Surprisingly, T implants suppressed the chorus-specific increase in calling that is evident in intact males. In addition, in response to the chorus, T-implanted males called less than did intact males, in spite of higher androgen levels. Furthermore, variation in androgens did not explain variation in evoked call rate. These data indicate that androgens influence the motivation to call, but that, when socially stimulated, androgens are necessary but insufficient for calling.     

Effect of sexual segregation on host-parasite interaction: Model simulation for abomasal parasite dynamics in alpine ibex (Capraibex)

We investigated whether sexual segregation might affect parasite transmission and host dynamics, hypothesising that if males are the more heavily infected sex and more responsible for the transmission of parasite infections, female avoidance of males and the space they occupy could reduce infection rates. A mathematical model, simulating the interaction between abomasal parasites and a hypothetical alpine ibex (Capraibex) host population composed of its two sexes, was developed to predict the effect of different degrees of sexual segregation on parasite intensity and on host abundance. The results showed that when females tended to be segregated from males, and males were distributed randomly across space, the impact of parasites was the lowest, resulting in the highest host abundance, with each sex having the lowest parasite intensity. The predicted condition that minimises the impact of parasites in our model was the one closest to that observed in nature where females actively seek out the more segregated sites while males are less selective in their ranging behaviour. The overlapping of field observation with the predicted optimal strategy lends support to our idea that there might be a connection between parasite transmission and sexual segregation. Our simulations provide the biological boundaries of host-parasite interaction needed to determine a parasite-mediated effect on sexual segregation and a formalised null hypothesis against which to test future field experiments.     

Hearing is not necessarily believing in nocturnal anurans

The recent discovery of the use of visual cues for mate choice by nocturnal acoustic species raises the important, and to date unaddressed, question of how these signals affect the outcome of mate choice predicted by female preference for male calls. In order to address this question, we presented female Hyla arborea tree frogs with a series of choices between combinations of acoustic and visual cues of varying quality in nocturnal conditions. While females exhibited the expected preference for a combination of attractive values for visual and acoustic signals over combinations of unattractive values for both signals, when presented with conflicting acoustic and visual cues, they equally adopted one of two strategies, preferring either attractive calls or intense vocal sac coloration. This constitutes novel evidence that the outcome of mate choice, as predicted on the basis of male calling quality, can be drastically different when additional communication modalities—in this case vision—are taken into account. These results also highlight the possible existence of individual variation in female rules for cue prioritization. The implications of these results for the study of mate choice in nocturnal acoustic species are discussed.     

Call differences and calling site segregation in anuran species from central Amazonian floating meadows

Summary The acoustic behaviour of 15 sympatric and synchronically breeding species of frogs in an area of floating meadows near Manaus (Brazil) was studied for a period of 8 months. The calling positions of each species can be identified with certain physiognomic types of vegetation.Sound analyses were used to compare the mating calls. The main variables are dominant frequency, call duration and pulse repetition rate. Each of the 15 species has a distinct mating call and differs from the acoustic behaviour of each other one. Eleven species are separated in their dominant frequency ranges within their specific calling sites. Species sharing emphasised frequency ranges within identical calling sites differ greatly in at least two temporal variables.The roles of calling position, spectral, and temporal features of mating calls in species recognition and premating reproductive isolation are discussed.