Discrimination of sinusoidally frequency-modulated sound signals mimicking species-specific communication calls in the FM-bat Phyllostomus discolor

In the lesser spear-nosed bat, Phyllostomus discolor, maternal directive calls are characterized by an individual type of sinusoidal frequency modulation (= SFM) pattern. Beside modulation frequency, modulation depth, carrier frequency, and number of modulation cycles per call contribute to the mother's vocal signature. Since juvenile P. discolor learn to adapt their isolation calls to the corresponding call characteristics of the own mother or even to playback of a computer-stored directive call, if hand-reared in the absence of conspecifics, the bats' auditory system ought to be able to resolve interindividual differences in communication call structure. However, quantitative psychoacoustic data on the discrimination of SFM signals in this species are not available. Thus, in the present study, lesser spear-nosed bats were trained in a two-alternative forced-choice procedure to discriminate between two alternatingly presented SFM sound signals differing in modulation frequency. Other characteristics of acoustic stimuli were identical and designed to mimick the fundamental of species-specific calls. By gradually reducing the difference in modulation frequency between both stimuli within the behavioural relevant range until the animals' performance dropped below the 75%-correct level, a considerable auditory spectro-temporal resolution has been revealed. Particularly in comparison to the overall interindividual variation of this call parameter (minimal modulation frequency = 49 Hz, maximum = 100 Hz), the determined average difference limen for modulation frequency of 2.42 ± 0.29 Hz seems substantial and sufficient for labelling individuals. Accepted: 30 November 1996     

Hearing in the FM-bat Phyllostomus discolor: a behavioral audiogram

Absolute auditory thresholds of six adult lesser spear-nosed bats Phyllostomus discolor (Chiroptera, Phyllostomidae) were determined in a two-alternative forced-choice procedure. Behavioral responses to pure tone stimuli could be elicited throughout the tested frequency range of 5–142 kHz. The shape of the average audiogram is characterized by two sensitivity peaks and a pronounced increase of thresholds around 55 kHz, and towards the limits of the tested frequency range. The spectral extent of both sensitivity peaks shows a close relation to the bandwidth of two types of species-specific vocalizations. The first low threshold area (> 10 and < 55 kHz) of the audiogram seems perfectly adapted to the directive call used for intraspecific communication, whereas the second sensitivity peak, centered around 85 kHz, covers most of the bandwidth of the species' echolocation calls.Abbreviations CF constant frequency - FM frequency modulation - l left - r right - SPL Sound pressure level     

Auditory sensitivity and frequency selectivity in greater spear-nosed bats suggest specializations for acoustic communication

We investigated the relationship between auditory sensitivity, frequency selectivity, and the vocal repertoire of greater spear-nosed bats (Phyllostomus hastatus). P. hastatus commonly emit three types of vocalizations: group-specific foraging calls that range from 6 to 11 kHz, low amplitude echolocation calls that sweep from 80 to 40 kHz, and infant isolation calls from 15 to 100 kHz. To determine if hearing in P. hastatus is differentially sensitive or selective to frequencies in these calls, we determined absolute thresholds and masked thresholds using an operant conditioning procedure. Both absolute and masked thresholds were lowest at 15 kHz, which corresponds with the peak energy of isolation calls. Auditory and masked thresholds were higher at sound frequencies used for group-specific foraging calls and echolocation calls. Isolation calls meet the requirements of individual signatures and facilitate parent-offspring recognition. Many bat species produce isolation calls with peak energy between 10 and 25 kHz, which corresponds with the frequency region of highest sensitivity in those species for which audiogram data are available. These findings suggest that selection for accurate offspring recognition exerts a strong influence on the sensory system of P. hastatus and likely on other species of group-living bats.     

The development of vocalizations in Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during post-natal growth and the maintenance of individual vocal signatures

The development of vocalizations during post-natal growth in the microchiropteran bat Pipistrellus pipistrellus is described. Vocalizations served as precursors of echolocation sounds and as isolation calls used to attract mothers. Although calls judged to be echolocation precursors tended to be of short duration and possessed high rates of frequency modulation when compared with isolation calls, a wide spectrum of intermediate calls existed making classification diffuse. Changes in the frequencies and durations of calls during growth are described. Multiple discriminant analysis showed considerable inter-individual variation in isolation calls, while the calls of any individual were remarkably consistent in their structure at both six days and 15 days of age. The relative importance of acoustic call parameters in contributing towards inter-individual variation changed between six days and 15 days. Vocal signatures of youngsters were probably important in allowing a mother to identify her own offspring in a creche thus preventing misdirected maternal care in this species, though vocal signatures of infants changed during development. Echolocation calls of flying juveniles were compared with calls from their mothers.     

Geographical variation in male advertisement calls and female preference of the wide‐ranging canyon treefrog,Hyla arenicolor

We surveyed the geographical variation in male advertisement calls of the wide‐ranging canyon treefrog, Hyla arenicolor, and found large call differences among geographically distant lineages that had been characterized by a recent phylogeographical study. To test whether these call differences were biologically relevant and could allow reproductive isolation of different lineages should they come into secondary contact, we assessed female preference in a lineage occurring in southern Utah and north‐western Arizona, USA. These females exhibited a strong preference for their own lineage's call type over the calls of two Mexican lineages, but not over the calls from the geographically nearest lineage. We also identified traits that female frogs probably use to discriminate between lineage‐specific advertisement calls. Our behavioural results, together with recent molecular estimates of phylogenetic relationships among lineages, will guide future work addressing the evolutionary forces that have led to this biologically significant variation in male sexual signals. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Discrimination of Infant Isolation Calls by Female Greater Spear-Nosed Bats, Phyllostomus hastatus

In colonial species, recognition of offspring should be under strong selection. For accurate identification to occur offspring must emit individually distinctive signals and parents must be able to discriminate between signals. Female greater spear-nosed bats (Phyllostomus hastatus) roost in stable social groups and use infant vocalizations, termed isolation calls, to locate and identify their young. In this study, we investigate both the production and perception of isolation calls in P. hastatus. First, we measured acoustic features and found that after controlling for ontogenetic effects, sufficient variation exists between pups for isolation calls to function as individual signatures. Moreover, pups from the same social group emit calls with more similar spectral and spectro-temporal features than pups from different social groups, indicating that these features are likely heritable. We used psychoacoustic experiments in the laboratory to determine if adult females could discriminate between calls from pups in the same or different social group. Females discriminated between pups when faced with a template-matching task and their performance was correlated with the salience of spectral and spectro-temporal features. We found no difference in performance when females had to discriminate between pups from the same and different social groups. These results indicate that females should be able to accurately identify their young using isolation calls.     

How Do Infanticidal Male Bank Voles (Myodes glareolus) Find the Nest with Pups?

Infanticide, the killing of conspecific young, occurs in most mammal species, like in our study species, the bank vole (Myodes glareolus). Infanticide by adult males is regarded as a strong factor affecting recruitment of young into population. It is considered as an adaptive behaviour, which may increase male fitness via resource gain or an increased access to mates. When an intruder is approaching the nest, the mother should not be present, as her nest guarding is very aggressive and successful. Pups use ultrasonic vocalisation to call their mother when mother leaves nest for foraging but it is not know which cues do infanticidal males use to find the nest with vulnerable pups to commit infanticide? We studied whether the pups' sounds or the olfactory cues of the nest guide the males of known infanticidal behavioural trait towards the nest with vulnerable pups. Four nest boxes in a large indoor arena offered different nesting cues: nest odour, pup vocalisation, both odour and sound or control with no cue. The result showed that infanticidal males were more active in their searching behaviour than non‐infanticidal males and seemed to target the nest providing only acoustic cues. Four of the males, all infanticidal, intruded the nest box. Infanticidal males seem to actively search for nests with vulnerable pups by eavesdropping pup begging calls for absent mother. However, under natural conditions, mother presence and aggressive nest protection may be an effective counter strategy against strange male infanticide. When trapping study voles from the wild, we monitored occurrence of male infanticide across the breeding season from early to late summer. Proportion of infanticidal males was between 25 and 29% of all males tested along the breeding season. Our results suggest that male infanticide seems to cause a stable threat for pup mortality in increasing breeding season density.     

Advertising individual identity by mother and adolescent contact calls in Siberian wapiti Cervus elaphus sibiricus

Individualistic contact calls facilitate mother‐offspring reunion after separation. However, in many mammals, both the acoustic structure and individuality of contact calls differ between mother and young. In contrast, in Siberian wapiti Cervus elaphus sibiricus, contact calls are similar in the acoustics between mother and young, whereas effects of this similarity on vocal individuality were not investigated. In this study, we analyzed acoustic differences between closed‐mouth (nasal) and open‐mouth (oral) contact calls and examined individuality of the most usual oral calls of 19 Siberian wapiti (9 hinds and 10 5–6‐month adolescents) emitted in response to mother‐offspring separation. In the oral calls, the values of frequency and power variables were higher than in the nasal calls. Calls of hinds and adolescents did not differ by the maximum fundamental frequency and duration, whereas the peak frequency was higher in the young. Discriminant function analysis (DFA) based on 11 acoustic variables of oral calls accurately classified to individual 92.5% of hind calls and 96.9% of adolescent calls (chi‐square test for differences between hinds and adolescents, p = 0.19). Variables mainly contributing to vocal identity (duration, start, and maximum fundamental frequency) were the same in calls of mothers and adolescents. We conclude that similarities in the acoustics calls of mothers and adolescents mean that they do not differ in their potential for encoding individual identity, suggesting a mutual process of mother‐offspring vocal recognition in Siberian wapiti.     

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.     

The genetic basis and evolution of acoustic mate recognition signals in a Ribautodelphax planthopper (Homoptera,Delphacidae) 1. The female call

Both sexes of the planthopper Ribautodelphax imitans produce species specific acoustic signals. Earlier experiments have shown that isolation between Ribautodelphax species in captivity is at least partly due to male preference for calls of conspecific females. The genetic basis of the female call is studied by bi-directional artificial selection for large and small interpulse intervals (IPI). This resulted in non-overlapping distributions of IPI after only five generations. The mean of eight realized heritability estimates over five generations was above 80%; estimates over ten generations were generally well above 50%. The character is shown to be of a polygenic nature, determined by at least 6 segregating genetic factors. The other features of the female call, strophe duration, and modulation of pulse repetition frequency within the strophe, showed significantly correlated responses. Sexual isolation tests after 10 generations of selection revealed significant symmetrical assortative mating, but coselected males did not exhibit a significant preference for playback calls of females from their own selection line. In view of the high heritability for the call character, and the considerable ecological isolation among Ribautodelphax species, it seems unlikely that the female call differentiated as an adaptation to prevent hybridization (reinforcement). More likely, call and call preference were shaped by sexual selection during allopatry, and may have (had) incidentally an effect in species isolation.     

Vocal behavior of Great Curassows,a vulnerable Neotropical bird

ABSTRACT The Cracidae rank among the most threatened families of Neotropical birds, and studies of their vocal behavior may help guide conservation and monitoring efforts. We describe the vocal behavior of Great Curassows (Crax rubra), a little‐studied Cracid species currently listed as vulnerable. From 2008 to 2010, we recorded curassows in northwest Costa Rica using both handheld and automated digital recorders. Analysis of recordings revealed that Great Curassows had a vocal repertoire of five call types. Yip and bark calls are sex‐specific alarm calls of short duration (0.12 and 0.08 s, respectively). The descending whistle is a longer duration alarm call (2.18 s) produced primarily by males. The snarl is a short call (0.67 s) associated with a threat display produced by adults with dependent young. The boom call was the most common Great Curassow vocalization, and was given only by males. Boom calls are long (8.86 s), low‐frequency (<150 Hz), multisyllable calls comprised of four stereotyped phrases. Great Curassows often uttered boom calls well before dawn, with a peak in activity at dawn and the hours following. Males produced bouts of repeated boom calls that lasted an average of 35 min, but sometimes continued for more than 5 h. Boom calls were given from February to June, with a peak in late April and early May when breeding begins. Discriminant analysis of boom calls of birds from 10 different locations revealed interindividual variation in call structure that may be useful for bioacoustic monitoring of individuals. Our results suggest that automated recorders might provide a way to monitor the abundance of male curassows because their boom calls are given frequently during the period from February to June and can be detected at distances up to 250 m.     

INDIVIDUAL VARIATION OF THE FEMALE ATTRACTION CALL PRODUCED BY AUSTRALIAN FUR SEAL PUPS THROUGHOUT THE MATERNAL DEPENDENCE PERIOD

ABSTRACT

Australian fur seals are colonial breeding animals that give birth on crowded rookeries. Females leave their pups unattended for extended periods while they forage at sea. On return to the colony, a mother must relocate her pup amongst the hundreds of other pups. Vocal recognition is thought to play a vital role in maintaining the mother-pup bond. In the present study, four sets of 7 different pups were recorded once each at different times throughout the maternal dependence period. The Female Attraction Call was used to determine whether Australian fur seal pups produce individually distinct calls which could be used as a basis for vocal recognition. Results from three different analyses (PIC, DFA and CART) indicated that the fundamental frequency, number of parts per call, duration, quavering and peak frequency changes at the start, mid-point and end of the call (i.e., along PEAK Fl) were important to recognition. In 75% of cases using DFA, the Female Attraction Call was classified to the correct caller, suggesting that there is sufficient stereotypy within individual calls, and sufficient variation between them, to enable vocal recognition by females.     

Does Gray Squirrel (Sciurus carolinensis) Response to Heterospecific Alarm Calls Depend on Familiarity or Acoustic Similarity?

In habitats in which multiple species are prey to the same predators, individuals can greatly benefit from recognizing information regarding predators that is provided by other species. Past studies have demonstrated that various mammals respond to familiar heterospecific alarm calls, but whether acoustic similarity to a familiar call can prompt a mammal's recognition of an unfamiliar call has yet to be shown. We presented alarm calls to free‐ranging eastern gray squirrels (Sciurus carolinensis) and recorded behavioral changes in vigilance and antipredatory response. Playbacks included alarm calls of a sympatric bird (American robin, Turdus migratorius), an allopatric bird with a call structure similar to that of the robin (common blackbird, Turdus merula), and an allopatric bird with a distinct call structure (New Holland honeyeater, Phylidonyris novaehollandiae). Squirrels responded significantly more frequently to squirrel alarm calls (positive control) than to robin song (negative control) or honeyeater calls. Squirrel response to robin and blackbird alarm calls was statistically similar to their response to squirrel alarm calls, indicating that squirrels responded to those alarm calls as if they provided information about the presence of predators. However, squirrel response to robin song was not statistically different from response to any of the other avian calls, including the robin and blackbird alarms, suggesting that squirrels neither respond to blackbird alarms as if they clearly signify danger, nor as if they clearly do not signify danger, perhaps reflecting some ambiguity in interpretation of the calls. These results suggest that squirrel responses to alarm calls are generally based on call familiarity, but that acoustic similarity of an unfamiliar allopatric call to a familiar call also can elicit antipredator behavior. The lack of response to honeyeater alarm calls also supports the hypothesis that call recognition by gray squirrels is dependent on familiarity, rather than simply detection of an acoustic feature common to alarm calls across a variety of avian species.     

A comparison of individual distinctiveness in three vocalizations of the dwarf mongoose (Helogale parvula)

Individual specificity can be found in the vocalizations of many avian and mammalian species. However, it is often difficult to determine whether these vocal cues to identity rise from “unselected” individual differences in vocal morphology or whether they have been accentuated by selection for the purposes of advertising caller identity. By comparing the level of acoustic individuality of different vocalizations within the repertoire of a single species, it is possible to ascertain whether selection for individual recognition has modified the vocal cues to identity in particular contexts. We used discriminant function analyses to determine the level of accuracy with which calls could be classified to the correct individual caller, for three dwarf mongoose (Helogale parvula) vocalizations: contact, snake, and isolation calls. These calls were similar in acoustic structure but divergent in context and function. We found that all three call types showed individual specificity but levels varied with call type (increasing from snake to contact to isolation call). The individual distinctiveness of each call type appeared to be directly related to the degree of benefit that signalers were likely to accrue from advertising their identity within that call context. We conclude that dwarf mongoose signalers have undergone selection to facilitate vocal individual recognition, particularly in relation to the species’ isolation call.     

FORMS OF CALL OVERLAP AND THEIR IMPACT ON ADVERTISEMENT CALL ATTRACTIVENESS TO FEMALES OF THE GRAY TREEFROG,HYLA VERSICOLOR

ABSTRACT

Male gray Lreefrogs, Hyla versicolor, advertise for females in choruses in which calls often overlap. Previous research has demonstrated that such acoustic interference among conspecifics can impair the ability of a male to attract a mate. However, the stimulus set used in those studies was quite limited. Here we performed single-speaker and two-speaker tests of phonotaxis with female Hyla versicolor to explore the impact of different degrees and forms of call overlap on the relative attractiveness of male signals. We found that: (1) overlapped calls are recognized as acceptable signals by females, although they are less attractive than calls that are not overlapped; (2) the relative phase of the overlapping calls matters. When calls were time-shifted by 50% of their pulse-period (180 degree offset), attractiveness of overlapped calls was reduced relative to non-overlapped calls as much as it would be by a reduction in intensity of about 12 dB SPL or a drop in call duration of between one third to one half. A 90 degree phase offset was equivalent to a 3 dB drop in SPL; (3) partial call overlap may not impair call attractiveness if one third or less of the call is overlapped; (4) if the ending portion of a call is overlapped it may impair attractiveness less than if previous segments of a call are obscured; (5) if most (three fourths or more) of a male's calls are free of interference, overlap of his remaining calls does not significantly impair his attractiveness.     

Genetic divergence is more tightly related to call variation than landscape features in the Amazonian frogs Physalaemus petersi and P. freibergi

Behavioural isolation from divergence in male advertisement calls and female preferences is hypothesized to cause genetic divergence and speciation in the Amazonian frogs Physalaemus petersi and P. freibergi, yet the importance of call variation and landscape features in genetic divergence is unresolved. We tested for correlations between genetic divergence at microsatellite loci and (1) call variables; and (2) landscape variables among 10 populations of these frogs. Genetic divergence was not correlated with geographical distance, rivers or elevation. There was a strong positive relationship, however, between genetic divergence and inter‐population differences in one call variable, whine dominant frequency. Effective population sizes varied among sites (range = 15–846) and were often small, suggesting that genetic drift could influence call evolution. Evidence for fine‐scale genetic structure within sites was also found. Our results support the hypothesis that behavioural isolation from divergence in male calls and female preferences causes genetic divergence and speciation.     

Differentiation of vocalizations in bushbabies (Galaginae, Prosimiae, Primates) and the significance for assessing phylogenetic relationships

A comparative bioacustic analysis of vocalizations of the prosimian subfamily Galaginae revealed that morphologically similar sibling taxa within the main groups of the lesser galagos and the greater galagos can be reliably identified phenotypically on the basis of the acoustic structure of their loud call or advertisement call. Results confirm the separation of two distinct species of greater galagos, Galago crassicaudatus and Galago garnettii, and strongly suggest the discrimination of three distinct species from the senegalensis lesser bushbaby group, Galago senegalensis, Galago moholi and Galao zanzibaricus. An investigation of the ontogenetic development of the loud call indicated that it is derived from the infant's isolation call, displaying in all studied bushbaby taxa a fairly similar acoustic pattern. Shared acoustic characters of the loud call among the different taxa as well as the infant's isolation call were used to propose a hypothesis about the phylogenetic affinities in bushbabies. The results seem to be supported by recent fossil records.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.