Anim Cogn (2012) 15:999–1006 DOI 10.1007/s10071-012-0527-5
ORIGINAL PAPER
Perception of size-related formant information in male koalas (Phascolarctos cinereus) Benjamin D. Charlton • William A. H. Ellis Rebecca Larkin • W. Tecumseh Fitch
•
Received: 8 February 2012 / Revised: 18 June 2012 / Accepted: 18 June 2012 / Published online: 28 June 2012 Ó Springer-Verlag 2012
Abstract Advances in bioacoustics allow us to study the perceptual and functional relevance of individual acoustic parameters. Here, we use re-synthesised male koala bellows and a habituation–dishabituation paradigm to test the hypothesis that male koalas are sensitive to shifts in formant frequencies corresponding to the natural variation in body size between a large and small adult male. We found that males habituated to bellows, in which the formants had been shifted to simulate a large or small male displayed a significant increase in behavioural response (dishabituation) when they were presented with bellows simulating the alternate size variant. The rehabituation control, in which the behavioural response levels returned to that of the last playbacks of the habituation phase, indicates that this was not a chance increase in response levels. Our results provide clear evidence that male koalas perceive and attend to size-related formant information in their own speciesspecific vocalisations and suggest that formant perception is a widespread ability shared by marsupials and placental mammals, and perhaps by vertebrates more widely.
B. D. Charlton (&) W. Tecumseh Fitch Department of Cognitive Biology, University of Vienna, Vienna, Austria e-mail:
[email protected] W. A. H. Ellis Koala Research Centre of Central Queensland, CQ University, Rockhampton, QLD 4702, Australia R. Larkin Department of Environment and Resource Management, Moggill Koala Hospital, Bellbowrie, Brisbane, QLD 4070, Australia
Keywords Koalas Vocal communication Formant frequencies Habituation–dishabituation Playback experiments
Introduction Exhaustive empirical study has shown that formants—the resonance frequencies of the vocal tract—are the key acoustic parameters underlying phonemic variation and vowel identity in human speech (Fant 1960; Lieberman and Blumstein 1988). The perceptual relevance and functions of formants in nonhuman mammal vocal communication systems, however, remain less well understood. Recent work on a range of mammals has shown that formant variation potentially provides receivers with important acoustic information on the caller’s body size (Fitch 1997; Riede and Fitch 1999; Vannoni and McElligott 2008; Sanvito et al. 2007; Harris et al. 2006; Reby and McComb 2003; Charlton et al. 2009b, 2011a) with lower and more closely spaced formant frequencies indicative of longer vocal tracts and larger body sizes. Despite speculation on the possible functions of formant frequencies in animal vocalisations though, there have been few attempts to test whether or not other members of the same species actually perceive this information, i.e., by demonstrating spontaneous responses by conspecifics to formant changes in the species’ own natural vocalisations. In fact, to our knowledge, this crucial step in investigating the adaptive significance of formants has so far only been conducted in four nonhuman mammal species, rhesus macaques (Macaca mullata) (Fitch and Fritz 2006; Ghazanfar et al. 2007), red deer (Cervus elaphus) (Reby et al. 2005; Charlton et al. 2007a, b, 2008a, b), dogs (Canis familiaris) (Taylor et al. 2010), and giant pandas
123
1000
(Ailuropoda melanoleuca) (Charlton et al. 2010). The diverse range of mammals used in these studies, however, suggests that a latent ability to perceive formant shifts in species-typical calls might be present throughout nonhuman mammals. If this is the case, then formants may also be expected to have functional importance in a range of nonhuman mammal species-specific vocal communication systems. Male koalas (Phascolarctos cinereus) bellow much more frequently during the breeding season (Smith 1980; Mitchell 1990; Ellis et al. 2011), strongly suggesting that these calls are linked to reproduction. Recent work has shown that the formant frequency spacing in male bellows provides reliable information on the caller’s body size (Charlton et al. 2011a). In addition, male and female koalas can discriminate between individuals on the basis of their bellows (Charlton et al. 2011b), suggesting that they are able to attend to the finer acoustic structure of these vocalisations, such as the formant frequencies. Since body size is a key determinant of male competitive ability in mammals (Owings and Morton 1998), it is reasonable to predict that formants will be perceptually and functionally relevant to male koalas. Indeed, if formants are salient to male koalas, then decisions could be made to avoid escalating contests with potentially more dangerous rivals using these acoustic cues where lower formants indicate larger males. Theoretical and technical progress in the field of bioacoustics now allows for the manipulation of specific acoustic parameters whilst holding all others constant, so that their perceptual and/or functional relevance can be determined using playback experiments (e.g. Reby et al. 2005; Fitch and Kelley 2000; Charlton et al. 2007b; Taylor et al. 2010). Here, we use re-synthesised koala bellows originating from eight different males and a habituation– dishabituation paradigm (Eimas et al. 1971; Charlton et al. 2007a; Swartz 1983) to test the hypothesis that male koalas perceive and respond to a shift in formant frequency spacing corresponding to the natural variation in body size between a small and large adult male. More specifically, we predict that after showing a diminishing response (habituating) to bellows in which the formant frequency spacing corresponds to the same size variant, male koalas would show a renewal of response levels (dishabituate) to a shift in formant frequency spacing corresponding to the alternate size variant. We also predict that male koalas will show more attention to bellows simulating large males. Perceptual abilities such as these could allow male koalas to acoustically assess the body size of rival males during the breeding season and would provide further evidence that formant perception in species-typical calls is a widespread ability shared by marsupials and placental mammals.
123
Anim Cogn (2012) 15:999–1006
Methods Experimental site and animals The study was carried out at the Queensland Parks and Wildlife Service Moggill Koala Hospital (MKH), Moggill, Brisbane, Australia, during the 2011 breeding season (September–December). The subjects in the experiment were 16 wild-sourced adult male koalas all individually housed in enclosures measuring approximately 2.0 9 3.0 9 3.0 m. Tooth wear was used to verify the adult status of the subjects. Selection of bellows for re-synthesis To create the playback stimuli, we selected bellows of comparable duration (22.1 ± 3.9 s) from eight adult male koalas aged between 3 and 11 years (mean = 7.5 years). These males were recorded by BC at Lone Pine Koala Sanctuary (Brisbane, Australia) and, therefore, were unfamiliar to the resident wild-sourced koalas at MKH. In addition, to ensure that our playback stimuli adequately represented this class of stimuli (Wiley 2003), we selected bellows characterised by a range of fundamental frequencies (from 19.3 to 40.0 Hz). The original recordings were made using a Sennheisser ME67 directional microphone and a Zoom H4 N portable solid-state digital recorder (sampling rate, 44.1 kHz; amplitude resolution, 16 bits) at distances ranging between 2 and 10 m. These recorded vocalisations were transferred onto an Apple Macintosh MacBook Pro computer and saved in WAV format at 16 bits amplitude resolution, 44.1 kHz sampling rate. Acoustic analysis of playback stimuli Male koala bellows are characterised by a series of inhalation and exhalation sections (Smith 1980) (see Fig. 1). Because the formant frequency spacing of the later inhalation sections of bellows is more predictive of male body size than that of the exhalation or initial inhalation phases (Charlton et al. 2011a), we extracted the formant frequencies of these phases to determine the appropriate factors by which to re-synthesise the playback stimuli. The frequency values of the first six formants were measured using Linear Predictive Coding (LPC; ‘To Formants (Burg)’ command in Praat 5.1.03 DSP package, www. praat.org) using the following analysis parameters: time step, 0.01 s; window analysis, 0.03 s; maximum formant value, 2,300 Hz; maximum number of formants, 6; and pre-emphasis, 50 Hz. Visual inspection of spectrograms allowed us to confirm that the lower six formants of each bellow fell below the maximum formant value setting (of 2,300 Hz). The other analysis settings were established by previous studies (Charlton et al. 2011a, b). The formant
Anim Cogn (2012) 15:999–1006
Relative amplitude (dB)
(a)
(b)
0.82
0
Introductory phase
Initial inhalation phase
Exhalation phase
Later inhalation phase
- 0.99 4000
Frequency (Hz)
Fig. 1 Waveform (a) and spectrogram (b) of a male koala bellow (spectrogram settings: FFT method; window length, 0.09 s; time step = 0.002 s; frequency step = 10 Hz; Gaussian window shape; dynamic range = 50 dB). Male bellows are characterised by an introductory phase that is followed by a continuous series of inhalations and shorter exhalations
1001
0 29.7
0
Time (s)
frequency values were then used to estimate the formant spacing (DF) achieved during each bellow. To do this, the measured formant values were regressed against those that would be expected in a straight uniform tube closed at one end (the glottis) and open at the other end (the mouth) (sensu Reby and McComb 2003). This gave us an original DF range of 406.7–324.7 Hz for bellows used to create the re-synthesised playback stimuli. Calculation of re-synthesis factors A previous study on 20 adult male koalas showed that DF for the later inhalation sections of male bellows ranged between 406.7 Hz for the smallest male (with an apparent vocal tract length of 43.8 cm) and 297.5 Hz for the largest (with an apparent vocal tract length of 58.3 cm) (Charlton et al. 2011a). This study also showed that no other acoustic features of male bellows consistently vary according to the caller’s body size (Charlton et al. 2011a). Thus, in order to realistically simulate variation in adult male body size, we re-synthesised bellows to create large and small adult male size variants with DFs of 300 and 400 Hz, respectively (see Fig. 2). The re-synthesis factor (k) required to change DF to these values was calculated by dividing the intended target values, 300 or 400, by the originally measured values for each bellow, for example, if the measured DF was 350 Hz and we wanted to change it to represent a small male, then k would be 400/350 = 1.14. Re-synthesis procedure To preserve the relative values of formants across bellows, and the realism of the stimuli, entire calls were
re-synthesised. Formant modification was achieved using a Praat script that incorporated a PSOLA (Pitch Synchronous Overlap and Add)-based algorithm (Moulines and Charpentier 1990). This script initially multiplies the fundamental frequency by k and duration by 1/k using PSOLA, before re-sampling at the original sampling rate multiplied by k, and then playing the samples at the original sampling frequency. This effectively speeds up or slows down the recording, compressing or expanding the entire sound spectrum. As F0 had already been shifted by k and duration by 1/k, the final step resets the pitch and duration to their original values, so that DF is changed by the factor (k) whilst leaving all other acoustic parameters unchanged. The mean relative intensity values for all the bellow stimuli were then standardised to 65 dB using the ‘scale intensity’ command in Praat. Playback experiments In order to evaluate the ability of males to perceive the re-synthesised shift in formant frequencies, we used a habituation–dishabituation paradigm (Eimas et al. 1971; Charlton et al. 2007a; Swartz 1983). In this paradigm, the subject is initially habituated to one stimulus of type A though repeated exposure before a dishabituation stimulus of type B is provided. A renewed response to stimulus B indicates an ability to discriminate the factor that changed between stimuli of type A and B. Finally, a re-habituation stimulus is provided by a re-exposure to a stimulus of type A to control for the possibility that dishabituation was due to a spontaneous recovery of pre-habituation response levels (Rendall et al. 1996; Reby et al. 2001; Charlton et al. 2007a, 2009a).
123
1002
Anim Cogn (2012) 15:999–1006
Fig. 2 Spectrograms of an inhalation section of a male bellow to illustrate the formant modification (spectrogram settings: FFT method; window length, 0.05 s; time step = 0.004 s; frequency step = 20 Hz; Gaussian window shape; dynamic range = 50 dB). The formants are labelled F1–F6. Note that the formant frequency values and spacing of the original inhalation section (a) have been lowered to create the large male size variant (b) and raised to create the small male size variant (c)
(a)
Original bellow
2800
Frequency (Hz)
F6 F5
F4 F3 F2 F1 0 0
0.5039
Time (s)
(b)
(c)
Large male size variant
2800
Small male size variant
2800
F6 F5 F4
Frequency (Hz)
Frequency (Hz)
F6
F5
F4
F3 F3 F2 F1 0
0 0
0.5039
Time (s)
The playback experiments were conducted in the mornings between 0900 and 1100 hours. Playback sequences were only initiated when subjects were settled and awake, and their attention was directed away from the playback speaker. The playback stimuli were broadcast using a Chaiyo Focus 505 loudspeaker (Taipei, Taiwan) at mean sound pressure levels sounding equivalent to that of naturally bellowing males of 75 dB (determined using a Radio Shack Sound Level Meter, set for C-weighted fast response and measured 1 m from the source). The playback speaker was positioned 5 m from the subject and at a height of 1.5 m from the ground. Each subject’s behaviour was videotaped during the experimental period using a Canon LEGRIA FS20 digital video camcorder mounted on a tripod. Playback sequences The playback sequences consisted of seven different bellows, each separated by 60 s and taken from the same
123
F2 F1 0
0.5039
Time (s)
individual male. The formant frequencies of the first five bellows comprised the habituation phase (H1–H5), and the seventh bellow, the rehabituation stimulus (RH), had been shifted to simulate the same size variant (large or small adult male). The sixth bellow of the playback sequence, the dishabituation stimulus (DH), had its formants shifted to simulate the alternate size variant. By using different bellows to create the playback sequences, we ensured that males became habituated to the sizerelated formant information and not to the repetition of the same call. Consequently, if the subject’s behavioural response significantly increased to the dishabituation stimulus (DH) and then fell back again after the rehabituation stimulus (RH), we concluded that the sixth and seventh bellows were perceived as different from the preceding stimuli and, therefore, that subjects perceived the change in size-related formant information. The bellows used to create the playback sequences were ordered, so that bellow durations decreased across the sequence.
Anim Cogn (2012) 15:999–1006
Behavioural and data analysis The videotapes were analysed frame by frame (frame = 0.04 s) using Gamebreaker v7 digital video analysis system for Mac OS 10.6. In order to quantify each subject’s response to the stimuli, the duration of all looks given to the playback source were measured. More precisely, a look was defined as starting as a subject raised or turned its head to face the speaker, having previously faced away, and ended when the head started to move away from the speaker position. Sometimes subjects were already looking towards the speaker when one of the bellows of a sequence was broadcast. In these cases, looking behaviour began at the onset of the playback. A movement leading to the subject looking away from the speaker position or the subject closing their eyes defined the end of a look. Because the data were not normally distributed and could not be normalised for all the response variables, nonparametric statistics were used to examine the data. Wilcoxon Signed Ranks tests were used to detect significant differences in mean looking duration between bellows H5 and DH, to test for dishabituation, and DH and RH, to test for rehabituation. In addition, to investigate whether males responded differentially to the two size variant conditions (large versus small male), we used a Mann–Whitney U test to determine whether mean looking duration to H1–H5 differed significantly between males according to the size variant used across the habituation phase. Finally, we entered the male exemplar used to create the playback stimuli as a factor (comprising eight levels) in a Kruskal–Wallis test to determine whether the origin of our re-synthesised playback stimuli affected overall response to H1–H5, DH, and RH (Kroodsma et al. 2001). One-tailed probability values are quoted when examining differences between H5 and DH, and DH and RH, because of our strong directional a priori hypothesis (Kimmel 1957; Ruxton and Neuhauser 2010). All other tests are two-tailed. It is worth noting, however, that statistically significant results obtained using one-tailed tests would have remained significant with a two-tailed approach. All statistical analyses were conducted using IBM SPSS statistics version 19, and significance levels were set at P = 0.05.
Results The male exemplar used to create the playback stimuli had no effect on mean looking duration to H1–H5 (v2 = 8.91, df = 7, P = 0.259), DH (v2 = 10.74, df = 7, P = 0.150), and RH (v2 = 7.37, df = 7, P = 0.391), confirming that the origin of our re-synthesised playback stimuli did not affect overall response. Given these results, it is justifiable to treat the 16 stimuli as providing independent observations. The results show that there was a significant increase in response duration between the dishabituation playback (mean ± SD: DH = 35.26 ± 27.75 s) and the last playback of the habituation phase (mean ± SD: H5 = 16.94 ± 17.72 s) (t = -4.52, df = 15, P = 0.001). In addition, a significant reduction in response duration between the dishabituation playback (mean ± SD: DH = 35.26 ± 27.75 s) and the rehabituation playback (mean ± SD: RH = 14.86 ± 21.13 s) was observed (t15 = 4.87, df = 15, P = 0.001), with the response levels falling back to that of the last habituation playback (H5) (see Fig. 3). Finally, the size variant used to habituate subjects had no affect on mean looking duration to H1–H5 (U = 23, N = 8, 8, P = 0.345), indicating that male koalas did not respond differentially to male bellows simulating different size callers.
100 P = 0.001 P = 0.001 |-------||-------|
80
Looking duration (s)
This ensured that subjects would not dishabituate to a sudden increase in bellow duration. In addition, the size variants used to provoke habituation and dishabituation were alternated, allowing us to create 16 unique playback sequences (from the 8 male exemplars) to present to our 16 male subjects. This meant that each size variant condition (large or small) for a given bellow was only used once in the experiment.
1003
60
40
20
0 H1
H2
H3
H4
H5
DH
RH
Playback
Fig. 3 Looking responses to the habituation–dishabituation playback sequences (N = 16). The box plots presented here (which illustrate the median, inter-quartile range, and 95 % confidence intervals) show an initial diminution of response levels across the habituation phase (H1–H5) followed by a renewal of response levels to the dishabituation stimulus (DH). Finally, a decrease in response levels after the rehabituation stimulus (RH), returning to that of the last playback of the habituation phase (H5), is seen. ‘o’ denotes an outlier
123
1004
Discussion This study provides the first evidence that a marsupial perceives and attends to formant shifts in its own speciesspecific vocalisations. Male koalas showed a significant renewal of response when presented with a bellow, in which the formant frequencies had been shifted from their previous values during the habituation phase. The significant fall back in behavioural response to the rehabituation control indicates that this was not a chance rebound in response levels. Accordingly, our findings show that male koalas perceive and respond to changes in formant frequencies in conspecific vocalisations within the natural range of variation, and that they find these differences significant enough to warrant dishabituation. A diverse range of nonhuman animals can be trained to discriminate between human speech sounds, which differ primarily in formant frequency (Baru 1975; Hienz et al. 1981, 1996, 2004; Hienz and Brady 1988; Burdick and Miller 1975; Sinnott 1989; Sinnott and Kreiter 1991; Sinnott and Mosteller 2001; Sinnott et al. 1997; Sommers et al. 1992; Dooling and Brown 1990). However, if formants have functional significance to a given species, then individuals should react to variation in this acoustic parameter in their own species-typical calls and without training, i.e., spontaneously. Thus, the type of spontaneous perception we have demonstrated in the current study (as opposed to that displayed by animals that have been trained to react to formant shifts) provides the strongest indication of functional significance within a given species’ vocal communication system. Because formants are reliable indicators of male body size in koalas (Charlton et al. 2011a), they have the potential to provide important information to other male koalas about the body size of rivals during the breeding season. Indeed, body size is a primary determinant of male mating success in this species (Ellis and Bercovitch 2011), and acoustic cues to body size fulfil important functional roles in male–male competition in other animals (Reby et al. 2005; Davies and Halliday 1978; Hardouin et al. 2007). Hence, there are good reasons to expect male koalas to make perceptual use of formants as cues to size in male bellows, and we might expect them to show more attention to bellows simulating larger, and presumably more threatening, rivals. Interestingly though, mean looking duration to the five bellows (H1–H5) used during the habituation phase of playback sequences did not differ according to the value of the formant frequency spacing, indicating that males were equally attentive to both size variant conditions. Notwithstanding this, other behavioural responses to size-related formant information (such as avoidance or approach behaviours, or differences in vocal response) may become apparent in free-ranging animals
123
Anim Cogn (2012) 15:999–1006
that are actively competing for females during the breeding season. Future studies should use re-synthesis tools and playbacks to present free-ranging koalas with bellows simulating different sized rivals, in order to further explore the role of formants as size cues in this species intra-sexual communication. Recent work on humans suggests that an underlying mechanism for processing size-related formant information exists in the medial geniculate body of the thalamus, but also suggests that similar auditory processes may be responsible for fundamental frequency processing (von Kriegstein et al. 2006). Given that humans are able to derive fundamental frequency purely from harmonic spacing in band passed speech (Schouten 1940), and also that cotton-top tamarins (Saguinus oedipus) appear to be able to derive the pitch of species-specific long calls lacking the fundamental frequency or second harmonic (Weiss and Hauser 2002), the perception of size-related information could perhaps be similarly derived using a ‘fundamental formant’ equivalent to the average spacing of the formants. Male koalas could attend to the re-scaling of many formants or to only a few (the ones with the most acoustic energy) to obtain information on body size. Future work in which only specific formants are modified or in which the lower or upper formants are band passed could explore these possibilities, and would contribute to our understanding of exactly how male koalas perceive sizerelated formant information. In conclusion, formants are ubiquitous in the vocalisations of nonhuman mammals (for a review see Taylor and Reby 2010), but up until now, spontaneous perception of formant shifts in species-typical vocalisations had only been demonstrated unequivocally (using re-synthesised calls in which only the formants differ) in rhesus macaques (M. mullata) (Fitch and Fritz 2006; Ghazanfar et al. 2007), red deer (C. elaphus) (Reby et al. 2005; Charlton et al. 2007a, b, 2008a, b), dogs (C. familiaris) (Taylor et al. 2010), and giant pandas (A. melanoleuca) (Charlton et al. 2010). Since formants are fundamental to vowel perception in human speech, investigating their perceptual and functional relevance in nonhuman animals is directly relevant to the evolution of spoken language (Fitch 2010). By showing that a marsupial responds to formant variation in its own species-typical calls, our findings suggest that formants are likely to play an important and evolutionarily ancient functional role (conveying information about the caller’s phenotype) across a broad range of mammalian species and possibly in the vocal communication systems of many other vertebrates. Playback experiments to determine how free-ranging male koalas use size-related formant information in bellows to make judgements on whether or not to escalate agonistic interactions with prospective rivals are now required.
Anim Cogn (2012) 15:999–1006 Acknowledgments We would like to thank Peter Theilemann and all the volunteers and staff at MKH for patiently allowing BC to complete the playback experiments. This work follows the Association for the study of Animal Behaviour/Animal Behaviour Society guidelines for the use of animals in research and was approved by the University of Queensland Animal Ethics Committee (approval number SAS/227/10). BC was supported by a University of Vienna startup grant and a European Research Council Advanced Grant SOMACCA (No. 230604) awarded to WTF.
References Baru AV (1975) Discrimination of synthesized vowels [a] and [i] with varying parameters (fundamental frequency, intensity, duration and number of formants) in dog. In: Fant G, Tatham MAA (eds) Auditory analysis and perception of speech. Academic, New York, pp 91–101 Burdick CK, Miller JD (1975) Speech perception by the chinchilla: discrimination of sustained/a/and/i/. J Acoust Soc Am 58(2): 415–427 Charlton BD, Reby D, McComb K (2007a) Female perception of sizerelated formants in red deer, Cervus elaphus. Anim Behav 74:707–714 Charlton BD, Reby D, McComb K (2007b) Female red deer prefer the roars of larger males. Biol Lett 3:382–385 Charlton BD, McComb K, Reby D (2008a) Free-ranging red deer hinds show greater attentiveness to roars with formant frequencies typical of young males. Ethology 114:1023–1031 Charlton BD, Reby D, McComb K (2008b) Effect of combined source (F0) and filter (formant) variation on red deer hind responses to male roars. J Acoust Soc Am 123(5):2936–2943 Charlton BD, Huang Y, Swaisgood RR (2009a) Vocal discrimination of potential mates by female giant pandas (Ailuropoda melanoleuca). Biol Lett 5:597–599 Charlton BD, Zhihe Z, Snyder RJ (2009b) The information content of giant panda, Ailuropoda melanoleuca, bleats: acoustic cues to sex, age and size. Anim Behav 78:893–898 Charlton BD, Zhihe Z, Snyder R (2010) Giant pandas perceive and attend to formant frequency variation in male bleats. Anim Behav 79(6):1221–1227 Charlton BD, Ellis WAH, McKinnon AJ, Brumm J, Nilsson K, Fitch WT (2011a) Perception of male caller identity in koalas (Phascolarctos cinereus): acoustic analysis and playback experiments. PLoS One 6:e20329 Charlton BD, Ellis WAH, McKinnon AJ, Cowin GJ, Brumm J, Nilsson K, Fitch WT (2011b) Cues to body size in the formant spacing of male koala (Phascolarctos cinereus) bellows: honesty in an exaggerated trait. J Exp Biol 214:3414–3422 Davies NB, Halliday T (1978) Deep croaks and fighting assessment in toads (Bufo bufo). Nature 274:683–685 Dooling RJ, Brown SD (1990) Speech-perception by budgerigars (Melopsittacus-Undulatus)—spoken vowels. Percept Psychophys 47(6):568–574 Eimas PD, Siqueland ER, Jusczyk P, Vigorito J (1971) Speech perception in infants. Science 171(3968):303–306 Ellis WAH, Bercovitch FB (2011) Body size and sexual selection in the koala. Behav Ecol Sociobiol 65(6):1229–1235 Ellis WAH, Bercovitch FB, FitzGibbon S, Roe P, Wimmer J, Melzer A, Wilson R (2011) Koala bellows and their association with the spatial dynamics of free-ranging koalas. Behav Ecol 22(2):372–377 Fant G (1960) Acoustic theory of speech production. Mouton, The Hague
1005 Fitch WT (1997) Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. J Acoust Soc Am 102(2):1213–1222 Fitch WT (2010) The evolution of language. Cambridge University Press, Cambridge Fitch WT, Fritz JB (2006) Rhesus macaques spontaneously perceive formants in conspecific vocalisations. J Acoust Soc Am 120(4):2132–2141 Fitch WT, Kelley JP (2000) Perception of vocal tract resonances by whooping cranes Grus americana. Ethology 106(6):559–574 Ghazanfar A, Turesson H, Maier J, Vandinther R, Patterson RD, Logothetis N (2007) Vocal-tract resonances as indexical cues in rhesus monkeys. Curr Biol 17(5):425–430 Hardouin LA, Reby D, Bavoux C, Burneleau G, Bretagnolle V (2007) Communication of male quality in owl hoots. Am Nat 169(4):552–562 Harris TR, Fitch WT, Goldstein LM, Fashing PJ (2006) Black and white colobus monkey (Colobus guereza) roars as a source of both honest and exaggerated information about body mass. Ethology 112(9):911–920 Hienz RD, Brady JV (1988) The acquisition of vowel discriminations by nonhuman primates. J Acoust Soc Am 84(1):186–194 Hienz RD, Sachs MB, Sinnott JM (1981) Discrimination of steadystate vowels by blackbirds and pigeons. J Acoust Soc Am 70(3):699–706 Hienz RD, Aleszczyk CM, May BJ (1996) Vowel discrimination in cats: thresholds for the detection of second formant changes in the vowel. J Acoust Soc Am 100(2):1052–1058 Hienz RD, Jones AM, Weerts EM (2004) The discrimination of baboon grunt calls and human vowel sounds by baboons. J Acoust Soc Am 116(3):1692–1697 Kimmel HD (1957) Three criteria for the use of one-tailed tests. Psychol Bull 54(4):351–353 Kroodsma DE, Byers BE, Goodale E, Johnson S, Liu WC (2001) Pseudoreplication in playback experiments, revisited a decade later. Anim Behav 61:1029–1033 Lieberman P, Blumstein SE (1988) Speech physiology, speech perception, and acoustic phonetics. Cambridge University Press, Cambridge Mitchell P (1990) Social behaviour and communication of koalas. In: Lee AK, Handasyde KA, Sanson GD (eds) Biology of the koala. Surrey Beatty, Chipping Norton, pp 151–170 Moulines E, Charpentier F (1990) Pitch synchronous waveform processing techniques for text-to-speech synthesis using diphones. Speech Commun 9:453–467 Owings DH, Morton ES (1998) Animal vocal communication: a new approach. Cambridge University Press, Cambridge Reby D, McComb K (2003) Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Anim Behav 65:519–530 Reby D, Hewison M, Izquierdo M, Pepin D (2001) Red deer (Cervus elaphus) hinds discriminate between the roars of their current harem-holder stag and those of neighbouring stags. Ethology 107(10):951–959 Reby D, McComb K, Cargnelutti B, Darwin C, Fitch WT, CluttonBrock TH (2005) Red deer stags use formants as assessment cues during intrasexual agonistic interactions. Proc R Soc Lond Ser B Biol Sci 272:941–947 Rendall D, Rodman PS, Emond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015 Riede T, Fitch WT (1999) Vocal tract length and acoustics of vocalization in the domestic dog (Canis familiaris). J Exp Biol 202(20):2859–2867 Ruxton GD, Neuhauser M (2010) When should we use one-tailed hypothesis testing? Methods Ecol Evol 1(2):114–117
123
1006 Sanvito S, Galimberti F, Miller EH (2007) Vocal signalling in male southern elephant seals is honest but imprecise. Anim Behav 73:287–299 Schouten JF (1940) The perception of pitch. Philips Tech Rev 5:286–294 Sinnott JM (1989) Detection and discrimination of synthetic English vowels by Old World monkeys (Cercopithecus, Macaca) and humans. J Acoust Soc Am 86(2):557–565 Sinnott JM, Kreiter NA (1991) Differential sensitivity to vowel continua in Old-World Monkeys (Macaca) and humans. J Acoust Soc Am 89(5):2421–2429 Sinnott JM, Mosteller KW (2001) A comparative assessment of speech sound discrimination in the Mongolian gerbil. J Acoust Soc Am 110(4):1729–1732 Sinnott JM, Street SL, Mosteller KW, Williamson TL (1997) Behavioral measures of vowel sensitivity in Mongolian gerbils (Meriones unguiculatus): effects of age and genetic origin. Hear Res 112(1–2):235–246 Smith M (1980) Behaviour of the koala, Phascolarctos cinereus (Goldfuss), in captivity. III. Vocalizations. Aust Wildl Res 7:13–34
123
Anim Cogn (2012) 15:999–1006 Sommers MS, Moody DB, Prosen CA, Stebbins WC (1992) Formant frequency discrimination by Japanese Macaques (Macaca fuscata). J Acoust Soc Am 91(6):3499–3510 Swartz KB (1983) Species discrimination in infant pigtail macques with pictorial stimuli. Dev Psychobiol 16(3):219–231 Taylor A, Reby D (2010) The contribution of source-filter theory to mammal vocal communication research. J Zool 280(3):221–236 Taylor AM, Reby D, McComb K (2010) Size communication in domestic dog, Canis familiaris, growls. Anim Behav 79:205–210 Vannoni E, McElligott AG (2008) Low frequency groans indicate larger and more dominant fallow deer (Dama dama) males. PLoS One 3(9):e3113 von Kriegstein K, Warren JD, Ives DT, Patterson RD, Griffiths TD (2006) Processing the acoustic effect of size in speech sounds. NeuroImage 32(1):368–375 Weiss DJ, Hauser MD (2002) Perception of harmonics in the combination long call of cottontop tamarins, Saguinus oedipus. Anim Behav 64:415–426 Wiley RH (2003) Is there an ideal behavioural experiment? Anim Behav 66:585–588
