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Here, we investigated the possible linkages among geophagy, soil characteristics, and gut mycobiome of indri (Indri indri), an endangered lemur species able to survive only in wild conditions. The soil eaten by indri resulted in enriched secondary oxide-hydroxides and clays, together with a high concentration of specific essential micronutrients. This could partially explain the role of the soil in detoxification and as a nutrient supply. Besides, we found that soil subject to geophagy and indris’ faeces shared about 8.9% of the fungal OTUs. Also, several genera (e.g. Fusarium, Aspergillus and Penicillium) commonly associated with soil and plant material were found in both geophagic soil and indri samples. On the contrary, some taxa with pathogenic potentials, such as Cryptococcus, were only found in indri samples. Further, many saprotrophs and plant-associated fungal taxa were detected in the indri faeces. These fungal species may be involved in the digestion processes of leaves and could have a beneficial role in their health. In conclusion, we found an intimate connection between gut mycobiome and soil, highlighting, once again, the potential consequent impacts on the wider habitat.

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.

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.

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...

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.

Indris (Indri indri) are the only singing lemurs and produce different types of songs that can be differentiated according to their temporal patterns. The most distinctive portions of the songs are “descending phrases” consisting of 2-5 units. In our study, indri songs were recorded in the Eastern rainforests of Madagascar from 2005 to 2015. All the recordings were made when the recorder operator was in visual contact with the singing social group and by recognizing individual indris using natural markings. Because the individual songs frequently overlap during the chorus, we extracted the pitch contour of 1084 descending phrases using the program Praat. We tested whether the structure of the phrases could provide conspecifics with information about sex and individual identity. We also examined whether the structure of the phrases was related to the genetic relatedness of the indris. The results suggest that the songs have consistent sex-, group-, and individual-specific features. We have also found a sig...

Active pursuit of extra-pair mating has been reported for Indri indri, the socially monogamous largest living lemur. This study, conducted in a mountain rainforest in eastern Madagascar, presents the first evidence for extra-pair mating of indri and discusses the alternative mating strategy and alteration of the social, territorial, spatial, and vocal behavior of the adult female of a group of wild indris. Further studies may investigate whether extra-pair copulation is an attempt to breed with a partner of superior quality and thus lead to extra-pair paternity. If so, it could potentially play a role in maintaining genetic variability within a population.

Contextual variation in the loud calls of strepsirhine primates is poorly understood. To understand whether songs given by indris in different contexts represent acoustically distinct variants and have the potential to elicit context-specific behaviours in conspecific listeners, we investigated the acoustic variability of these songs and the distance travelled by vocalizers after their emissions. Songs of 41 individuals were recorded from 16 indri groups in four different forest sites in eastern Madagascar. We collected a total of 270 duets and choruses arising during territorial defence, advertisement and cohesion. We demonstrated that the structure of indri songs conveyed context-specific information through their overall duration, but shared the sequential pattern of harsh units (roars) followed by long notes and, finally, descending phrases. Analysing in detail individual contributions to advertisement songs and cohesion songs, we found that the acoustic structure of units could be classified ...