Benjamin D. Charlton

Female red deer prefer the roars of larger males

Surprisingly little is known about the role of acoustic cues in mammal female mate choice. Here, we examine the response of female red deer (Cervus elaphus) to male roars in which an acoustic cue to body size, the formants, has been re-scaled to simulate different size callers. Our results show that oestrous red deer hinds prefer roars simulating larger callers and constitute the first evidence that female mammals use an acoustic cue to body size in a mate choice context. We go on to suggest that sexual selection through female mating preferences may have provided an additional selection pressure along with male–male competition for broadcasting size-related information in red deer and other mammals.

Female perception of size-related formant shifts in red deer, Cervus elaphus

Little is known about the role of specific acoustic cues in mammal vocal communication systems. Recent advances in bioacoustics allow us to use playback experiments in order to study the perceptual and functional relevance of individual acoustic parameters. In the current study we used re-synthesised male red deer roars in a habituation-discrimination paradigm to determine whether female red deer are sensitive to shifts in formant frequencies corresponding to the natural variation between the vocal tract lengths of a small and large adult red deer male. We found that hinds habituated to a given size variant show a significant dishabituation when they are presented with roars in which the formants have been modified to simulate the other size variant. The significant reduction in behavioural response to a final rehabituation playback shows this was not a chance rebound in response levels. Our results indicate that formants are salient for red deer hinds and that hinds can detect a shift in formant frequencies that has strong potential biological significance. We discuss the possible functions of formant perception in female red deer and more generally in nonhuman mammals.

Vocal cues to identity and relatedness in giant pandas (Ailuropoda melanoleuca).

A range of acoustic characteristics typically carry information on individual identity in mammalian calls. In addition, physical similarities in vocal production anatomy among closely related individuals may result in similarities in the acoustic structure of vocalizations. Here, acoustic analyses based on source-filter theory were used to determine whether giant panda bleats are individually distinctive, to investigate the relative importance of different source-(larynx) and filter-(vocal tract) related acoustic features for coding individuality, and to test whether closely related individuals have similarities in call structure. The results revealed that giant panda bleats are highly individualized and indicate that source-related features, in particular, mean fundamental frequency, amplitude variation per second, and the mean extent of each amplitude modulation, contribute the most to vocal identity. In addition, although individual pairwise relatedness was not correlated with overall acoustic similarity, it was highly correlated with amplitude modulation rate and fundamental frequency range, suggesting that these acoustic features are heritable components of giant panda bleats that could be used as a measure of genetic relatedness. The ecological relevance of acoustically signaling information on caller identity and the potential practical implications for acoustic monitoring of population levels in this endangered species are discussed.

Effect of combined source (F0) and filter (formant) variation on red deer hind responses to male roars

Studying female response to variation in single acoustic components has provided important insights into how sexual selection operates on male acoustic signals. However, since vocal signals are typically composed of independent components, it is important to account for possible interactions between the studied parameter and other relevant acoustic features of vocal signals. Here, two key components of the male red deer roar, the fundamental frequency and the formant frequencies (an acoustic cue to body size), are independently manipulated in order to examine female response to calls characterized by different combinations of these acoustic components. The results revealed that red deer hinds showed greater overall attention and had lower response latencies to playbacks of roars where lower formants simulated larger males. Furthermore, female response to male roars simulating different size callers was unaffected by the fundamental frequency of the male roar when it was varied within the natural range. Finally, the fundamental frequency of the male roar had no significant separate effect on any of the female behavioral response categories. Taken together these findings indicate that directional intersexual selection pressures have contributed to the evolution of the highly mobile and descended larynx of red deer stags and suggest that the fundamental frequency of the male roar does not affect female perception of size-related formant information.

Oestrous red deer hinds prefer male roars with higher fundamental frequencies.

Across vertebrates, the observation that lower-pitched vocalizations are typically associated with larger and/or higher quality males has lead to the widespread belief that inter- and intra-sexual selection will produce male calls with low fundamental frequencies (F0). Here we investigated the response of oestrous red deer hinds to playback of re-synthesized male roars characterized by either higher than average or lower than average F0. We found that hinds prefer higher rather than lower ‘pitched’ roars, providing, to our knowledge, the first evidence of such a bias in nonhuman mammals. Our findings can be interpreted in relation to previous observations that the minimum F0 of roars is positively correlated with male reproductive success in free-ranging red deer stags, and that across Cervids the F0 of male mating calls shows extreme variability. Females showing preferences for higher-pitched roars might derive genetic benefits through more competitive male offspring. Our results emphasize the need for further investigations of female preferences in mammals in order to better understand the extreme variation of F0 values observed in male sexual calls.

Vocal cues indicate level of arousal in infant African elephant roars

Arousal-based physiological changes influence acoustic features of vocalizations in mammals. In particular, nonlinear phenomena are thought to convey information about the callers arousal state. This hypothesis was tested in the infant African elephant (Loxodonta africana) roar, a call type produced in situations of arousal and distress. Ninety-two percent of roars exhibited nonlinear phenomena, with chaos being the most common type. Acoustic irregularities were strongly associated with elevated fundamental frequency values. Roars produced in situations of highest urgency, based on the occurrence of behavioral indicators of arousal, were characterized by the lowest harmonics-to-noise ratio; this indicates low tonality. In addition, roars produced in these situations lasted longer than those produced in contexts of lower presumed urgency. Testing the infant roars for individual distinctiveness revealed only a moderate classification result. Combined, these findings indicate that infant African elephant roars primarily function to signal the callers arousal state. The effective communication of this type of information may allow mothers to respond differentially based on their infants degree of need and may be crucial for the survival of infant African elephants in their natural environment.

VOCAL BEHAVIOUR IN THE ENDANGERED CORSICAN DEER: DESCRIPTION AND PHYLOGENETIC IMPLICATIONS

ABSTRACT Here we present the first description of the vocal behaviour of the Tyrrhenian subspecies of Red Deer, the Corsican Deer. Vocalisations from calves, hinds and stags were recorded. Their acoustic characteristics were analysed in order to contrast these with published data characterising central European Red Deer hind and calve contact calls and Scottish Red Deer stag mating calls. We found that the vocal repertoire of Corsican Deer was very comparable with that of central European and Scottish Red Deer, with the exception of one call type, the harsh roar, absent in the Corsican Deer repertoire. Because Corsican Deer are the smallest subspecies of Red Deer, we expected calls to be characterised by higher spectral components. However, while male roars did have higher vocal tract resonances, consistent with a shorter vocal tract, we found that the fundamental frequency (FO) was much lower than predicted, in fact the lowest recorded in any studied Red Deer subspecies. We also found a strong sexual dimorphism in FO, with male calls approximately twice as low as female calls, suggesting that the low FO observed in Corsican male roars is a result of sexual selection for lower-pitched males. The results of this study emphasise the phenotypic originality of Corsican Deer, and strengthen the case for its conservation. We also argue that future studies should compare the vocal behaviour of Corsican Deer with that of other circum-Mediterranean populations.

Female giant panda (Ailuropoda melanoleuca) chirps advertise the caller's fertile phase

Although female mammal vocal behaviour is known to advertise fertility, to date, no non-human mammal study has shown that the acoustic structure of female calls varies significantly around their fertile period. Here, we used a combination of hormone measurements and acoustic analyses to determine whether female giant panda chirps have the potential to signal the callers precise oestrous stage (fertile versus pre-fertile). We then used playback experiments to examine the response of male giant pandas to female chirps produced during fertile versus pre-fertile phases of the callers reproductive cycle. Our results show that the acoustic structure of female giant panda chirps differs between fertile and pre-fertile callers and that male giant pandas can perceive differences in female chirps that allow them to determine the exact timing of the females fertile phase. These findings indicate that male giant pandas could use vocal cues to preferentially associate and copulate with females at the optimum time for insemination and reveal the likely importance of female vocal signals for coordinating reproductive efforts in this critically endangered species.

Vocal cues to male androgen levels in giant pandas

Little is known about the potential of non-human mammal vocalizations to signal information on the hormonal status of the caller. In the current study, we used endocrine data and acoustic analyses to determine whether male giant panda bleats provide reliable information about the callers current androgen levels. Our results revealed significant relationships between acoustic features of male giant panda bleats and the callers faecal androgen metabolite concentrations. To our knowledge, this constitutes the first demonstration that the acoustic structure of a non-human mammal call has the potential to yield information about the callers current androgen levels. We go on to discuss the anatomical basis for our findings and the potential functional relevance of signalling information on male androgen levels in giant panda sexual communication.

Female koalas prefer bellows in which lower formants indicate larger males

Despite an extensive literature on the role of acoustic cues in mate choice little is known about the specific vocal traits that female mammals prefer. We used resynthesis techniques and playback experiments to examine the behavioural responses of oestrous female koalas, Phascolarctos cinereus, to male bellows in which a specific acoustic cue to body size, the formants, were modified to simulate callers of different body size. Oestrous females looked longer towards, and spent more time in close proximity to, loudspeakers broadcasting bellows simulating larger male koalas. These findings suggest that female koalas use formants (key components of human speech) to select larger males as mating partners, and represent the first evidence of a marsupial mating preference based on a vocal signal. More generally, these results indicate that intersexual selection pressures to lower formants and exaggerate size are present in a marsupial species, raising interesting questions about the evolutionary origins of formant perception.