Maternal influence on the development of nut-cracking skills in the chimpanzees of the Taï forest, Côte d'Ivoire (Pan troglodytes verus).

Chimpanzees' (Pan troglodytes) nut-cracking behavior represents one of the most complex forms of tool-use known among nonhuman animals. Given the close phylogenetic relationship between these apes and humans, investigating how such complex behavior develops in immatures can reveal the evolutionary roots of the cognitive processes that enabled the evolution of outstanding technological skills in our lineage. In this study, we investigated whether maternal behavior directly enhanced nut-cracking skills in immature individuals. We analyzed the behavior of 11 immatures and their mothers (N = 8) during nut-cracking activity, spanning over three consecutive nut-cracking seasons in the Taï National Park, Côte d'Ivoire. We used generalized linear mixed models to (a) obtain values of maternal scaffolding (defined as provision of learning opportunities) and active nut-sharing behavior of each mother according to the age of their offspring, and their average nut-cracking efficiency; (b) to test whether these variables enhanced immatures' nut-cracking skills; and (c) to test whether immatures' features (age, sex, and begging behavior) influenced maternal behavior as observed in our videos. Although the predicted values of maternal scaffolding and active nut-sharing did not obviously affect immatures' skills, they were positively influenced by the average maternal efficiency and by sharing hammers with their mothers. In addition, our observations showed that mothers were more likely to share nuts with their sons than with their daughters, and the more their offspring begged. Concurrently, male immatures were also found to beg more often than females. Our results add evidence on the ontogenetic pathway leading to the full acquisition of nut-cracking in wild chimpanzees and on the effect that maternal behavior can have in promoting the acquisition of this complex tool-use behavior. Moreover, our study strengthens the importance of naturalistic observations to understand complex skill acquisition. Finally, we suggest future avenues for investigating the maternal influence on learning.

Extraction of honey from underground bee nests by central African chimpanzees (Pan troglodytes troglodytes) in Loango National Park, Gabon: Techniques and individual differences.

A detailed analysis of tool use behaviors can disclose the underlying cognitive traits of the users. We investigated the technique used by wild chimpanzees to extract the underground nests of stingless bees (Meliplebeia lendliana), which represent a hard-to-reach resource given their highly undetectable location. Using remote-sensor camera trap footage, we analyzed 151 visits to 50 different bee nests by 18 adult chimpanzees of both sexes. We quantified the degree of complexity and flexibility of this technique by looking at the behavioral repertoire and at its structural organization. We used Generalized Linear Mixed Models to test whether individuals differed in their action repertoire sizes and in their action sequencing patterns, as well as in their preferences of use of different behavioral elements (namely, actions, and grip types). We found that subjects showed non-randomly organized sequences of actions and that the occurrence of certain actions was predicted by the type of the previous action in the sequences. Subjects did not differ in their repertoire sizes, and all used extractive actions involving tools more often than manual digging. As for the type of grip employed, the grip involving the coordinated use of hands and feet together was most frequently used by all subjects when perforating, and we detected significant individual preferences in this domain. Overall, we describe a highly complex and flexible extractive technique, and propose the existence of inter-individual variation in it. We discuss our results in the light of the evolution of higher cognitive abilities in the human lineage.

Erratum to: Born to sing! Song development in a singing primate.

[This corrects the article DOI: 10.1093/cz/zoab018.].

Consistent diel activity patterns of forest mammals among tropical regions.

An animal's daily use of time (their "diel activity") reflects their adaptations, requirements, and interactions, yet we know little about the underlying processes governing diel activity within and among communities. Here we examine whether community-level activity patterns differ among biogeographic regions, and explore the roles of top-down versus bottom-up processes and thermoregulatory constraints. Using data from systematic camera-trap networks in 16 protected forests across the tropics, we examine the relationships of mammals' diel activity to body mass and trophic guild. Also, we assess the activity relationships within and among guilds. Apart from Neotropical insectivores, guilds exhibited consistent cross-regional activity in relation to body mass. Results indicate that thermoregulation constrains herbivore and insectivore activity (e.g., larger Afrotropical herbivores are ~7 times more likely to be nocturnal than smaller herbivores), while bottom-up processes constrain the activity of carnivores in relation to herbivores, and top-down processes constrain the activity of small omnivores and insectivores in relation to large carnivores' activity. Overall, diel activity of tropical mammal communities appears shaped by similar processes and constraints among regions reflecting body mass and trophic guilds.

Born to sing! Song development in a singing primate.

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 Indris Have Got Rhythm! Timing and Pitch Variation of a Primate Song Examined between Sexes and Age Classes.

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.