Notes on a tree: reframing the relevance of primate choruses, duets, and solo songs

The complexity of primates’ singing behavior has long gathered the attention of researchers interested in understanding the selective pressures underpinning the evolution of language. Among these pressures, a link between territoriality, pair-living, and singing displays has been suggested. Historically, singing primates have been found in a few taxa that are not closely related to each other, and, in the last years, their phylogeny has dramatically changed. Hence, we aimed at understanding if the dogmatic association between territorial behavior and a monogamous social structure still holds in the light of current research. Moreover, singing behavior has often been considered a whole, but animals can perform different singing forms depending on how many individuals call simultaneously. Currently, it is unclear to which extent these singing forms are widespread among these primate groups. Given that there is no unique definition for a song, solo, duet, and chorus, we envisioned some of the most used descriptions. We then formulated some new definitions that we followed in our review of the presence/absence of these different forms of song organization among singing primates’ taxa. In particular, we suggested that tarsier species that are typically considered non-singers may indeed sing, and we pointed out that non-duetting gibbons may perform duet interactions. We found that, besides duets, chorusing behavior and solo songs are essential features of primates’ communication, but their study is still in a descriptive phase. Moreover, while territorial behavior seems to be conserved in these singing taxa, we highlighted that the monogamous social structure is not the rule. Pair-living plus multi- females groups displaying singing behavior are common too. We suggest that ending to consider these taxa as uniform in their sociality and vocal behavior might be a significant turning point to unravel the different selective pressures that influenced the emergence and organization of such peculiar vocal behavior.

Inter-sexual multimodal communication during mating in wild geladas: the leading role of females

Female primates can emit vocalizations associated with mating that can function as honest signals of fertility. Here, we investigated the role of mating calls and visual signals in female geladas Theropithecus gelada. Since females have a central role in the gelada society and seem to solicit sexual interactions, we answered whether they emit vocalizations in conjunction with gazing to increase mating success probability. Before and during copulations, females can emit pre-copulation calls and copulation calls. For the first time, we identified a new female vocalization emitted at the final stage of copulations (end-copulation call), possibly marking the occurrence of ejaculation. We found that longer pre-copulation call sequences were followed by both prolonged copulations and the presence of end-copulation calls thus suggesting that females use pre-copulation calls to ensure successful copula completion. Moreover, we found that different combinations of female vocal types and gazing had different effects on male vocal behavior and motivation to complete the copula. The analysis of the vocal and visual signals revealed a complex inter-sexual multimodal chattering with the leading role of females in the signal exchange. Such chattering, led by females, modulates male sexual arousal, thus increasing the probability of the copula success.

Passive Acoustic Monitoring and Automatic Detection of Diel Patterns and Acoustic Structure of Howler Monkey Roars

Nighttime studies are underrepresented in ecological research. Even well-known behaviors, such as the loud call of howler monkeys, are rarely studied at night. Our goal was to help fill this knowledge gap by studying the 24 h vocal behavior of the Guianan red howler monkey (Alouatta macconnelli) and to compare the acoustic structures of howling bouts made during the day to those made at night. We used passive acoustic monitoring coupled with automatic acoustic detection to study three groups of howlers over three months in the Viruá National Park, Roraima, Brazil. The automatic classifier we built detected 171 howling bouts with a 42% recall rate and 100% precision. Though primarily diurnal, howlers vocalized mainly at night. Greater vocal activity before nautical twilight might be associated with territorial and resource defense behaviors, with howlers calling from roosting sites before starting their daily routines. We also found that during the day, howling bouts were longer and had lower harmonic-to-noise ratios, lower frequencies, and more symmetric energy distributions than bouts at night. Our study adds to growing evidence that passive acoustic monitoring and automatic acoustic detection can be used to study primates and improve our understanding of their vocal behavior.

Variation in the Non-mimetic Vocalizations of Brood-Parasitic Indigobirds and Their Potential Role in Speciation

Indigobirds (Vidua spp.) are obligate brood parasites in which imprinting on heterospecific hosts shapes adult vocal behavior and mating preferences. Adult male indigobirds mimic the songs and other vocalizations of their respective hosts, which signals their own host environment to prospective mates and has important implications for speciation. In this study, we examined variation within and among indigobird species in the non-mimetic components of their vocal behavior, including both chatter calls and their impressive repertoires of intricate non-mimicry songs. We test whether indigobird species in Tanzania (V. chalybeata, V. codringtoni, V. funerea, and V. purpurascens) differ consistently in general features of their non-mimetic vocalizations, and we test whether local ecological conditions influence vocal behavior. Indigobird non-mimetic song repertories are learned from and shared with other males of the same species. We find that local dialect “neighborhoods” are variable in size among species and regions, depending on habitat continuity and the distribution of male territories. Despite the complete turnover of the specific songs comprising non-mimicry song repertoires from one local dialect to the next, we find significant species effects for more general measures of non-mimicry songs such as repertoire size and diversity, frequency, song length, and pace. For some traits, we also found significant regional differences, which may be mediated by significant relationships between elevation and morphometrics. Chatter calls were broadly similar across both species and localities, but we found significant species and region effects for frequency and to a lesser extent pace. We discuss the possibility that learning and mimicking the vocalizations of different hosts might influence the production of non-mimetic vocalizations and explain many of the species differences we detected. Whether these species differences are purely due to phenotypic plasticity or also reflect genetic divergence in traits influencing sound production and/or female preferences, they may contribute to reproductive isolation among nascent and recently evolved indigobird species.

Local field potentials in a pre-motor region predict learned vocal sequences

Neuronal activity within the premotor region HVC is tightly synchronized to, and crucial for, the articulate production of learned song in birds. Characterizations of this neural activity detail patterns of sequential bursting in small, carefully identified subsets of neurons in the HVC population. The dynamics of HVC are well described by these characterizations, but have not been verified beyond this scale of measurement. There is a rich history of using local field potentials (LFP) to extract information about behavior that extends beyond the contribution of individual cells. These signals have the advantage of being stable over longer periods of time, and they have been used to study and decode human speech and other complex motor behaviors. Here we characterize LFP signals presumptively from the HVC of freely behaving male zebra finches during song production to determine if population activity may yield similar insights into the mechanisms underlying complex motor-vocal behavior. Following an initial observation that structured changes in the LFP were distinct to all vocalizations during song, we show that it is possible to extract time-varying features from multiple frequency bands to decode the identity of specific vocalization elements (syllables) and to predict their temporal onsets within the motif. This demonstrates the utility of LFP for studying vocal behavior in songbirds. Surprisingly, the time frequency structure of HVC LFP is qualitatively similar to well-established oscillations found in both human and non-human mammalian motor areas. This physiological similarity, despite distinct anatomical structures, may give insight into common computational principles for learning and/or generating complex motor-vocal behaviors.