We investigated the close-range hoo calls of free-ranging lar gibbons in a natural forest habitat of North-eastern Thailand to establish whether there were acoustic differences between the various contexts they were emitted in. Close-range calls of wild gibbons have not received much attention nor have they previously been analysed in detail, in contrast to countless studies on their singing behaviour [42,45-47]. Results revealed that both adult males and females produced context-specific hoo calls, according to the following patterns. First, both sexes were not distinguishable in the acoustic structure of their hoo calls given in specific contexts. For example, measures of peak and low frequency showed that the hoos given in response to raptors were significantly lower than the hoos given as part of a daily duet song, for both males and females. Furthermore, raptor hoos showed significant differences in a number of acoustic parameters compared to many of the other contexts: they were significantly shorter in duration than duet and leopard hoos for both males and females and raptor hoo intensity was significantly lower than the duet hoos, leopard hoos and tiger hoos. In addition, inter-call intervals were significantly longer for raptor hoos than hoos in other contexts, such as tiger, duet, leopard (males and females), and encounter hoos (males only). In fact, raptor hoos were acoustically distinct from all other context, including leopards and tigers, suggesting that they can be classified as a predator-specific call variant. This is in contrast to gibbon loud vocal responses to other predators [37,48]. Due to the gibbons’ relatively small body size raptors are a real threat to infants and juveniles, but probably not to mature gibbons, which may explain the different anti-predator responses by adult gibbons to raptors and cats [48]. Raptor hoos are occasionally also emitted by non-adults and it would therefore be interesting to acoustically compare non-adult and adult hoos in a future study. Raptor hoos were less intense, more widely spread out, and of shorter duration, lower frequency and smaller frequency span than the other hoos, making them the least audible of all hoo variants. This is consistent with the interpretation that raptor hoos are given in circumstances the gibbons may perceive less threatening or to prevent attracting the attention of the predator. For example some passerine bird raptor alarm “seet” calls are difficult to localise [49]. Raptors hear best in the range of 1-4 kHz [50,51], with sensitivity to sounds below and above this being much poorer than primates. Of note, gibbon hoos are consistently below the 1 kHz threshold, with raptor hoos being the lowest frequency of all. The gibbons’ relatively cryptic responses to different predators is consistent with what has been reported in other primates [52,53].
We also found further differences between other hoo contexts. For example, duet hoos tended to be higher in frequency than the other contexts, significantly so when compared with feeding, leopard, tiger and raptor hoos (males) and raptor and tiger hoos (females). The delta frequency of the tiger and leopard hoos tended to be greater than in feeding hoos (females). For encounters, we only obtained recordings from the males, since females did not usually engage in inter-group encounters, but here we also found significant differences in frequency measures if compared to the tiger, leopard and feeding context and significant differences in delta frequency if compared to tiger hoos. The only two contexts that did not differ significantly from one another were tiger and leopard hoos, suggesting that callers perceived these two predators as belonging to the same class.
Apart from contextual effects we also found some significant sex differences in the acoustic structure of hoo calls, despite the absence of sexual dimorphism in this species. Overall, female hoo calls had a significantly lower peak frequency than male hoo calls, in line with an earlier study [42]. Male hoo low frequencies were also significantly higher than female hoos, but we found no differences in delta frequency or intensity between the sexes.
Overall, the data presented here show that the differences between males and females are mainly in terms of frequency-related parameters, while the way that both sexes vocalise to contexts is identical. Among mammals in general, males tend to have lower frequency voices than females, possibly due to larger body size [54] so our findings are surprising. In gibbons, female voices are lower in frequency than males, despite the absence of obvious differences in body size across gibbon species [43]. One possibility is that subtle differences in H. lar body mass may be responsible: males are 0.56 kg (9%) heavier than females [55], though we would expect the opposite relationship with voice frequency if this slight difference in mass was important. Another possibility is that testosterone levels are partly responsible; the singing voices of adult male gibbons with higher testosterone have higher F0 [56], and since males typically have higher testosterone than females, this may better explain our findings. However, the ontogeny of gibbon voice qualities and their relationship with steroid hormones in both sexes require further research.
A DFA revealed intercall interval separated raptor hoos from big cat and duet hoos (females and males), and also encounter hoos (males). Low frequency separated big cat and raptor from duet hoos (females) and delta frequency separated duet, encounter and raptor from big cats (males). Overall, intercall intervals separated big cat and raptor hoos (males and females), while frequency-related measures separated duet from big cat hoos (males and females). For all contexts, there was also considerable overlap, suggesting that other acoustic variables may also contribute to distinguishing call context. For example, intensity appeared to be important but for reasons explained earlier, we omitted it from the final DFA. Also, without being able to fully control for the effects of distance from vocaliser to microphone and amount of vegetation, which could attenuate vocal signals, we remain cautious in interpreting the role of intensity in gibbon hoo communication. A larger sample size of excellent quality hoo recordings would be necessary to explore this preliminary finding.
In future work, it will be important to carry out systematic playback experiments of different hoo variants to determine whether this call type functions as a referential system in the way that their long-distance songs do [37].
The hoo calls described in this paper are virtually indistinguishable to human observers and call variants became only apparent in statistical analyses. Gibbon hoos should therefore be classed as an example of an acoustically graded call type, alongside other primate vocalisations, such as chimpanzee pant hoots [14] or chacma baboon grunts [57]. Social variables, such as an individual’s physical condition or social status, might additionally influence some of the acoustic parameters, which could explain some of the overlap seen in Figure 2. Since hoos are produced in multiple contexts, the motivational states of the callers will likely vary between them, which is particularly the case in predator hoos and inter-group encounter hoos. Some authors interpret such findings as evidence that animal signals do not carry any “meaning” [58,59], but that they serve to influence rather than inform listeners, which subsequently can become conventionalised using linguistic pragmatics [58]. However, while attention-getting vocalisations may not be designed to inform, it is difficult to argue that they do not do so [60], which in our opinion make such findings relevant to understand the origins of “meaningful” communication, including language [26].
Given the obvious selective advantage of ‘labelling’ contexts with distinct signals, why do gibbons and other non-human primates not produce acoustically more discrete signals for different contexts, instead of the subtle acoustic variations within just one call type? We can think of the following possibilities. Firstly, non-human primates may generally be prevented from the required vocal tract control to produce more discrete signals, due to anatomical and neurological constraints, the classic argument to explain limitations in vocal flexibility and control in non-human primates [61]. Gibbons are not alone in this, as there is increasing evidence that subtle changes within the main basic call types can generate meaningful information (see [62]). Secondly, the acoustic variation seen in gibbon hoos (and in other primate vocalisation types) may simply be the basis of acoustic flexibility, similar to human speech, in which subtle acoustic parameters, like pitch, can be important carriers of meaning (e.g. Chinese or Thai: [63]).
Context-specific calling behaviour appears to be widespread and therefore was likely present in the ancestor of modern primates and humans. Similar abilities are found in birds whose distinctive vocal organs are very different, suggesting that context-specific graded vocal behaviour has evolved independently, as did vocal flexibility and vocal learning. Amongst the primates, gibbons are an especially interesting taxon because, like birds, they produce songs, and may have greater vocal tract control than other non-human primates [64]. More research on gibbon song is needed to describe its complexity and the cognitive factors associated with song production [23,37-39,48,64].
Comparing the vocalisations of non-human primates with human language is of interest because of shared phylogeny. So far, the main difference between human and non-human primates is largely in terms of flexibility in production, but less so in terms of comprehension [65-67]. However, ours and other authors’ research show that non-human primates have the capacity to generate considerable acoustic variability, within the constraints of their basic vocal repertoire, which widens their communicative power considerably.