1 Introduction

The vocal repertoires of mammals usually consist of a fixed number of calls, some of which are closely linked to particular contexts. Though not to the same extent as humans, other mammals have been documented to emit highly modifiable calls with a cognitively rich set of meanings (Seyfarth and Cheney 2010). Fixed vocal production coupled with modifiable context emission and comprehension may have been homologous traits present in our prelinguistic ancestor, since they appear to be present in a wide array of taxonomic groups. Seyfarth and Cheney (2012) suggest that the common ancestor of Old World monkeys, apes, and humans had limited vocal production and open-ended comprehension, and by making comparisons with our closest living relatives, we can further illustrate the implications of theories concerning language evolution.

Our limitless repertoire of sound combinations and capacity for vocal learning is unmatched in the animal kingdom. To date, songbirds have been the focus of vocal learning studies in non-human animals, and evidence in mammals has been restricted to species of cetaceans, pinnipeds, elephants, and bats (Lattenkamp and Vernes 2018). Surprisingly, our closest living relatives, the non-human primates, are deficient in their ability to learn new vocalizations. This inability may be a result of a lack of neuronal potential required for vocal learning although the vocal tract is speech-ready (Fitch et al. 2016). Vocal production is, for the most part, highly constrained in non-human animals, and mammalian repertoires usually consist of a variety of grunts, threatening vocalizations, alarm calls, and screams (Seyfarth and Cheney 2012). Comparing the diverse array of vocal repertoires and communication across taxa is one way to identify the selective pressures behind vocal complexity and the biological underpinnings of language-specific traits. Finding an appropriate measure of vocal complexity, however, is challenging when there are no standard methods for quantifying, classifying, or describing vocal repertoires.

2 Measuring Vocal Complexity

2.1 Vocal Repertoire Size

Although communication is undoubtedly multimodal in nature, across the modalities the number of distinct signals or signaling units can be used as a representative of communicative complexity (Peckre et al. 2019). For studies investigating the modality of acoustic communication, one possible metric of vocal complexity is repertoire size. Repertoire size is defined by the number of call types produced by a species or population (Peckre et al. 2019). Therefore, repertoire size is a strictly numeric measure unable to provide any information concerning the function or usage of the calls that constitute them. Variable data collection methods among studies constrain the ability to make exact comparisons across species and genera, further limiting the informative value of repertoire size alone. In addition, comparing repertoire size leaves out the identification of species-specific calls that may have evolved.

Hohmann (1991) carried out a comparative analysis of the vocal repertoires of four species of Old World monkey (Macaca radiata, Macaca silenus, Presbytis johnii, Presbytis entellus). For the species under Hohmann’s (1991) investigation, previous reports of their vocalizations were very fragmented. To bypass this challenge and make accurate comparisons, Hohmann (1991) recorded calls from these four species and used the same methods to analyze the call recordings. Even though this study involved an intensive classification of the vocal repertoire of four different species, emphasis was placed on comparisons of the frequencies of call type emission and vocal activity among sex/age classes, rather than identifying species-specific calls or call usage. Therefore, the extent to which vocal complexity among the four species was investigated is limited.

2.2 Identifying Homologous and Derived Calls

Gustison et al. (2012) proposed that the identification of homologous (acoustically similar calls shared between species) and derived vocalizations (acoustically unique to a species) among closely related species can be used as a measure of vocal complexity. By focusing on the identification of acoustically homologous calls (Hohmann 1991; Gustison et al. 2012) and identifying species-specific derived calls, researchers are not constrained by the variable methods used across studies to classify vocal repertoires. Furthermore, comparing homologous and derived vocalizations among closely related species is essential in the identification of phylogenetic, social, and ecological factors influencing varying degrees of vocal complexity.

To date, few studies in non-human primates have approached investigations on vocal complexity through the identification of derived calls. Kudo (1987) compared the vocal behavior of mandrills (Mandrillus sphinx) to savannah baboons (Papio spp.) and geladas (Theropithecus gelada) and found that differences among the three species’ vocal behavior were due to the ecological pressures associated with the attenuation of sound in forest versus savannah habitats. More recently, Gustison et al. (2012) identified the homologous and derived vocalizations in two closely related species, geladas and chacma baboons (Papio ursinus). In this comparison, derived vocalizations were uttered in social and reproductive contexts unique to a species, suggesting that differences in sociality and reproductive ecology were the driving factors in the evolution of these species-specific vocalizations.

3 Understanding the Evolution of Vocal Complexity

To understand the evolution of vocal complexity, it is necessary to make comparisons across closely related species. Although broader interspecies comparisons do exist and reveal some interesting patterns (McComb and Semple 2005), in-depth investigations among closely related species allow researchers to tease apart which factors have driven the evolution of communication (Bouchet et al. 2013). Macaques may be an ideal genus for investigations of vocal complexity because of several characteristics. Vocalizations in the Macaca genus have garnered a considerable amount of attention over the years, and the literature is rich enough to make detailed comparisons across many species. In addition, the genus is the most geographically widespread and behaviorally diverse genus of non-human primate because macaques display a high range of interspecific variation and inhabit the greatest range of habitats (Thierry et al. 2000). By documenting the diversity across the macaques through a comparative perspective and the identification of derived calls, I can investigate how potential selective pressures, like phylogeny, sociality, and ecology, shape which calls are conserved or vary in the vocal repertoires of the genus.

The effects of phylogeny, sociality, and ecology are essential in the explorations on the evolution of vocal complexity (Freeberg et al. 2012). Phylogeny may act as a starting point for mapping the evolutionary convergence of vocal characters. For example, complex oropendola bird songs are conserved and relatively invariant among the three genera (Price and Lanyon 2002), and primate vocalizations appear to be largely genetically predetermined (Newman and Symes 1982). It is widely accepted in the literature that sociality may be an essential driving factor in species with high degrees of vocal complexity (Blumstein and Armitage 1997; Wilkinson 2003; Freeberg 2006; Furrer and Manser 2009). In their investigation on Tonkean macaques (Macaca tonkeana), Masataka and Thierry (1993) concluded that sociality determines the vocal repertoire of a species as strongly as phylogenetic constraints. Lastly, since macaques inhabit a wide range of habitats, interspecific variation in vocal repertoires may be the result of these ecological differences (Masataka and Thierry 1993). It is likely, however, that any one of these factors is insufficient to explain vocal diversity and that a complex interplay of phylogenetic, social, and ecological factors influences degrees of vocal complexity.

In this contribution, I explore vocal homologs and derived calls in the Macaca genus through the:

  1. 1.

    Identification of the main categories of call production

  2. 2.

    Selection of call types from each category of call production to compare across the genus

  3. 3.

    Identification of homologs based on acoustic characteristics

  4. 4.

    Identification of species-specific derived calls and main differences across the genus

  5. 5.

    Comparisons with the Tibetan macaque vocal repertoire

  6. 6.

    Exploration of phylogenetic, social, and ecological factors that may influence homologous and derived calls

4 Methods

4.1 Categories of Call Production

Two previous studies designated categories for comparison across different species of Old World monkeys (M. radiata, M. silenus, P. johnii, P. entellus: Hohmann 1991; Papio ursinus, T. gelada, Gustison et al. 2012). I followed Gustison et al. (2012) and identified calls in macaques within three main categories and included the subcategories differentiated for each: allospecific (alarm and food calls), social (long-distance and close-range calls (competitive, distress, and contact)), and other (see Fig. 7.1). Allospecific calls are elicited by external stimuli and include alarm and food calls. The majority of vocalizations in mammals are emitted during social interactions with conspecifics (Gustison et al. 2012). Such social calls are further categorized into two subclasses: long-distance and close-range calls. For close-range calls, a further subdivision is necessary; so I classified close-range calls into three additional subcategories to cover the many different contexts in which these calls are emitted: contact, competition, and distress. The last category, other, includes calls that are not strictly emitted in a particular context or the context is unknown.

Fig. 7.1
figure 1

Call categories and call types investigated in the genus Macaca. The main categories and subcategories are in bold, and calls in italics indicate the call types chosen for homologous and derived comparisons. (*) Non-tonal screams are not strictly distress calls since they are also emitted in feeding contexts

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4.2 Exploring Vocal Homologs and Derived Calls in the Genus Macaca

The homologous call types investigated come from a review of the macaque literature and the identification of calls that were similar in acoustic structure alone, even if they were designated different names in the literature or were emitted in different contexts. Derived calls are defined as acoustically unique to a species and were also identified via visual inspection of spectrograms. Similar to my previous study (Bernstein et al. 2016), I followed Rowell and Hinde (1962) and first identified calls as either clear or harsh. Clear calls are tonal with energy concentrated in harmonic frequency bands, while harsh calls are atonal and acoustically unstructured with underlying harmonic frequency bands obscured by broadband noise and a distribution of energy across a wide frequency spectrum (Palombit 1992; Rowell and Hinde 1962). Once calls were classified as either clear or harsh, I then focused on temporal and frequency characteristics to identify homologous calls. These characteristics included the presence or absence of harmonic frequency bands, the modulation of frequency bands, spectral shifts (e.g., abrupt changes like the presence of a fast-rise transient from high pitch to low pitch), the concentration of spectral energy, whether or not calls were attached to or superimposed onto a noisy portion, and the duration of the call.

In order to make comparisons in the macaque genus, I used reports from which the entire repertoire was systematically investigated and excluded investigations that described only particular call types. This method is similar to the one adopted by McComb and Semple (2005) in their investigation of the coevolution of vocal communication and repertoire size as a measure of vocal complexity. To date there are repertoire studies from 11 different macaque species, including my study on Tibetan macaques (Tibetan macaques, Macaca thibetana, Bernstein et al. 2016; Formosan macaques, M. cyclopis, Hsu et al. 2005; Barbary macaques, M. sylvanus, Hammerschmidt and Fischer 1998; Tonkean macaques, M. tonkeana, Masataka and Thierry 1993; long-tailed macaques, M. fascicularis, Palombit 1992; bonnet macaques, M. radiata, Hohmann 1989; lion-tailed macaques, M. silenus, Hohmann and Herzog 1985; Sugiyama 1968; stump-tailed macaques, M. arctoides, Lillehei and Snowdon 1978; Japanese macaques, M. fuscata, Green 1975; Itani 1963; rhesus macaques, M. mulatta, Rowell 1962; Rowell and Hinde 1962). Comparison of call emission frequency and in which contexts calls were uttered was analyzed when the results were available across the published repertoires in the genus.

4.3 Comparisons with Tibetan Macaques and Phylogenetic, Social, and Ecological Factors

I included a wider array of species for comparisons with the Tibetan macaque vocal repertoire based on phylogenetic closeness, even if their repertoires have not been systematically analyzed and reported. I made this attempt to incorporate studies on specific calls for a more robust comparison with particular Tibetan macaque calls that were not included in the genus comparison. I chose interspecific call types based on their acoustic similarity and not context (for context comparisons, see Table 7.2).

After I identified the homologous and derived calls in the genus, I explored potential phylogenetic, social, and ecological factors. Depending on the source and the type of genetic study, the phylogenetic classification of macaques can vary. One of the most recent studies by Li et al. (2009) investigated the phylogeny of the macaques based on Alu elements. I used their classification for the comparisons investigated here (for each species’ designation in the phylogeny, see Table 7.1). For the social component, I compared the contexts of emission and, if available, the rate at which the call types are emitted in a species’ repertoire. In addition, I used reviews of the Macaca genus (Thierry et al. 1996, 2000; van Schaik et al. 1999; Maestripieri and Roney 2005; Pradhan et al. 2006) and the life history traits provided by Singh and Sinha (2004) to explore social and ecological factors.

Table 7.1 Shared call types in the macaque genus
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5 Results

5.1 Homologous and Derived Calls in the Genus

I selected call types from the three main categories (allospecific, social, and other) of call production across the genus. I identified the following as the shared calls in the 11 macaque species investigated: coo, threat rattle/growl, non-tonal scream, girney/greeting call, tonal scream, squeak, food call, alarm call (non-tonal harsh and tonal segmented types), female and male copulation call, bark, and loud call (Table 7.1). The main category allospecific calls includes the tonal segmented and non-tonal harsh alarm calls and the food call. Threat rattle/growl, bark, non-tonal scream, coo, girney, female and male copulation call, long distance, and loud call are in the social category, and the tonal screams are in the other category since they are emitted in feeding and distress contexts (for subcategories, see Fig. 7.1).

For the 11 species investigated, I identified 9 derived calls based solely on acoustic structure: the krahoo (M. fascicularis); food yell, atonal greeting, and tonal girney (M. cyclopis); warble, harmonic arch, chirp, and male copulation scream (M. mulatta); male copulation grunt (M. arctoides); tonal estrus call (M. fuscata); and female copulation call (M. thibetana).

The main differences found in the homologous calls concerned the frequency of emission and the range of call types within a specific context. For example, M. arctoides have a limited use of coo calls with considerably more harsh, noisy calls in a purely graded signal system (Bruce and Estep 1992). Macaca tonkeana and M. cyclopis macaques have a wider range of agonistic and girney/greeting calls, respectively, that is unparalleled in the rest of the genus (Masataka and Thierry 1993; Hsu et al. 2005).

5.2 Comparisons with the Vocal Repertoire of Tibetan Macaques

The Tibetan macaque vocal repertoire consists of five clear calls (coo, squawk, leap coo, weeping, modulated tonal scream) and seven harsh calls (squeal, noisy scream, growl, bark, compound squeak, pant, female copulation call) (for a quantitative analysis of the vocal repertoire, see Bernstein et al. (2016); see Fig. 7.2). In order to make congeneric comparisons with the Tibetan macaque vocal repertoire, I included a wider array of species based on phylogenetic closeness, even if their repertoires have not been systematically analyzed and reported. I made this attempt to incorporate studies on specific calls for a more robust comparison with particular Tibetan macaque calls that were not included in the genus comparison above (i.e., squawk, squeal, leap coo, weeping, and pant). I chose interspecific call types based on their acoustic similarity and not context (for context comparisons see Table 7.2).

Fig. 7.2
figure 2

Adapted from Bernstein et al. (2016). Calls in bold are homologous calls shared with the rest of the genus. (a) Representative spectrograms of the clear calls in the repertoire (b) Representative spectrograms of the harsh calls in the repertoire (c) Representative spectrogram of the female copulation call

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Table 7.2 Tibetan macaque vocal repertoire and congeneric comparisons
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Overall, the acoustic structure and context of emission was similar among the species investigated. A few main differences in context were a result of the group composition and various species-specific behaviors present in the congeneric species, but not in Tibetan macaques. For example, all of the infants died during my study on the vocal repertoire of Tibetan macaques, and therefore information about the calls associated with mother-infant interactions are limited (Bernstein et al. 2016). Also, an absence of calls from infants leaves out one vital age class that is necessary for a more complete comparison across species. Additionally, Tibetan macaques are one of two macaque species that show bridging behavior where two adults simultaneously lift an infant (Ogawa 1995, this volume). Bridging may be another context associated with infants where individuals emit calls that I was unable to observe.

Also, within the context of mating, female Tibetan macaques do not show any behaviors indicative of estrus (Li et al. 2005) and do not emit an estrous call. My study took place in the Valley of the Wild Monkeys, China, a site where the provisioned macaque groups that inhabit the mountainous sparsely covered terrain have been protected from hunting and trapping since the 1940s (Wada et al. 1987). During my observations, the Tibetan macaques did not emit an alarm or food call. Although Tibetan macaques were observed to emit loud calls that propagated over a large distance, these calls were clustered in the noisy scream category.

The female Tibetan macaque copulation call was the only call in my previous study that was a derived vocalization distinct from what has been reported in the rest of the genus (Bernstein et al. 2016). Usually, female macaques emit soft grunts during copulations. The Tibetan macaque females also emit quiet calls, but their acoustic structure does not involve biphasic “inhale-exhale” components, and they are instead shrill, undulating calls that are not always given in phrases. In comparison to the rest of the macaque genus, female copulation call rate was low and resembled that of M. tonkeana and M. fuscata (Masataka and Thierry 1993; Hohmann 1989; Oda and Masataka 1992; see Table 7.3). Similar to M. radiata, a closely related species in the same lineage, females do not emit an estrous call and copulation calls are the only auditory cue females emit in a copulation context. Males did emit copulation calls as well, but at a much higher frequency. Harassment of copulatory dyads is evident in Tibetan macaques, involves a wider range of age/sex classes than what is reported for most other members of the genus, and appears to be associated with the number of females in the audience.

Table 7.3 Copulation calls in Macaca and life history traits
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5.3 Potential Effects of Phylogeny, Sociality, and Ecology

Phylogenetic Factors

In the macaque species whose repertoires have been systematically analyzed and reported, there are two main types of acoustically structured alarm calls: non-tonal barks and roars (NT) or tonal segmented (TS) calls. Hohmann (1989) proposed that the type of alarm call (NT or TS) present in the repertoire of a macaque species is mostly conserved within phylogenetic groups (NT, sylvanus and silenus; TS, sinica and fascicularis). This pattern holds true for the silenus, sinica, and fascicularis groups (see Table 7.1). Indeed, species in the silenus group (M. nemestrina and M. silenus) have non-tonal alarm calls (Caldecott 1986; Hohmann and Herzog 1985). The only two terrestrial species of macaque with a purely graded signal system, M. sylvanus of the sylvanus lineage and M. arctoides of the sinica group, also have non-tonal alarm calls (Fischer and Hammerschmidt 2002; Chevalier-Skolnikoff 1974). The only exception in the silenus group, M. tonkeana, emits tonal segmented alarm calls. This pattern, where the acoustic structure of an alarm call is conserved within phylogenetic groups, is found in sympatric species from different phylogenetic groups that may be prey to the same predators (M. silenus and M. radiata, Hohmann 1989).

Fooden (1976) sorted the macaque lineages based on the reproductive anatomy of males and females. Although his study relied only on behavioral and anatomical features, his classification is still mostly accurate even with more sophisticated genetic analyses. The evolution of different reproductive anatomy likely stemmed from each lineage going through a genetic bottleneck (Tosi et al. 2003). The three species that emit derived copulation calls (M. thibetana, M. mulatta, M. arctoides) are more closely related than they initially appear. Recent studies in the whole genome sequencing of Tibetan macaques have found that they are most closely related to Chinese rhesus macaques despite having been reported in different lineages (Fan et al. 2014). Analyses of mitochondrial loci in the macaque genus show stump-tailed macaques to potentially be a hybrid of proto-M. thibetana (Tosi et al. 2003).

Social Factors

Most of the derived calls in the macaque genus are related to the context of mating, in particular, female and male copulation calls. Throughout the genus, males typically produce squeak-like copulation calls, while females emit grunts characterized by an “inhale-exhale element” (Pradhan et al. 2006). However, a few species stray from these genus characteristic calls and emit acoustically distinct calls associated with copulations. Two species emit acoustically distinct male copulation calls: M. mulatta copulation screams (Hauser 1993) and M. arctoides copulation grunts (Bauers 1993). Japanese macaques are the only macaque species that have studies reporting a distinct estrous call from the female copulation call (Oda and Masataka 1992), and my previous study reports an acoustically distinct shrill female copulation call in Tibetan macaques (Bernstein et al. 2016). All of these species that emit acoustically distinct calls in the context of copulations are seasonal breeders, have promiscuous mating systems, all exhibit the interruption of copulations by conspecifics, and have similar adult female-to-male ratios (1.3:2.9, Singh and Sinha 2004; Pradhan et al. 2006).

A large number of call types in the context of agonistic interactions is a characteristic of M. tonkeana. This species has high degrees of tolerance, small rank differences, a high frequency of conciliatory patterns, small interindividual distances, and a high rate of bidirectional agonistic interactions (Masataka and Thierry 1993). Context-dependent differences were also found in the derived girney/greeting calls of M. cyclopis. All of the girney/greeting calls were paired with particular contexts and age/sex classes, with acoustic structure changing according to the recipient of the girney/greeting call (Hsu et al. 2005).

Ecological Factors

Overall, loud calls adhere to the bioacoustic requirements for long-distance propagation of sound (e.g., the repetition of units and phrases, no intergradations to other vocal patterns, a stereotyped structure, a large range of frequencies, and a concentration of energy on the lower frequencies; Hohmann and Herzog 1985). Loud calls are harsh calls where the fundamental frequency is in the lower frequency range. However, only some species show a large range of frequencies and utter loud calls that are composed of both tonal and non-tonal harsh units. Three macaque species utter loud calls that are acoustically distinct from the rest of the genus and are composed of tonal and harsh units in a wider range of frequencies (M. silenus, loud call, Hohmann and Herzog 1985; M. fascicularis, krahoo, Palombit 1992; M. tonkeana, loud call, Masataka and Thierry 1993). Also, for all three species, only males have been reported to emit these loud calls. The loud calls of M. silenus are mixed units with a noise-like inhalation phase followed by a tonal exhalation (Hohmann and Herzog 1985), the krahoo of M. fascicularis is distinct for its harsh “kra” syllable at the beginning of the call (Palombit 1992), and M. tonkeana’s loud call is characterized by a distinct flag and mast with a sharp upward and downward frequency modulation (Masataka and Thierry 1993). All three species live in rainforest habitats and are mostly arboreal.

Food calls are common in the genus, but so far only two species have been reported to give acoustically distinct calls strictly emitted in food-related contexts. M. mulatta warbles, harmonic arches, and chirps are acoustically distinct calls made exclusively in a food context (Hauser and Marler 1993). M. cyclopis emit food yells similar to the M. sinica food call, but are acoustically distinct (Hsu et al. 2005). Reports from these two species are from provisioned groups living in human habitations or captivity.

6 Discussion

Mammalian vocalizations consist mainly of grunts, harsh non-tonal threatening vocalizations, and the sometimes tonal alarm calls and screams (Seyfarth and Cheney 2012). Indeed, the macaque genus shared these basic vocalizations (e.g., grunts, girneys, estrus calls, female copulation calls; harsh non-tonal calls, barks, growls; tonal alarm calls; screams, shrieks, tonal, non-tonal screams) but also emitted additional tonal calls (e.g., coos, squawks, and male copulation calls). Overall, macaque repertoires can be described as a graded signal system with intergradations between calls, and the contexts of emission for shared calls were consistent.

Although primate vocalizations appear to be largely genetically predetermined (Newman and Symes 1982), there are differences in the flexibility and conservation of the call types investigated. The flexibility observed in the derived vocalizations seems to be a by-product of the characteristics of the contexts in which calls are emitted or species-specific features. The most salient difference found in my congeneric comparison were the calls emitted in the copulation context. Three species emit derived copulation calls (M. thibetana female copulation call, M. mulatta male copulation scream, M. arctoides male copulation grunt). These species that emit copulation calls uncharacteristic of the genus have species-specific features in their copulation styles.

6.1 The Tibetan Macaque Vocal Repertoire

In sum, the Tibetan macaque vocal repertoire was generally comparable to that of other macaque species. The context of emission was also similar across species, but with a few key differences. For example, my previous study could not investigate the vocalizations of infants because of a 100% mortality rate during the 2014 mating season (Bernstein et al. 2016). Future studies on the vocalizations of infants and infant-related contexts may find that Tibetan macaques do emit calls not previously described in the analysis of the repertoire. The main differences found between Tibetan macaques and the rest of the genus may not only be a result of a missing age class but also the method used to quantify the repertoire and species-specific aspects of their social behavior.

An absence of a food call or alarm call may be the result of site management. These call types may not be absent. It is possible that I simply did not observe them over the course of my study or that provisioning and predators being hunted out of the area have removed these contexts that would elicit calls they may have present in their repertoire. Although Tibetan macaques do emit calls that propagate over a large distance, they were not a distinct call type like the loud calls described for other species. Most of the species that emit loud calls live in rainforest habitats where certain acoustic requirements are necessary for sound propagation. Tibetan macaques inhabit mountainous terrain with sparse tree coverage, where the propagation of their calls is not limited by a densely covered forest (Xia et al. 2010). My quantitative method of relying solely on acoustic characters to define distinct call types may have clustered calls identified separately in other studies into more overarching categories. The same could be true for greeting calls. In some cases, variants of the coo call are considered as a separate category, but for my study, individual classification of coo call variants was not warranted.

The unique copulatory behavior of Tibetan macaques may be one reason an acoustically distinct female call was selected for. Also within the context of mating, female Tibetan macaques do not show any behaviors indicative of estrus (Li et al. 2005), and therefore, it is not surprising that their concealed ovulation would yield the absence of an estrous call. The similarity between M. thibetana, M. tonkeana, and M. fuscata in terms of a low female copulation call rate may imply a cost-benefit strategy that differs between the sexes. All of these species are seasonal breeders, living in multi-male, multi-female groups, and exhibit high rates of copulation interruptions (see Table 7.3). Macaca tonkeana and M. fuscata copulation call emission rate may also be low because females additionally produce estrous calls to solicit males. These species may have evolved an alternate strategy of mating promiscuously and a low call rate to reduce female competition. My preliminary investigation on the association between female copulation call rate and harassment of copulatory dyads does indicate that harassment increases with the number of females in the audience.

However, the presence of both male and female copulation calls might indicate that part of their function is to synchronize male and female mating behavior, especially in seasonally breeding species. Additionally, for males, it might not be so costly to call as it is for females. Adult females harass copulations, sneak copulate with lower-ranking males, and mate promiscuously with males outside of their consortship. In primates, there are very few studies that have investigated a cost-benefit analysis of signaling in the mating context (Hauser 1993). Future studies should investigate the costs and benefits of producing copulation calls along with emission rate and how intra- and intersexual selection plays a role in the mating strategies and auditory sexual signals of males and females.

6.2 Phylogenetic, Social, and Ecological Factors Influencing Macaque Vocal Repertoires

The type of alarm call was conserved within phylogenetic groups (non-tonal, sylvanus and silenus; tonal segmented, sinica and fascicularis) and followed the designation described by Hohmann (1989) with a few exceptions. Macaca sylvanus and M. arctoides, the exceptions in the sinica group, would be expected to have non-tonal harsh alarm calls since their repertoires consist of mostly harsh calls and their placement in the phylogeny of macaques is contested (M. arctoides, Li et al. 2009). Macaca tonkeana, the only exception in the tonkeana group, emit tonal segmented alarm calls, which may be the result of this species having a wide array of tonal calls in their repertoire (Masataka and Thierry 1993). In conclusion alarm calls are one salient example of a vocalization type that is mediated by phylogeny and a repertoire’s acoustic structure, which is largely genetically predetermined (Newman and Symes 1982).

The species that emit derived species-specific copulation calls are all closely related. Phylogenetic and social factors associated with reproduction may be the selective factors under which derived calls have evolved in these three species. Future studies are needed to investigate the copulation calls of females in more detail, to understand their effect as an auditory sexual signal, and to make more in-depth comparisons of their acoustic structure with the rest of the genus.

Certain aspects of M. tonkeana social behavior may drive the need for a larger number of agonistic vocalizations (Masataka and Thierry 1993). The high degree of variability in the frequency of the acoustic structure of girney/greeting calls in M. cyclopis could also be a result of sociality since they were heavily context dependent. Some of these acoustically distinct girney/greeting calls are different from what has been reported in the rest of the genus and could be considered as derived calls.

Factors that influence call production and the extent to which a sound travels can sometimes be enhanced or restricted based on the type of environment that a species inhabits. The environment can affect the context in which a call is given, or change the motivational threshold to call (Green 1981). Macaques inhabit the widest range of habitats; therefore, environmental factors may drive the differences seen among the repertoires of various macaque species. The loud calls of M. silenus and M. tonkeana, and the krahoo of M. fascicularis, are acoustically distinct from the rest of the genus. Their loud calls are made up of tonal and harsh units in a wider range of frequencies, and their arboreal lifestyle and rainforest habitat may have selected for a call with an acoustic structure that enables the propagation of sound in a dense forest.

The acoustically distinct warbles, harmonic arches, and chirps of M. mulatta and the food yells of M. cyclopis and M. sinica are allospecific food calls emitted by species from provisioned groups living in human habitations or captivity. These allospecific calls are related to the quantity or quality of a food source (Gustison et al. 2012), and provisioning heightens these characteristics in a given environment. Food calls and alarm calls are special in that they both are emitted in response to non-conspecifics and they combine call elements to procure new meanings. Therefore, it is possible that other species that do not emit a food-specific call still have the basic acoustic requirements needed to flexibly alter the acoustic structure of a call to convey a food context-specific meaning.

7 Conclusions

The main differences in the genus are in the calls associated with copulation. Macaques are the most behaviorally diverse and widespread primate genus, yet reproductive features appear to be the most important discriminating factor among species. This may explain the flexibility of derived call types observed in the copulation calls of males and females. However, particularly for this genus, it is difficult to tease apart the effects of phylogeny and behavior on reproduction. Instead, a complex interplay of phylogenetic and social features of a species’ reproduction drives the evolution of derived calls in the context of copulations. In conclusion, it is not likely that any particular factor is mutually exclusive. Instead, a complex interplay of phylogenetic, social, and ecological factors may shape the development of derived calls and the preservation of homologous calls across the macaque genus.