Age‐ and sex‐specific patterns of vocal behavior in De Brazza's monkeys (Cercopithecus neglectus)

Abstract

Although vocal production is strongly genetically determined in nonhuman primates, vocal usage is more likely to be influenced by experience. Nonetheless, sex differences in both production and usage can be found in the vocal repertoire of adults, but little attention has been paid to their ontogeny. Here, we provide the first comprehensive analysis of the vocal repertoire of De Brazza's monkeys (Cercopithecus neglectus), with particular attention to age- and sex-specific patterns. This species has special interest because it is the only monogamous species of guenons, but it nevertheless shares the strong sexual morphological and behavioral dimorphism seen in other guenons. A structurally based classification of calls recorded in 23 captive individuals has been cross-validated by an analysis of the associated contexts of emission. We identified sound units that could be uttered alone or concatenated to form 10 call types, including only three types shared by all age-sex-classes. Both age- and sex-discrepancy in terms of phonation could be explained by maturational changes and morphological dimorphism. In general, call production and usage parallel those seen in other guenons, suggesting that phylogeny and sexual dimorphism play important roles in vocal communication in this species. However, the boundary between adult male and female vocal repertoires appeared to be less strict than previously reported, suggesting that both sexes have the capacity to produce calls of the other sex but that social roles may constrain this expression. Similarly, age-specific vocal patterns would reflect respective social roles, and experience to some extent. Finally, calling rates would reflect age-/sex-specific degree of involvement in intragroup social networks. These findings highlight the relative importance of phylogeny, morphology, and social system on the shaping of individual repertoires in nonhuman primates.

Vocal repertoire of free‐ranging adult golden snub‐nosed monkeys (Rhinopithecus roxellana)

“…Similar findings have already been reported in some species of Old World monkeys ( Cercocebus torquatus : Bouchet et al, 2010; C. neglectus : Bouchet et al, 2012), whereas a high degree of call type sharing between sexes is found in some other species, particularly macaques ( M. sylvanus : Hammerschmidt & Fischer, 1998; Macaca thibetana : Bernstein, Sheeran, Wagner, Li, & Koda, 2016). The great sex discrepancy in terms of call production in adult R. roxellana could be attributed to two non‐exclusive factors.…”

“…For example, increasing the intensity of mounting grunts may lead to grunts , and further, if the duration increases and the f 0 decreases in grunts , long grunts may result. Although some primates have been considered to have graded vocal repertoires ( Macaca fuscata : Green, 1975; Macaca sylvanus : Hammerschmidt & Fischer, 1998) and some others have discrete vocal repertoires ( Cercopithecus diana : Zuberbühler, Noë, & Seyfarth, 1997; Cercopithecus neglectus : Bouchet et al, 2012), a mixed vocal system with both graded and discrete signals appears to be the norm for most primates, living in either relatively open or closed habitats (reviewed in Green & Marler, 1979; Papio hamadryas : Rendall, Notman, & Owren, 2009; Cercopithecus campbelli : Lemasson & Hausberger, 2011). The level of gradedness or discreteness is likely to be varied among different call types depending on their specific functions (Bouchet et al, 2013; Lemasson & Hausberger, 2011).…”

“…Within a vocal repertoire, the production and use of vocal signals are affected by several factors including sex, age, body size, and social role (Bouchet, Blois‐Heulin, & Lemasson, 2012; Bouchet, Pellier, Blois‐Heulin, & Lemasson, 2010; Pfefferle & Fischer, 2006). The effects of these factors may not be mutually exclusive.…”

“…For example, sex‐specific discrepancies in terms of call production are common in nonhuman primates (Bouchet et al, 2010; Briseño‐Jaramillo, Biquand, Estrada, & Lemasson, 2017; Hohmann, 1991). These differences are often attributed to the sex differences in social role, and in some species, the sex that is more social produces more call types than the other (Bouchet et al, 2012, 2010). In addition, some acoustic parameters (e.g., fundamental frequency and formant dispersion) depend on the size of vocal tract/folds, which is positively related to body size (Hauser, 1993; Pfefferle & Fischer, 2006).…”

“…Thus, in species with sexual dimorphism, sex differences in call production may also be attributed to the sex differences in body size. For example, it has been suggested that the fundamental frequency is negatively correlated with body size (Pfefferle & Fischer, 2006), and thus the larger body size may limit one sex (usually males) to produce some high pitched calls that the other sex can emit (Bouchet et al, 2012). …”