Singing more, singing harsher: occurrence of nonlinear phenomena in a primate' song.

Nonlinear phenomena (NLP) in animal vocalizations arise from irregularities in the oscillation of the vocal folds. Various non-mutually exclusive 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 communicative role of these features, if any, is still unclear. We here investigate the occurrence of NLP in the song of a singing primate, the indri (Indri indri), testing for the effect of sex, age, season, and duration of the vocal display on their emission. Our results show that NLP occurrence in indri depends on phonation, i.e., the cumulative duration of all the units emitted by an individual, and that NLP have higher probability to be emitted in the later stages of the song, probably due to the fatigue indris may experience while singing. Furthermore, NLP happen earlier in the vocal display of adult females than in that of the adult males, and this is probably due to the fact that fatigue occurs earlier in the former because of a greater contribution within the song. Our findings suggest, therefore, that indris may be subjected to physiological constraints during the singing process which may impair the production of harmonic sounds. 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.

BIOMEDICAL EVALUATION OF THE GOLDEN-CROWNED SIFAKA (PROPITHECUS TATTERSALLI) IN DARAINA, MADAGASCAR.

Complete medical examinations were performed on 25 wild golden-crowned sifaka (Propithecus tattersalli) from northeastern Madagascar. Each animal received a complete physical examination and weight, body temperature, heart rate, and respiratory rate were documented. Blood samples were collected for packed cell volume, estimated total white blood cell count, serum biochemical profile, fat-soluble vitamin analysis, trace mineral analysis, and Toxoplasma gondii serology. All animals examined were adults and determined to be in good health and body condition. No ectoparasites were observed. Fecal samples were collected for endoparasite examination and bacterial culture; while no endoparasites were observed, fecal samples from two females cultured positive for Bacillus cereus. One male lemur had a positive antibody titer to Toxoplasma gondii immunoglobulin G. These baseline health data provide an important foundation for continued monitoring of this critically endangered species.

Dynamics and determinants of glucocorticoid metabolite concentrations in wild Verreaux's sifakas.

Glucocorticoids have wide-ranging effects on animals' behaviour, but many of these effects remain poorly understood because numerous confounding factors have often been neglected in previous studies. Here, we present data from a 2-year study of 7 groups of wild Verreaux's sifakas (Propithecus verreauxi), in which we examined concentrations of faecal glucocorticoid metabolites (fGCMs, n = 2350 samples) simultaneously in relation to ambient temperatures, food intake, rank, reproduction, adult sex ratios, social interactions, vigilance and self-scratching. Multi-variate analyses revealed that fGCM concentrations were positively correlated with increases in daily temperature fluctuations and tended to decrease with increasing fruit intake. fGCM concentrations increased when males were sexually mature and began to disperse, and dominant males had higher fGCM concentrations than subordinate males. In contrast to males, older females showed a non-significant trend to have lower fGCM levels, potentially reflecting differences in male and female life-history strategies. Reproducing females had the highest fGCM concentrations during late gestation and had higher fGCM levels than non-reproducing females, except during early lactation. Variation in fGCM concentrations was not associated with variation in social interactions, adult sex ratios, vigilance and self-scratching. Altogether, we show that measures of glucocorticoid output constitute appropriate tools for studying energetic burdens of ecological and reproductive challenges. However, they seem to be insufficient indicators for immediate endocrinological responses to social and nonsocial behaviours that are not directly linked to energy metabolism.

Sexually dimorphic phrase organization in the song of the indris (Indri indri).

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.

Lactating Coquerel's sifaka (Propithecus coquereli) exhibit reduced stress responses in comparison to males and nonlactating females.

Cortisol is a glucocorticoid hormone that plays a principal role in metabolic function and stress responses in wild primates. Stressors are ubiquitous in environments and elicit a variety of physiological and behavioral responses. While stress responses are adaptive in the short-term, they can have negative effects when experienced over longer durations. As a physiological stressor, the process of lactation is an energetically expensive activity for mammals. Milk production increases water loss and increased hydration demands are amplified in mammalian species inhabiting xeric habitats, including lemur species living in northwestern Madagascar-the region for this research work. Here, sifakas give birth during the dry season (May-October) and wean infants during the subsequent wet season (November-April). The author collected fecal samples during the 24 weeks following infant births in 10 groups of Coquerel's sifaka in Ankarafantsika Park, Madagascar. The author analyzed the samples by comparing the first 12-week time block to the second 12-week time block, which corresponded to the dry and the beginning of the wet seasons, respectively. Analyses were based on 375 samples collected over two birth seasons (2010 and 2011). A linear mixed model determined the relationships between reproductive class and temporal cortisol variation. The three reproductive classes had significantly different cortisol concentrations. Lactating females had lower cortisol than adult males and nonlactating females in all weeks postnatal. Males had significantly higher cortisol in weeks 13-24 relative to weeks 1-12. Examining seasonal changes in cortisol concentrations demonstrates how lemurs respond physiologically to the energetic constraints of lactation during the critical life history stage of infant development.

Getting into Shape: Limb Bone Strength in Perinatal Lemur catta and Propithecus coquereli.

Functional studies of skeletal anatomy are predicated on the fundamental assumption that form will follow function. For instance, previous studies have shown that the femora of specialized leaping primates are more robust than those of more generalized primate quadrupeds. Are such differences solely a plastic response to differential loading patterns during postnatal life, or might they also reflect more canalized developmental mechanisms present at birth? Here, we show that perinatal Lemur catta, an arboreal/terrestrial quadruped, have less robust femora than perinatal Propithecus coquereli, a closely related species specialized for vertical clinging and leaping (a highly unusual locomotor mode in which the hindlimbs are used to launch the animal between vertical tree trunks). These results suggest that functional differences in long bone cross-sectional dimensions are manifest at birth, belying simple interpretations of adult postcranial form as a direct record of loading patterns during postnatal life. Despite these significant differences in bone robusticity, we find that hindlimb bone mineralization, material properties, and measures of whole-bone strength generally overlap in perinatal L. catta and P. coquereli, indicating little differentiation in postcranial maturity at birth despite known differences in the pace of craniodental development between the species. In a broader perspective, our results likely reflect evolution acting during prenatal ontogeny. Even though primates are notable for relatively prolonged gestation and postnatal parental care, neonates are not buffered from selection, perhaps especially in the unpredictable and volatile environment of Madagascar. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 303:250-264, 2020. © 2018 American Association for Anatomy.

Subordination signals improve the quality of social relationships in Verreaux's Sifaka: Implications for the evolution of power structures and social complexity.

OBJECTIVES: Unidirectional dominance-related signals can be used to communicate submission (an immediate behavioral response) or subordination (the status of an established relationship). Subordination signals are defined as emitted during peaceful interactions and are hypothesized to be critical for the evolution of social complexity and robust power structures because they reduce uncertainty in social relationships. The chatter vocalization in Verreaux's sifaka (Propithecus verreauxi) is a unidirectional submissive signal. I tested the hypothesis that chatter vocalizations can signal subordination and thereby reduce agonism in a dyad. MATERIALS AND METHODS: I examined 780 chatters from 18 dyads collected over 881 observation hours on four groups of sifaka in Kirindy Forest, Madagascar. RESULTS: Sifaka emitted 63% of chatters in the peaceful context. Peaceful chatters significantly predicted grooming rate, fighting rate, reconciliation, and proportion of wins in a dyad but did not predict time in proximity. Dyad-type significantly predicted the frequency of peaceful chatters, with intrasexual dyads exhibiting chatters in peaceful contexts more often than intersexual dyads. DISCUSSION: Sifaka communicate both submission and subordination with chatter vocalizations. Subordination signaling increased tolerance and affiliation. It reduced conflicts and the probability dominant individuals usurped resources. Moreover, intrasexual power may be more institutionalized than intersexual power in sifaka. The finding of complex and cognitively demanding social communication in a lemur with low levels of cooperation (1) challenges previous assumptions that the evolution of social complexity is dependent on frequent triadic interactions and high levels of cooperation, and (2) highlights the need for taxonomic diversity in studies of social complexity.

Evidence of genetic monogamy in the lemur Indri (Indri indri).

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.

Morphometric signals of population decline in diademed sifakas occupying degraded rainforest habitat in Madagascar.

Anthropogenic habitat change can have varied impacts on primates, including both negative and positive outcomes. Even when behavioural shifts are seen, they may reflect decreased health, or simply behavioural flexibility; understanding this distinction is important for conservation efforts. This study examines habitat-related variation in adult and immature morphometrics among diademed sifakas (Propithecus diadema). We collected morphometric data from sifakas at Tsinjoarivo, Madagascar (19 years, 188 captures, 113 individuals). Captures spanned 12 groups, five within continuous forest ("CONT"), and seven in degraded fragments ("FRAG") where sifakas have lower nutritional intakes. Few consistent differences were found between CONT and FRAG groups. However, using home range quality as a covariate rather than a CONT/FRAG dichotomy revealed a threshold: the two FRAG groups in the lowest-quality habitat showed low adult mass and condition (wasting), and low immature mass and length (stunting). Though less-disturbed fragments apparently provide viable habitat, we suggest the sifakas in the most challenging habitats cannot evolve fast enough to keep up with such rapid habitat change. We suggest other long-lived organisms will show similar morphometric "warning signs" (wasting in adults, stunting in immatures); selected morphometric variables can thus be useful at gauging vulnerability of populations in the face of anthropogenic change.