A laryngeal fibrous mass impacts the acoustics and attractiveness of a multicomponent call in túngara frogs (Physalaemus pustulosus)

The evolution of elaborate signals can emerge from changes in anatomical signaling structures. In the male túngara frog, a simple advertisement call (‘whine’) can be ornamented facultatively with a suffix (‘chuck’) to produce a more attractive complex call, or ‘whine-chuck’. A fibrous mass (FM1) supported by the vocal cords plays a role in chuck production. Here, we examine the effects of FM1 ablation on a large set of spectral and temporal features of both the whine and chuck and we test the hypothesis that FM1 ablation reduces call attractiveness to females. Both call components were impacted by FM1 ablation, but especially the suffix. The proportion of energy in the suffix’s odd compared to even harmonics diminished markedly as did the relative amplitude, effectively eliminating the chuck percept. FM1 ablation also reduced the whine’s frequency and its rate of frequency modulation. Moreover, post-surgery chucks no longer enhanced the attractiveness of the simple call and whines also appeared to diminish in attractiveness. Together, our results demonstrate that FM1 plays a role in the production of both call components in a way that stimulates the female auditory system and that the growth of FM1 had potentially positive sexual selection implications for the pre-existing simple call.     

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.     

The Consequences for Communication of Call Overlap in the Tungara Frog,a Neotropical Anuran with a Frequency-modulated Call

We presented male tungara frogs, Physalaemus pustulosus, with call-triggered computer-synthesized whines that either did or did not overlap the frogs' own frequency-modulated whines in time. When the stimulus was nonoverlapping, males added a high proportion of chuck notes to their calls. When the stimulus was overlapping, males responded with either no or only small increases in chucking. This suggests they have difficulty detecting whines while vocalizing. When female tungara frogs were given a choice between alternating whines and out-of-phase overlapping whines they did not discriminate. The result with males was similar to that previously obtained with species of frogs that have amplitude-modulated advertisement calls (Schwartz 1987a), the result with females was different. We discuss our findings in relation to peripheral processing of spectral and temporal information in the anuran auditory system.     

Female mate choice and the potential for ornament evolution in túngara frogs Physalaemus pustulosus

The potential for ornament evolution in response to sexual selection rests on the interaction between the permissive-ness or selectivity of female preferences and the constraints on male development of signaling related traits. We investigate the former by determining how latent female preferences either exaggerate the magnitude of current traits (I.e. Elaborations) or favor novel traits (I.e. Innovations). In tungara frogs, females prefer complex mating calls (whine-chucks) to simple calls (whine only). The whine is critical for mate recognition while the chuck further enhances the attractiveness of the call. Here we use a combina-tion of synthetic and natural stimuli to examine latent female preferences. Our results show that a diversity of stimuli, including conspecific and heterospecific calls as well as predator-produced and human-made sounds, increase the attractiveness of a call when added to a whine. These stimuli do not make simple calls more attractive than a whine-chuck, however. In rare cases we found stimuli that added to the whine decrease the attractiveness of the call. Overall, females show strong preferences for both elaborations and innovations of the chuck. We argue that the emancipation of these acoustic adornments from mate recognition allows such female permissiveness, and that male constraints on signal evolution are probably more important in explaining why males evolved their specific adornment. Experimentally probing latent female preferences for stimuli out of the species' range is a useful means to gain insights about the potential of female choice to influence signal evolution and thus the astounding diversity in male sexually-selected traits.     

Frequency modulated calls and species recognition in a neotropical frog

Summary The neotropical frogPhysalaemus pustulosus (Leptodactylidae) has a complex advertisement call and different call components perform different functions. The whine is a necessary and sufficient stimulus for species recognition. The chuck provides information about male body size that is used by females in mate choice (Ryan 1980, 1983), but the chuck must be combined with the species-identifying whine to elicit maximum behavioral responses from males and females. One of the important features of the whine in eliciting behavioral responses from both sexes is the direction of frequency modulation. This suggests that current models of species recognition in anurans based on a frequency filtering mechanism of the peripheral auditory system and selective responses to combinations of frequencies in the central nervous system are not sufficient to explain species recognition inP. pustulosus. Recent neurophysiological studies of the anuran torus semicircularis are discussed in terms of a mechanism for decoding frequency sweeps.     

Acoustic Competition in Physalaemus pustulosus, a Differential Response to Calls of Relative Frequency

The response of the male túngara frog ( Physalaemus pustulosus ) to conspecific whines of different frequencies was examined. In the first series of playback experiments (fixed frequency), three types of synthetic stimuli were used, corresponding to calls of high frequency (HFF; x + 2 SD), mid-frequency (MFF; x ), and low frequency (LFF; x − 2 SD) for the study population. In the second series of interactive playback experiments (relative frequency), whines of frequency relative to that of the male subject were used: male frequency + 2 SD (HRF), male frequency (MRF), and male frequency −2 SD (LRF). In the fixed frequency experiments, male vocal response did not vary among treatments. However, in the relative frequency experiments, males responded with more whines, and above all, with more chucks, to stimuli of similar or higher frequency than to stimuli of lower frequency than their own. In other words, male vocal competition escalates when competitors have whines with similar or relatively higher frequencies to their own, but does not increase when competitors have call frequencies that are at the mean or higher for the population. This differential response might result from competition between males of different sizes, since the frequency of the whine and male size is significantly correlated.     

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.     

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.     

Sexual Selection in Insect Choruses: Influences of Call Power and Relative Timing

Female preference for male song in acoustic insects is primarily influenced by call energy or power, but nonenergy features such as the relative timing of male calls may also be critical in preference. Preferences for leading calls, which may be a type of precedence effect, are an example of the latter factor. In various species, females preferentially orient toward the leading of two or more spatially separated calls presented in controlled playback experiments, however the importance of this effect on mate choice in actual choruses and natural populations is generally unknown. We studied the determinants of mate choice in reenacted choruses of the tettigoniid Ephippiger ephippiger, a species in which females prefer leading calls in two-choice experiments, and neighboring males adjust their relative call timing in a way that reduces the incidence of following calls. We found that mate choice, as indicated by the pattern of female settlement, largely reflects call rate and call constancy. But, we also found suggestions that female choice is influenced by the acoustic neighborhood in which a male sings, males in neighborhoods with more overall singing being preferred, and by a males incidence of leading calls relative to his neighbors. Although statistically inconclusive owing to few relevant samples, we note that the level of preference for leading calls observed in E. ephippiger choruses is comparable to that found in controlled playback experiments.     

The effects of time,space and spectrum on auditory grouping in túngara frogs

Male túngara frogs (Physalaemus pustulosus) produce complex calls consisting of two components, a ~350 ms FM sweep called the “whine” followed by up to seven ~40 ms harmonic bursts called “chucks”. In order to choose and locate a calling male, females attending to choruses must group call components into auditory streams to correctly assign calls to their sources. Previously we showed that spatial cues play a limited role in grouping: calls with normal spectra and temporal structure are grouped over wide angular separations (≤135°). In this study we again use phonotaxis to first test whether an alternative cue, the sequence of call components, plays a role in auditory grouping and second, whether grouping is mediated by peripheral or central mechanisms. We found that while grouping is not limited to the natural call sequence, it does vary with the relative onset times of the two calls. To test whether overlapping stimulation in the periphery is required for grouping, the whine and chuck were filtered to restrict their spectra to the sensitivity ranges of the amphibian and basilar papillae, respectively. For these dichotic-like stimuli, grouping still occurred (albeit only to 45° separation), suggesting that stream formation is mediated by central mechanisms.     

Ecological and Social Factors Affecting the Vocal Behavior of Adult Female Squirrel Monkeys

Focal recordings of the vocalizations of squirrel monkeys, Saimiri sciureus, occupying an undisturbed Peruvian habitat were collected to evaluate the importance of both the ecological and social functions of female vocal behavior. The rates and sequences of six call types were examined by context: single, double, and multiple chuck, peep, tweet, and tweet-chuck. In contrast to laboratory studies, our findings emphasize the primacy of ecological functions in the wild, where calling permits females to operate as a convoy of spatially separated individuals in an arboreal habitat where visual contact is limited. Chuck calls are probably best interpreted as contact calls. The rate of chucks and tweet-chucks increased when the nearest adult female was > 5 m away. However, call production did not predict a change in the spatial separation between a female and her nearest adult female. During travel, the rate of single and double chucks was greater and the rate of multiple chucks was reduced. No direct relationship was found between foraging activities and vocal behavior. Although secondary, social factors did have a subtle effect on vocal behavior: the larger the social alliance of a female, the lower the rate and repetitiveness of her chuck vocalizations. We also consider the role of variations in vocalization rates among primates and the differing conclusions of field and captive studies of squirrel monkey vocal behavior.     

Two-choice phonotaxis in Hyperolius marmoratus (Anura: Hyperoliidae): the effect of temporal variation in presented stimuli

Female painted reed frogs, Hyperolius marmoratus, were subjected to two-choide discrimination experiments to determine whether temporal overlap in the presented stimuli affects frequency preferences. The results showed that females preferred low frequency calls when the stimuli were presented alternately. Simultaneous presentation of stimuli resulted in a random response by females. When presented stimuli partially overlapped or abutted each other, the females responded significantly more often to the leading call irrespective of its frequency. These findings provide some insight into the possible effects of male vocal interactions on the ability of females actively to choose mates based on call frequency in natural breeding assemblages.     

Modelling the production of complex calls in the túngara frog (Physalaemus pustulosus)

Relatively few studies have used experimental manipulations to investigate the mechanics of vocal production in frogs and toads, even though many frogs produce complex signals with multiple components and/or nonlinearities. Modelling approaches can add to empirical studies by illuminating how various components of the vocal system interact to produce communication signals. In this study, we use bond graphs, a lumped-element modelling technique, to explore how the combination of active modulation of vocal production and the passive dynamics of a unique laryngeal structure result in the complex calls produced by males in an anuran model system. The túngara frog (Physalaemus (= Engystomops) pustulosus) produces advertisement calls with a ‘whine’ and a facultative ‘chuck’. Whines are amplitude and frequency modulated. The chuck is characterized by its spectral complexity and appears to contain a period doubling bifurcation resulting in subharmonics. In our model, we focus on how a fibrous mass attached to the vocal cords results in subharmonics in the chuck. Our models suggest that active (neural) modulation of the fibrous mass is not necessary for the transition between the spectral characteristics of the whine and chuck. Rather, it is possible that the vibratory mode of the fibrous mass and thus the vocal cords changes passively as a result of changes in airflow through the system.     

The separate and combined effects of harmonic structure, phase, and FM on female preferences in the barking treefrog (Hyla gratiosa)

In natural advertisement calls of the barking treefrog, Hyla gratiosa, a small amount of incoherent frequency modulation (FM) is present. Incoherency in the FM of a call creates inharmonicity and phase changes between its frequency components. In this study, the combined and separate effects of the harmonic structure, phase spectrum, and FM of an advertisement call on female choice were tested. The harmonic structure of a call can have a direct effect on female preference; females showed a significant preference for static-inharmonic calls over static-harmonic calls. Neither differences in phase or FM alone conferred a preference in two choice tests. However, when FM is present in both calls it does influence female preference for harmonic structure -namely harmonic calls become preferable to inharmonic calls. This reversal of female preference for inharmonicity in a call by the presence of FM suggests that call parameters may interact, and thereby effect mate choice.Abbreviations AP amphibian papilla - BP basilar papilla - FM frequency modulation - PM phase modulation - HS harmonic structure - GB Gaussian Band     

Recognition of order effects in squirrel monkey antiphonal call sequences

Squirrel monkeys exchange chuck vocalizations in antiphonal sequences that suggest a request for information, and a response to that request. Chucks are characterized by measurable acoustic differences, notably in peak frequency, related to their position in a sequence. To determine the cues by which animals might identify a chuck that is a request for information from one that is a response, first-in-sequence (α) and second-in-sequence (β) chucks, differing in peak frequency, were recorded from familiar individuals and strangers. These chucks, and a sham control, were played back, in the temporal context of a first-in-sequence call, to a target group of socially housed captive squirrel monkeys. Animals responded more strongly to α chucks than to β chucks for calls originating from familiar individuals. No distinction was made between the α and β chucks of strangers, and all strangers' chucks got a weaker response than did familiar α chucks. Squirrel monkeys probably use acoustic differences, rather than context, to discriminate the ordinal significance of a chuck, but cannot do so unless they are familiar with the caller. © 1993 Wiley-Liss, Inc.     

Preferences for Call Spectral Properties in Hyla intermedia

We studied the pattern of variation in the spectral properties of male advertisement calls and female preference functions for these same properties in the Italian treefrog (Hyla intermedia). The call spectral properties (fundamental and dominant frequencies) were highly negatively correlated with body size, they showed low within‐individual variation, and, at the population level, they were found to be under weak stabilizing selection. In two‐choice discrimination tests, females did not show preferences between calls with fundamental and dominant frequencies within two standard deviations from the population mean, whereas females significantly discriminated against calls when their frequencies were three (or more) standard deviations above or below the population mean. Consistent with the observed permissiveness in female preference over the call spectral structure, in the natural population, we found no evidence either of directional selection on male body size or of a size‐assortative mating pattern. The pattern of preferences observed at the population level did not mirror the preferences of individual females. In fact, in a multi‐trial discrimination experiment, females showed significant differences in their choice between the average frequency call and a two standard deviation lower than average frequency alternative, for which no significant preferences were observed at the population level. Variations in preference were not found to correlate with female body size.     

Spatially-mediated call pattern recognition and the cocktail party problem in treefrog choruses: can call frequency differences help during signal overlap?

Male gray treefrogs, Hyla versicolor, advertise for mates in dense assemblages characterized by high levels of noise and acoustic clutter. In pairwise interactions, males alternate pulsatile advertisement calls and so reduce call overlap to levels below that expected by chance. However, in choruses consisting of more than two males, acoustic interference increases dramatically. Moreover, males do not seem to exhibit selective attention in a way that reduces call interference among nearest neighbours. Previous research has also demonstrated that although females discriminate strongly against overlapped calls, negative effects of call overlap can be attenuated by a large angular separation between signal sources. However, call stimuli employed were identical in spectrum and so this situation differs from that likely in nature. Based on studies of ‘auditory stream segregation’ with other taxa, we hypothesized that realistic differences in the frequencies of overlapping calls could improve the ability of females to discern critical call features during overlap of separated call sources. We found that, although, under some circumstances, differences in call frequency may help females distinguish among neighbouring males giving temporally proximate calls, naturalistic spectral differences do not seem to help females perceptually separate the overlapping calls of neighbouring conspecific males.     

Vocalization of the tree frogPolypedates maculatus (Rhacophoridae)

The period of calling activity ofPolypedates maculatus lies between April and October. Males possess an indistinct subgular vocal sac which turns yellow during the breeding season. Mating calls type I, type II and distress calls have been identified. Mating calls type I and type II consist of a single pulse group. Type I call comprises of 7–22 pulses, whereas type II call consists of 4–6 pulses. Pulses are short. The frequency spectrum is broad and continuous. Distress calls, with 6 hormonics, are given by the females with their mouth open.     

Chuck Vocalizations of Wild Female Squirrel Monkeys (Saimiri sciureus) Contain Information on Caller Identity and Foraging Activity

Analysis of the acoustic signal of the chuck vocalizations of adult female squirrel monkeys (Saimiri sciureus) in Parque Nacional de Manu, Peru, revealed consistent differences within and between individuals. We quantified four peak frequency parameters: (a) the peak frequency of single chucks, (b) the first and (c) the second peak frequencies of double chucks, and (d) the peak difference: the difference between the first and the second double chuck peaks. One-way ANOVAs and a posteriori comparisons of these variables revealed that each distinguished more than 70% of all possible pairs of females. When all double chuck measures were included in a discriminant analysis, 57% of double chucks were correctly assigned to the caller. Another category of information potentially encoded in the acoustic structure of chuck vocalizations is foraging activity. When the chucks of squirrel monkeys during foraging and nonforaging activities were compared, the single chuck peak frequency, and the first peak frequency and the peak difference of double chucks, were significantly reduced during foraging contexts. Previously Boinski and Mitchell (1992) concluded that chucks facilitate group cohesion among widely dispersed troop members by providing information of the location of callers; the rate of chucks produced by an adult female increases as she becomes more spatially and visually separated from other adult females. The additional information potentially conveyed by chucks on caller identity and foraging activity documented in these new analyses further emphasizes the role chucks serve to enhance group coordination and cohesion.     

Call recognition and female choice in a treefrog with a multicomponent call

Acoustic mating signals are typically species‐specific, and often additionally are subject to directional female preferences. Male executioner treefrogs, Dendropsophus carnifex, produce a multicomponent advertisement call composed of an introductory screech note followed by two or more click notes. Here, we tested (i) call recognition by comparing female directed phonotaxis towards individual and combined call components: screech vs. clicks vs. screech + clicks, (ii) female preferences for greater numbers of click notes and (iii) female preferences for faster call rates. The results demonstrated that screeches and clicks, presented either separately or together as a complete call, evoke similar female responses, suggesting that either note was sufficient to elicit a mate‐recognition response. Additionally, females preferred calls with greater numbers of click notes and with faster call rates. We interpret these results within the context of female mate selection in natural choruses.