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.
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.
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 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 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. K E Y W O R D Slanguage evolution, Levenshtein distance, primates, singing, syntax
Intra and intergroup spatial dynamics of a pair-living singing primate, Indri Indri. A multiannual study on three indri groups in the forest of Maromizaha, Madagascar.
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 multifemales 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.
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