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Strepsirrhine vocalisations are extraordinarily diverse and cross-species comparisons are needed to explore how this variability evolved. We contributed to the investigation of primate acoustic diversity by comparing the vocal repertoire of two sympatric lemur species, Propithecus diadema and Indri indri. These diurnal species belong to the same taxonomic family and have similar activity patterns but different social structures. These features make them excellent candidates for an investigation of the phylogenetic, environmental, and social influence on primate vocal behavior. We recorded 3 P. diadema groups in 2014 and 2016. From 1,872 recordings we selected and assigned 3814 calls to 9 a priori call types, on the basis of their acoustic structure. We implemented a reproducible technique performing an acoustic feature extraction relying on frequency bins, t-SNE data reduction, and a hard-clustering analysis. We first quantified the vocal repertoire of P. diadema, finding consistent results for the 9 putatively identified call types. When comparing this repertoire with a previously published repertoire of I. indri, we found highly species-specific repertoires, with only 2% of the calls misclassified by species identity. The loud calls of the two species were very distinct, while the low-frequency calls were more similar. Our results pinpoint the role of phylogenetic history, social and environmental features on the evolution of communicative systems and contribute to a deeper understanding of the evolutionary roots of primate vocal differentiation. We conclude by arguing that standardized and reproducible techniques, like the one we employed, allow robust comparisons and should be prioritized in the future.

Rhythmic patterns in interactive contexts characterize human behaviours such as conversational turn-taking. These timed patterns are also present in other animals, and often described as rhythm. Understanding fine-grained temporal adjustments in interaction requires complementary quantitative methodologies. Here, we showcase how vocal interactive rhythmicity in a non-human animal can be quantified using a multi-method approach. We record vocal interactions in harbour seal pups ( Phoca vitulina ) under controlled conditions. We analyse these data by combining analytical approaches, namely categorical rhythm analysis, circular statistics and time series analyses. We test whether pups' vocal rhythmicity varies across behavioural contexts depending on the absence or presence of a calling partner. Four research questions illustrate which analytical approaches are complementary versus orthogonal. For our data, circular statistics and categorical rhythms suggest that a calling partner affects a pup's call timing. Granger causality suggests that pups predictively adjust their call timing when interacting with a real partner. Lastly, the ADaptation and Anticipation Model estimates statistical parameters for a potential mechanism of temporal adaptation and anticipation. Our analytical complementary approach constitutes a proof of concept; it shows feasibility in applying typically unrelated techniques to seals to quantify vocal rhythmic interactivity across behavioural contexts. This article is part of a discussion meeting issue ‘Face2face: advancing the science of social interaction’.

Nonlinear phenomena (NLP) in animal vocalizations arise from irregularities in the oscillation of the vocal folds. Various hypotheses have been put forward to explain the occurrence of NLP, from adaptive to physiological ones. Non-human primates often display NLP in their vocalizations, yet the meaning of these features is still unclear. We present here the first study of NLP occurrence in the song of a singing primate: the indri (Indri indri). We found that the more an individual sings, the higher the likelihood of emitting NLP. Our results show that NLP occurrence in indri depends on phonation, i.e., the cumulative duration of all the units emitted by an individual. Furthermore, NLP occurrence depends on the timing of the signal and increases as the singing progresses. Our findings suggest that indris may be subjected to physiological constraints during the singing process which may limit the production of harmonic sounds because of the fatigue needed to perform loud and long calls. However, indris may still benefit from emitting NLP by strengthening the loudness of their signals for better advertising their presence to the neighboring conspecific groups.

Vocal and gestural sequences of several primates have been found to conform to two general principles of information compression: the compensation between the duration of a construct and that of its components (Menzerath-Altmann law) and an inverse relationship between signal duration and its occurrence (Zipf's law of abbreviation). Even though Zipf's law of brevity has been proposed as a universal in animal communication, evidence on non-human primate vocal behavior conformity to linguistic laws is still debated, and information on strepsirrhine primates is lacking. We analyzed the vocal behavior of the unique singing lemur species (Indri indri) to assess whether the song of the species shows evidence for compression. As roars have a chaotic structure that impedes the recognition of each individual utterance, and long notes are usually given by males, we focused on the core part of the song (i.e., the descending phrases, composed of two-six units). Our results indicate that indris' songs conform to Zipf's and Menzerath-Altmann linguistic laws. Indeed, shorter phrases are more likely to be included in the song, and units' duration decrease at the increase of the size of the phrases. We also found that, despite a sexual dimorphism in the duration of both units and phrases, these laws characterize sequences of both males and females. Overall, we provide the first evidence for a trade-off between signal duration and occurrence in the vocal behavior of a strepsirrhine species, suggesting that selective pressures for vocal compression are more ancestral than previously assumed within primates.

In animal vocal communication, the development of adult-like vocalization is fundamental to interact appropriately with conspecifics. However, the factors that guide ontogenetic changes in the acoustic features remain poorly understood. In contrast with a historical view of nonhuman primate vocal production as substantially innate, recent research suggests that inheritance and physiological modification can only explain some of the developmental changes in call structure during growth. A particular case of acoustic communication is the indris’ singing behavior, a peculiar case among Strepsirrhine primates. Thanks to a decade of intense data collection, this work provides the first long-term quantitative analysis on song development in a singing primate. To understand the ontogeny of such a complex vocal output, we investigated juvenile and sub-adult indris’ vocal behavior, and we found that young individuals started participating in the chorus years earlier than previously reported. Our results indicated that spectro-temporal song parameters underwent essential changes during growth. In particular, the age and sex of the emitter influenced the indris’ vocal activity. We found that frequency parameters showed consistent changes across the sexes, but the temporal features showed different developmental trajectories for males and females. Given the low level of morphological sexual dimorphism and the marked differences in vocal behavior, we hypothesize that factors like social influences and auditory feedback may affect songs’ features, resulting in high vocal flexibility in juvenile indris. This trait may be pivotal in a species that engages in choruses with rapid vocal turn-taking.

The critically endangered indri (Indri indri) is the largest extant lemur species and its population size is projected to decline over the next three generations due to habitat loss, hunting and climate change. Accurate information on the demographic parameters driving the population dynamics of indri is urgently needed to help decision-making regarding the conservation of this iconic species. We monitored and followed the life histories of 68 individually recognizable indris in 10 family groups in the Maromizaha New Protected Area (Madagascar) for 12 years. We estimated age and sex-specific survival trajectories using a Bayesian hierarchical survival model and found that the survival curves for male and female indris show a similar pattern, consistent with what found typically in primates; i.e., a high infant mortality rate which declines with age in the juvenile phase and increases again for adults. Also, life expectancies at 2 years of age (e2), were found to be similar between the sexes (e2 females = 7.8 years; e2 males = 7.5 years). We suggest that the lack of strong differences in the survival patterns for male and female indris are related to the strictly monogamous mating system and the lack of sexual dimorphism in this species. Our study provides, for the first time, robust estimates for demographic parameters of indris and one of the very few datasets on survival trajectories available for primates.

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.

In mammals, olfactory communication plays an essential role in territorial and mating dynamics. Scent depositions in various species, including lemurs, can be placed via marking or overmarking (marking over previous depositions). We focused on the role that marking and overmarking play in territorial defence and intrasexual competition. We investigated these aspects in diademed sifaka (Propithecus diadema) in the primary rainforest of Maromizaha (eastern Madagascar). We collected scent marking data for five groups from April to November 2018 and from May to December 2019. We aimed to understand whether the lemurs deposited scent marks homogeneously across the home range and whether sex, rank, and occurrence of intergroup encounters affected the lemur’s deposition rate. We also asked whether males overmarked adult females more often than other depositions, and the marking and overmarking rates changed between the migration and non-migration seasons. We found that scent marking was performed higher in peripheral and overlapping areas than in the home range central areas. In addition, males had higher scent marking rates, but intergroup encounters did not affect deposition rates. Males showed higher rates of overmarking and primarily targeted dominant females’ depositions, particularly during the “migration” season (including premating and mating seasons). Our findings suggest a border-marking strategy in Propithecus diadema. More frequent scent marking in the “migration” season suggests intrasexual competition in males. Our results suggest that marking is associated with territorial and resource defence, suggesting that it plays a role in monopolizing females using a mate-guarding strategy and may also serve for males’ self-advertisement to females and subordinate depositors.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships. Publisher PDF

Summary What are the origins of musical rhythm? One approach to the biology and evolution of music consists in finding common musical traits across species. These similarities allow biomusicologists to infer when and how musical traits appeared in our species 1 . A parallel approach to the biology and evolution of music focuses on finding statistical universals in human music 2 . These include rhythmic features that appear above chance across musical cultures. One such universal is the production of categorical rhythms 3 , defined as those where temporal intervals between note onsets are distributed categorically rather than uniformly 2 , 4 , 5 . Prominent rhythm categories include those with intervals related by small integer ratios, such as 1:1 (isochrony) and 1:2, which translates as some notes being twice as long as their adjacent ones. In humans, universals are often defined in relation to the beat, a top-down cognitive process of inferring a temporal regularity from a complex musical scene 1 . Without assuming the presence of the beat in other animals, one can still investigate its downstream products, namely rhythmic categories with small integer ratios detected in recorded signals. Here we combine the comparative and statistical universals approaches, testing the hypothesis that rhythmic categories and small integer ratios should appear in species showing coordinated group singing 3 . We find that a lemur species displays, in its coordinated songs, the isochronous and 1:2 rhythm categories seen in human music, showing that such categories are not, among mammals, unique to humans 3 .

Animal acoustic communication often takes the form of complex sequences, composed of multiple distinct acoustic units, which can vary in their degree of stereotypy. Studies of sequence variation may contribute to our understanding of the structural flexibility of primates' songs, which can provide essential ecological and behavioral information about variability at the individual, population, and specific level and provide insights into the mechanisms and drivers responsible for the evolutionary change of communicative traits. Several methods have been used for investigating different levels of structural information and sequence similarity in acoustic displays. We studied intra and interindividual variation in the song structuring of a singing primate, the indri (Indri indri), which inhabits the montane rain forests of Madagascar. Indri groups emit duets and choruses in which they combine long notes, short single units, and phrases consisting of a variable number of units (from two to six) with slightly descending frequency. Males' and females' contributions to the song differ in the temporal and frequency structure of song units and repertoire size. We calculated the similarity of phrase organization across different individual contributions using the Levenshtein distance, a logic distance that expressed the minimum cost to convert a sequence into another and can measure differences between two sequences of data. We then analyzed the degree of similarity within and between individuals and found that: (a) the phrase structure of songs varied between reproductive males and females: female structuring of the song showed a higher number of phrases if compared to males; (b) male contributions to the song were overall more similar to those of other males than were female contributions to the song of other females; (c) male contributions were more stereotyped than female contributions, which showed greater individual flexibility. The picture emerging from phrase combinatorics in the indris is in agreement with previous findings of rhythmic features and song repertoire size of the indris, which also suggested that female songs are potentially less stereotyped than those of males.

Territorial pair-living species tend to occupy and defend stable areas, assumed to contain all the resources needed for the lifetime of the group. Furthermore, groups have to mediate spatial relationships with neighboring groups. We investigated the relationship between social and spatial dynamics at the intra- and intergroup level in a pair-living territorial singing primate: the indri (Indri indri). We collected spatial data on three neighboring groups during 396 sampling days between 2009 and 2014 in Maromizaha forest, Madagascar. We evaluated the stability of territories in terms of size and location using minimum convex polygons, defined the presence and stability of core areas, and investigated if singing locations and intergroup encounters were concentrated in the core areas. Territories were generally stable in location and size, although some degree of territorial shift occurred, leading to readjustment of intergroup spacing. Groups had core areas that were not stable across years but were concentrated in the area of the territories that groups occupy consistently over time (stable areas). Singing locations were equally distributed inside and outside core areas, suggesting an even distribution through the territories; meanwhile 9 of 12 intergroup encounters took place in the core areas at the edge of territories. Together, our results support the pattern of territorial stability predicted for a pair-living species, where groups regulate territory exclusivity and spacing with neighbors. Singing behavior also plays an important role in mediating intergroup spatial dynamics. The spatial pattern we found in indris is comparable with that found in other territorial and pair-living primates with different ecological needs, suggesting that in addition to ecological factors, social dynamics influence intergroup spatial dynamics.

Among the behavioral traits shared by some nonhuman primate species and humans there is singing. Unfortunately, our understanding of animals’ rhythmic abilities is still in its infancy. Indris are the only lemurs who sing and live in monogamous pairs, usually forming a group with their offspring. All adult members of a group usually participate in choruses that are emitted regularly and play a role in advertising territorial occupancy and intergroup spacing. Males and females emit phrases that have similar frequency ranges but may differ in their temporal structure. We examined whether the individuals’ contribution to the song may change according to chorus size, the total duration of the song or the duration of the individual contribution using the inter-onset intervals within a phrase and between phrases. We found that the rhythmic structure of indri’s songs depends on factors that are different for males and females. We showed that females have significantly higher variation in the rhythm of their contribution to the song and that, changes according to chorus size. Our findings indicate that female indris sustain a higher cost of singing than males when the number of singers increases. These results suggest that cross-species investigations will be crucial to understanding the evolutionary frame in which such sexually dimorphic traits occurred.

We used a logic distance to investigate intra and inter-individual variation in the phrase combinatorics of a singing primate, the indri, which inhabits the montane rain forests of Madagascar. Indris combine long notes, short single notes, and phrases consisting of two, three, four, or five units with slightly descending frequency. We calculated the similarity across different individual songs using the Levenshtein distance. We then analyzed the degree of similarity within and between individuals and found that: i) the phrase structure of songs varied between reproductive males and females; ii) male contributions to the song are overall more similar to those of other males; iii) male contributions are more stereotyped than females' ones. The picture emerging from phrase combinatorics in the indris is in agreement with previous findings of rhythmic features and repertoire size, which also suggested that female songs are potentially more distinctive than those of males.

In the dense tropical rainforests of Madagascar, visual communication is impeded by obstacles. Lemurs use scent marking to communicate at a short distance and loud calls to communicate at a long range. The Indri (Indri indri) is a diurnal primate that emits choruses of three distinct types. The song types are essential in advertising position within the group territory, in deciding the sorts of aggressive group encounters, and in maintaining cohesion between animals dispersed during feeding. A detailed examination of the advertisement songs showed that three main parts constitute them. The last, most consistent of these parts, showed phrases consisting of units emitted with a descending frequency. The rhythm of these units changed significantly between phrases of different durations and the sexes. We also found that the unit structure may provide conspecifics with information on the individual identity of the emitter and that male songs, but not female’s, are more similar to those of their parent of the same sex than to other indris. The song of the indris is an effective way to transfer information at a long distance and may transmit sex and individual identity information.In the dense tropical rainforests of Madagascar, visual communication is impeded by obstacles. Lemurs use scent marking to communicate at a short distance and loud calls to communicate at a long range. The Indri (Indri indri) is a diurnal primate that emits choruses of three distinct types. The song types are essential in advertising position within the group territory, in deciding the sorts of aggressive group encounters, and in maintaining cohesion between animals dispersed during feeding. A detailed examination of the advertisement songs showed that three main parts constitute them. The last, most consistent of these parts, showed phrases consisting of units emitted with a descending frequency. The rhythm of these units changed significantly between phrases of different durations and the sexes. We also found that the unit structure may provide conspecifics with information on the individual identity of the emitter and that male songs, but not female’s, are more similar to those of their parent of the s...

Although there is a growing number of researches focusing on acoustic communication, the lack of shared analytic approaches leads to inconsistency among studies. Here, we introduced a computational method used to examine 3360 calls recorded from wild indris (Indri indri) from 2005&ndash, 2018. We split each sound into ten portions of equal length and, from each portion we extracted spectral coefficients, considering frequency values up to 15,000 Hz. We submitted the set of acoustic features first to a t-distributed stochastic neighbor embedding algorithm, then to a hard-clustering procedure using a k-means algorithm. The t-distributed stochastic neighbor embedding (t-SNE) mapping indicated the presence of eight different groups, consistent with the acoustic structure of the a priori identification of calls, while the cluster analysis revealed that an overlay between distinct call types might exist. Our results indicated that the t-distributed stochastic neighbor embedding (t-SNE), successfully been employed in several studies, showed a good performance also in the analysis of indris&rsquo, repertoire and may open new perspectives towards the achievement of shared methodical techniques for the comparison of animal vocal repertoires.

Estimating the number of animals participating in a choral display may contribute reliable information on animal population estimates, particularly when environmental or behavioral factors restrict the possibility of visual surveys. Difficulties in providing a reliable estimate of the number of singers in a chorus are many (e.g., background noise masking, overlap). In this work, we contributed data on the vocal chorusing of the indri lemurs (Indri indri), which emit howling cries, known as songs, uttered by two to five individuals. We examined whether we could estimate the number of emitters in a chorus by screening the fundamental frequency in the spectrograms and the total duration of the songs, and the reliability of those methods when compared to the real chorus size. The spectrographic investigation appears to provide reliable information on the number of animals participating in the chorusing only when this number is limited to two or three singers. We also found that the Acoustic Complexity Index positively correlated with the real chorus size, showing that an automated analysis of the chorus may provide information about the number of singers. We can state that song duration shows a correlation with the number of emitters but also shows a remarkable variation that remains unexplained. The accuracy of the estimates can reflect the high variability in chorus size, which could be affected by group composition, season and context. In future research, a greater focus on analyzing frequency change occurring during these collective vocal displays should improve our ability to detect individuals and allow a finer tuning of the acoustic methods that may serve for monitoring chorusing mammals.

The increasing interest in the evolution of human language has led several fields of research to focus on primate vocal communication. The ‘singing primates’, which produce elaborated and complex sequences of vocalizations, are of particular interest for this topic. Indris (Indri indri) are the only singing lemurs and emit songs whose most distinctive portions are “descending phrases” consisting of 2-5 units. We examined how the structure of the indris’ phrases varied with genetic relatedness among individuals. We tested whether the acoustic structure could provide conspecifics with information about individual identity and group membership. When analyzing phrase dissimilarity and genetic distance of both sexes, we found significant results for males but not for females. We found that similarity of male song-phrases correlates with kin in both time and frequency parameters, while, for females, this information is encoded only in the frequency of a single type. Song phrases have consistent individual-specific features, but we did not find any potential for advertising group membership. We emphasize the fact that genetic and social factors may play a role in the acoustic plasticity of female indris. Altogether, these findings open a new perspective for future research on the possibility of vocal production learning in these primates.

Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair-living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra-pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair-living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra-pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair-living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair-living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species.

A crucial, common feature of speech and music is that they show non-random structures over time. It is an open question which of the other species share rhythmic abilities with humans, but in most cases the lack of knowledge about their behavioral displays prevents further studies. Indris are the only lemurs who sing. They produce loud howling cries that can be heard at several kilometers, in which all members of a group usually sing. We tested whether overlapping and turn-taking during the songs followed a precise pattern by analysing the temporal structure of the individuals' contribution to the song. We found that both dominants (males and females) and non-dominants influenced the onset timing one another. We have found that the dominant male and the dominant female in a group overlapped each other more frequently than they did with the non-dominants. We then focused on the temporal and frequency structure of particular phrases occurring during the song. Our results show that males and females have dimorphic inter-onset intervals during the phrases. Moreover, median frequencies of the unit emitted in the phrases also differ between the sexes, with males showing higher frequencies when compared to females. We have not found an effect of age on the temporal and spectral structure of the phrases. These results indicate that singing in indris has a high behavioral flexibility and varies according to social and individual factors. The flexible spectral structure of the phrases given during the song may underlie perceptual abilities that are relatively unknown in other non-human primates, such as the ability to recognize particular pitch patterns.

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In this talk, we propose an account of the evolution of language that builds on the hypothesis of human self-domestication (HSD), arguing that the evolution of one of the hallmarks of communication, i.e., conversational abilities, is strongly linked to the reduction of reactive aggression, one of the characteristic features and one of the triggering factors of HSD. Our argument rests on two steps: to argue in favor of a continuity of animal proto-conversation (PC) with modern human conversation; to show that the analysis of how PC of human infants develop into sophisticated conversational skills, in part from changes in the management of aggression/emotions, can shed light on how full-fledged conversational abilities emerged from PC in modern humans under HSD forces. Overall, we argue for a gradual transition from PC to full-fledged conversation under the gradual increase of HSD features in our species.