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.     

The sound of a blood meal: Acoustic ecology of frog‐biting midges (Corethrella) in lowland Pacific Costa Rica

Animal communication systems are often exploited by eavesdropping antagonists, especially predators and ectoparasites. Female frog‐biting midges (Diptera: Corethrellidae) are known to use male anuran advertisement calls to locate their blood hosts, frogs. Here, we use acoustic midge traps broadcasting synthetic and recorded calls to identify those frog call parameters that affect midge attraction. At our study site in Pacific lowland Costa Rica, we found that overall midge attraction was influenced by both spectral and temporal acoustic parameters. Low dominant frequencies (below 1 kHz) and short pulse durations (between 125 and 500 ms) attracted the highest numbers of midges in tests with synthetic sinusoidal pure tones. These preferences partially explained the relative attractiveness of the advertisement calls of ten local frog species. The advertisement calls of the common and widespread Giant Bullfrog, Leptodactylus savagei (Anura: Leptodactylidae), attracted by far the largest number of midges, suggesting that this frog species might be a key resource for frog‐biting midges in Costa Rica. Although we found that calls of different frog species attracted different midge species/morphospecies in statistically different proportions, acoustic niche differentiation among midge species appeared to be moderate, suggesting either a limited degree of host specialization or the use of additional short‐range, that is, chemical, host recognition cues.     

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.     

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.     

Incidental invertebrate-derived DNA detection of invasive and threatened species in temperate dry Southeast Australian forest

Well-informed biodiversity conservation practice can often be precluded by poor species detectability. For example, populations being missed during surveys can lead to them being omitted from species lists or area management plans. iDNA (invertebrate-derived DNA) is a recently developed set of techniques for improving the detectability of elusive vertebrates by exploiting their associated invertebrates. Parasitic and scavenging invertebrates can be readily collected, and their gut contents DNA barcoded to detect local vertebrate diversity. However, most iDNA surveys have targeted mammals and have been carried out in tropical areas and/or rainforests. We carried out iDNA surveys targeting frogs in temperate dry sclerophyll forests in south-eastern Australia. We set mosquito traps broadcasting recorded frog calls with the aim of collecting frog-biting flies, which are attracted to frog calls. We collected 156 fly specimens, although none were of frog-biting species, and no frogs were detected via iDNA, despite many being observed in the field. However, two mammal and one reptile species were detected via iDNA: the feral cat (Felis catus: Felidae), domestic dog or dingo (Canis lupus: Canidae) and the threatened Rosenberg's monitor (Varanus rosenbergi: Varanidae). Vertebrate-sampling flies are likely highly abundant in the area since they were collected apparently incidentally in traps lacking appropriate attractants; a promising result for further surveys is different attractants are employed. This study is one of the few in which an invasive species has been detected through iDNA, and highlights its potential for improved detectability of threatened species outside of the tropics and early detection of invasive species.     

Cues used in host‐seeking behavior by frog‐biting midges (Corethrella spp. Coquillet)

We investigated the role of carbon dioxide and host temperature in host attraction in frog‐biting midges (Corethrella spp). In these midges, females are known to use frog calls to localize their host, but the role of other host‐emitted cues has yet not been investigated. We hypothesized that carbon dioxide acts as a supplemental cue to frog calls. To test this hypothesis, we determined the responses of the midges to carbon dioxide, frog calls, and both cues. A significantly lower number of midges are attracted to carbon dioxide and silent traps than to traps broadcasting frog calls. Adding carbon dioxide to the calls does not increase the attractiveness to the midges. Instead, carbon dioxide can have deterrent effects on frog‐biting midges. Temperature of calling frogs is not a cue potentially available to the midges. Contrary to our hypothesis, there was no supplemental effect of carbon dioxide when presented in conjunction to calls. Midge host‐seeking behavior strongly depends on the mating calls emitted by their anuran host. Overall, non‐acoustic cues such as host body temperature and carbon dioxide are not important in long‐distance host location by frog‐biting midges.     

How the environment shapes animal signals: a test of the acoustic adaptation hypothesis in frogs

Long‐distance acoustic signals are widely used in animal communication systems and, in many cases, are essential for reproduction. The acoustic adaptation hypothesis (AAH) implies that acoustic signals should be selected for further transmission and better content integrity under the acoustic constraints of the habitat in which they are produced. In this study, we test predictions derived from the AAH in frogs. Specifically, we focus on the difference between torrent frogs and frogs calling in less noisy habitats. Torrents produce sounds that can mask frog vocalizations and constitute a major acoustic constraint on call evolution. We combine data collected in the field, material from scientific collections and the literature for a total of 79 primarily Asian species, of the families Ranidae, Rhacophoridae, Dicroglossidae and Microhylidae. Using phylogenetic comparative methods and including morphological and environmental potential confounding factors, we investigate putatively adaptive call features in torrent frogs. We use broad habitat categories as well as fine‐scale habitat measurements and test their correlation with six call characteristics. We find mixed support for the AAH. Spectral features of torrent frog calls are different from those of frogs calling in other habitats and are related to ambient noise levels, as predicted by the AAH. However, temporal call features do not seem to be shaped by the frogs’ calling habitats. Our results underline both the complexity of call evolution and the need to consider multiple factors when investigating this issue.     

Calls of Recently Introduced Coquí Frogs Do Not Interfere with Cricket Phonotaxis in Hawaii

Acoustically-signaling animals such as crickets may experience interference from environmental noise, a particular concern given the rise in anthropogenic or other novel sources of sound. We examined the potential for acoustic interference of female phonotaxis to calling song in the Pacific field cricket (Teleogryllus oceanicus) by invasive coqui frogs (Eleutherodactylus coqui) in Hawaii. The frogs were introduced to Hawaii from Puerto Rico in the 1980s. When female crickets were exposed to male calling songs with and without simultaneous broadcast of a coqui chorus, they were equally likely to move toward the cricket song, regardless of the location of the frog sound (ground level or above ground). Unlike some species of frogs and birds, T. oceanicus do not appear to experience acoustic interference from an introduced signaler, even though the introduced species’ calls subjectively seem to be masking the crickets’ songs.     

Effects of Eavesdropping on Subsequent Signalling Behaviours in Male Canaries

Signalling interactions could provide information for an observing third party. This behaviour has been labelled as eavesdropping. Studies on eavesdropping in birds have concerned only few species and have mainly been conducted in the wild. Our experiment was designed to evaluate the effects of eavesdropping on subsequent interactions in male canaries in a controlled laboratory context. The experiment had two stages: a presentation stage and a test stage. During the presentation stage, subjects heard three different interaction types: an alternating interaction, an overlapping interaction or two song sequences presented separately one after the other, i.e. without interaction. Then during the test stage, subjects were allowed to listen to the songs previously heard separately. We noted calls emitted by subjects during the two stages. During the presentation stage, responses of male canaries did not differ according to the type of interaction they could hear. During the test stage, we found a clear effect of the song status on the calls emitted by subjects. They emitted less calls during the songs of the winner than during all other songs. Surprisingly, subjects also produced intermediate responses by emitting fewer calls during the second song previously heard during the presentation phase, and during the song of the looser when compared to the three other songs. Our results show that male canaries obtain information on the relative threat from an overlapping interaction whereas an alternating interaction does not seem to provide any kind of relative information on singers' status. In following encounters, the higher the potential threat of a singer was, the less the subjects emitted calls, probably to avoid the more serious rival. This inhibiting effect is discussed.     

Body size correlates negatively with the frequency of distress calls and songs of Neotropical birds

ABSTRACT The allometric relationship between body size and song frequency has been established in previous studies of temperate and tropical bird communities. However, the relationship between body size and the frequency of distress calls has been examined in only one study of temperate birds. We examined size‐frequency relationships in the distress calls and songs of a Neotropical bird community in northwestern Costa Rica. In 2008 and 2009, we recorded distress calls and determined the body mass of 54 mist‐netted birds representing 38 species, 35 genera, and 14 families. We obtained songs for these same species from sound libraries and commercially available compact discs. For each vocalization, we measured minimum frequency and frequency of maximum amplitude. Larger birds produced lower‐frequency distress calls and songs than smaller birds. Phylogenetically controlled analyses revealed that the frequency of maximum amplitude was negatively correlated with body mass for both distress calls and songs. Minimum frequency was negatively correlated with mass for distress calls, but not songs. Our analyses suggest that the influence of phylogeny on the relationship between frequency characteristics and body size is modest. Pair‐wise comparisons across 37 species revealed that distress calls and songs had similar minimum frequencies, but songs had significantly lower frequencies of maximum amplitude than distress calls. This difference may arise from differences in signal function. Lower‐frequency sounds should transmit farther through forest habitats and songs must often transmit longer distances to reach their intended audience than distress calls. Our results support the general theory that body size is negatively correlated with the frequency of acoustic signals by demonstrating that this pattern holds true for both distress calls and songs in a Neotropical bird community.     

Signal Interception and the Use of Soft Song in Aggressive Interactions

Song sparrows, like many species of songbirds, produce songs of especially low amplitude during aggressive contests. Such ‘soft songs’ have been shown to be reliable signals of intention to attack in song sparrows. Low intensity is a paradoxical feature in a highly aggressive signal, in that it seems likely to make the signal less intimidating to an opponent. A hypothesis that resolves this paradox is that use of soft songs benefits a signaler by limiting the interception of his signals by third party receivers. Here, we test this hypothesis with respect to song sparrows and two classes of third party receivers, predators and conspecific males. We tested whether selection to avoid predation is responsible for use of soft song by examining whether male song sparrows increase production of soft song in an aggressive context when they also receive signals (alarm calls) that indicate a predator is present. We found that the proportion of soft song produced by male song sparrows was actually significantly lower in the predator context than in a control context, directly contradicting the prediction. We tested whether avoiding eavesdropping by conspecific males is a benefit of soft song by removing territory owners and simulating interactions on their territories using playback from two loudspeakers. We found that intrusions by third party males were more likely in trials in which the simulated owner countered an intruder's songs using soft songs than in trials in which the simulated owner countered with loud song, again directly contradicting the hypothesis. We conclude that limiting interception by predators and conspecific males does not provide an explanation for use of soft song by song sparrows.     

QUIET SONG IN SONG BIRDS: AN OVERLOOKED PHENOMENON

ABSTRACT

The theory of communication networks offers functional arguments for the evolution of unobtrusive signals in birds. The vulnerability of interacting conspecifics to predation and to eavesdropping by neighbours during both territorial disputes and courtship would select for short range signals such as the quiet songs of birds. In addition to suggesting contexts in which quiet songs should be used, we use our knowledge of the physics of sound transmission to make predictions about the physical structure of such songs relative to the well studied full songs. We present support for these predictions in six species where quiet singing has been observed.     

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.     

Microclimate and Stream Noise Predict Geographic Divergence in the Auditory Signal of a Threatened Poison Frog

According to the acoustic adaptation hypothesis, abiotic noise generated by streams should promote the evolution of high‐pitched signals in acoustically communicating animals. The putatively selective effect is best demonstrated by studying trait–environment correlations across recently or currently diverging lineages, and when we understand the ecological interactions that underlie the selective pressures. We studied microclimate, frog distribution, abiotic noise, and the frequency of the advertisement call of the Andean poison frog Andinobates bombetes across variable environmental clines at five localities. Our general hypothesis involves three steps: microclimatic clines determine frogs’ distribution, which in turn is associated with different levels of abiotic noise that select for differentially pitched calls. Microclimate changed more abruptly with distance to streams in comparatively dry localities. There, frogs were more aggregated alongside streams and, in turn, experienced higher levels of abiotic noise. As predicted, frogs living alongside streams in dry forests called at higher frequencies, and thus attained comparable signal‐to‐noise ratios, compared with stream‐away frogs. Our data support a role for microclimate in determining frog distribution and thereby the noise conditions that promoted a divergence in a mate‐recognition signal.     

Do frog-eating bats perceptually bind the complex components of frog calls?

The mating calls of male túngara frogs, Physalaemus pustulosus, attract intended (conspecific females) and unintended (eavesdropping predators and parasites) receivers. The calls are complex, having two components: a frequency-modulated “whine” followed by 0–7 harmonic bursts or “chucks”. The whine is necessary and sufficient to elicit phonotaxis from females and the chuck enhances call attractiveness when it follows a whine. Although chucks are never made alone, females perceptually bind the whine and chuck when they are spatially separated. We tested whether an unintended receiver with independent evolution of phonotaxis, the frog-eating bat, Trachops cirrhosus, has converged with frogs in its auditory grouping of the call components. In contrast to frogs, bats approached chucks broadcast alone; when the chuck was spatially separated from the whine the bats preferentially approached the whine, and bats were sensitive to whine–chuck temporal sequence. This contrast suggests that although disparate taxa may be selected to respond to the same signals, different evolutionary histories, selective regimes, and neural and cognitive architectures may result in different weighting and grouping of signal components between generalist predators and conspecific mates.     

Diversity of the Vocal Signals of Concave-Eared Torrent Frogs (Odorrana tormota): Evidence for Individual Signatures

Male concave-eared torrent frogs ( Odorrana tormota ) have an unusually large call repertoire and have been shown to communicate ultrasonically. We investigated the individual specificity of male advertisement calls in order to explore the acoustic bases of individual recognition, which was demonstrated in an accompanying study. Vocalizations of 15 marked males were recorded in the field. A quantitative analysis of the signals revealed eight basic call-types. Two of them (the single- and multi-note long-calls) were investigated in more detail. Long-calls were characterized by pronounced and varying frequency modulation patterns, and abundant occurrence of nonlinear phenomena (NLP), i.e., frequency jumps, subharmonics, biphonations and deterministic chaos. The occurrence of NLP was predictable from the contour of the fundamental frequency in the harmonic segment preceding the onset of the NLP, and this prediction showed individual-specific patterns. Fifteen acoustic variables of the long calls were measured, all of which were significantly different among individuals, except biphonic segment duration. Discriminant function analysis (DFA) showed that 54.6% of the calls could be correctly assigned to individual frogs. The correct classification was above chance level, suggesting that individual specificity of calls underlie the ability of males to behaviorally discriminate the vocal signals of their neighbors from those of strangers, a remarkable feat for a frog species with a diverse vocal repertoire. The DFA classification results were lower than those for other anurans, however. We hypothesize that there is a tradeoff between an increase in the fundamental frequency of vocalizations to avoid masking by low-frequency ambient background noise, and a decrease in individual-specific vocal tract information extractable from the signal.     

Eavesdropping on heterospecific alarm calls: from mechanisms to consequences

Animals often gather information from other species by eavesdropping on signals intended for others. We review the extent, benefits, mechanisms, and ecological and evolutionary consequences of eavesdropping on other species' alarm calls. Eavesdropping has been shown experimentally in about 70 vertebrate species, and can entail closely or distantly related species. The benefits of eavesdropping include prompting immediate anti‐predator responses, indirect enhancement of foraging or changed habitat use, and learning about predators. Eavesdropping on heterospecifics can provide more eyes looking for danger, complementary information to that from conspecifics, and potentially information at reduced cost. The response to heterospecific calls can be unlearned or learned. Unlearned responses occur when heterospecific calls have acoustic features similar to that used to recognize conspecific calls, or acoustic properties such as harsh sounds that prompt attention and may allow recognition or facilitate learning. Learning to recognize heterospecific alarm calls is probably essential to allow recognition of the diversity of alarm calls, but the evidence is largely indirect. The value of eavesdropping on different species is affected by problems of signal interception and the relevance of heterospecific alarm calls to the listener. These constraints on eavesdropping will affect how information flows among species and thus affect community function. Some species are ‘keystone’ information producers, while others largely seek information, and these differences probably affect the formation and function of mixed‐species groups. Eavesdroppers might also integrate alarm calls from multiple species to extract relevant and reliable information. Eavesdropping appears to set the stage for the evolution of interspecific deception and communication, and potentially affects communication within species. Overall, we now know that eavesdropping on heterospecific alarm calls is an important source of information for many species across the globe, and there are ample opportunities for research on mechanisms, fitness consequences and implications for community function and signalling evolution.     

Social Calls Provide Tree‐dwelling Bats with Information about the Location of Conspecifics at Roosts

Animals can use signals emitted by other animals as sources of information. Auditory signals are important in communication networks, as they can potentially convey information about the location and state of conspecifics and other species over long distances. Signalling is important in fission–fusion societies, in which animals from the same social group temporarily split into subgroups and frequently change roost sites. We used playbacks of social calls of the noctule Nyctalus noctula produced in roosts, to show how bats might maintain group cohesion and to test the hypothesis that noctules can locate conspecifics when returning from foraging trips by eavesdropping on or communicating with roosting individuals. Noctules responded strongly to broadcasted social calls. Their reactions included inspections and landing on a loudspeaker broadcasting social calls and occasional social vocalisation. Responses by other bat species to the noctule social calls were negligible. The high amplitude, low‐frequency vocalisations emitted by noctules in roosts can propagate over long distances and allow group members to announce their position. Bats can extract information about the location of roosts containing conspecifics by eavesdropping or by communication. Social calls may thus be sufficient to locate conspecifics in roosts and maintain spatial associations of groups in mammals.     

Pure Ultrasonic Communication in an Endemic Bornean Frog

Huia cavitympanum, an endemic Bornean frog, is the first amphibian species known to emit exclusively ultrasonic (i.e., >20 kHz) vocal signals. To test the hypothesis that these frogs use purely ultrasonic vocalizations for intraspecific communication, we performed playback experiments with male frogs in their natural calling sites. We found that the frogs respond with increased calling to broadcasts of conspecific calls containing only ultrasound. The field study was complemented by electrophysiological recordings from the auditory midbrain and by laser Doppler vibrometer measurements of the tympanic membrane''s response to acoustic stimulation. These measurements revealed that the frog''s auditory system is broadly tuned over high frequencies, with peak sensitivity occurring within the ultrasonic frequency range. Our results demonstrate that H. cavitympanum is the first non-mammalian vertebrate described to communicate with purely ultrasonic acoustic signals. These data suggest that further examination of the similarities and differences in the high-frequency/ultrasonic communication systems of H. cavitympanum and Odorrana tormota, an unrelated frog species that produces and detects ultrasound but does not emit exclusively ultrasonic calls, will afford new insights into the mechanisms underlying vertebrate high-frequency communication.     

Vigilance against predators induced by eavesdropping on heterospecific alarm calls in a non-vocal lizard Oplurus cuvieri cuvieri (Reptilia: Iguania)

Prey animals can reduce their risk of predation by detecting potential predators before encounters occur. Some animals gain information about nearby predators by eavesdropping on heterospecific alarm calls. Despite having well-developed ears, most lizards do not use vocal information for intraspecific communication, and few studies have shown practical use of the ears in wild lizards. Here, we show that the Madagascan spiny-tailed iguana (Oplurus cuvieri cuvieri) obtains auditory signals for predator detection. The Madagascan spiny-tailed iguana and the Madagascar paradise flycatcher (Terpsiphone mutata) are syntopic inhabitants of the Ampijoroa dry deciduous forest of Madagascar. The iguana and the flycatcher have neither a predator–prey relationship nor resource competition, but they have shared predators such as raptors and snakes. Using playback experiments, we demonstrated that the iguana discriminates mobbing alarm calls of the flycatcher from its songs and then enhances its vigilance behaviour. Our results demonstrate the occurrence of an asymmetrical ecological relationship between the Madagascan spiny-tailed iguana and the paradise flycatcher through eavesdropping on information about the presence of predators. This implies that indirect interspecific interactions through information recognition may be more common than generally thought in an animal community.