Maximum trunk tip force assessment related to trunk position and prehensile 'fingers' implication in African savannah elephants.

African elephants have a wide range of abilities using their trunk. As a muscular hydrostat, and thanks to the two finger-like processes at its tip, this proboscis can both precisely grasp and exert considerable force by wrapping. Yet few studies have attempted to quantify its distal grasping force. Thus, using a device equipped with force sensors and an automatic reward system, the trunk tip pinch force has been quantified in five captive female African savanna elephants. Results showed that the maximum pinch force of the trunk was 86.4 N, which may suggest that this part of the trunk is mainly dedicated to precision grasping. We also highlighted for the first time a difference in force between the two fingers of the trunk, with the dorsal finger predominantly stronger than the ventral finger. Finally, we showed that the position of the trunk, particularly the torsion, influences its force and distribution between the two trunk fingers. All these results are discussed in the light of the trunk's anatomy, and open up new avenues for evolutionary reflection and soft robot grippers.

Effect of the habitat and tusks on trunk grasping techniques in African savannah elephants.

Among tetrapods, grasping is an essential function involved in many vital behaviours. The selective pressures that led to this function were widely investigated in species with prehensile hands and feet. Previous studies namely highlighted a strong effect of item properties but also of the species habitat on manual grasping behaviour. African savannah elephants (Loxodonta africana) are known to display various prehensile abilities and use their trunk in a large diversity of habitats. Composed of muscles and without a rigid structure, the trunk is a muscular hydrostat with great freedom of movement. This multitasking organ is particularly recruited for grasping food items while foraging. Yet, the diet of African savannah elephants varies widely between groups living in different habitats. Moreover, they have tusks alongside the trunk which can assist in grasping behaviours, and their tusk morphologies are known to vary considerably between groups. Therefore, in this study, we investigate the food grasping techniques used by the trunk of two elephant groups that live in different habitats: an arid study site in Etosha National Park in Namibia, and an area with consistent water presence in Kruger National Park in South Africa. We characterised the tusks profiles and compared the grasping techniques and their frequencies of use for different foods. Our results show differences in food-grasping techniques between the two groups. These differences are related to the food item property and tusk profile discrepancies highlighted between the two groups. We suggest that habitat heterogeneity, particularly aridity gaps, may induce these differences. This may reveal an optimisation of grasping types depending on habitat, food size and accessibility, as well as tusk profiles.

Influence of food physical properties and environmental context on manipulative behaviors highlighted by new methodological approaches in zoo-housed bonobos (Pan paniscus).

Research on manipulative abilities in nonhuman primates, in the context of hominid evolution, has mostly focused on manual/pedal postures considered as static behaviors. While these behavioral repertoires highlighted the range of manipulative abilities in many species, manipulation is a dynamic process that mostly involves successive types of grips before reaching its goal. The present study aims to investigate the use of manual/pedal postures in zoo-housed bonobos in diverse dynamic food processing by using an innovative approach: the optimal matching analysis that compares sequences (i.e., succession of grasping postures) with each other. To characterize the manipulative techniques spontaneously employed by bonobos, we performed this sequential analysis of manual/pedal postures during 766 complete feeding sequences of 17 individuals. We analyzed the effectiveness with a score defined by a partial proxy of food intake (i.e., the number of mouthfuls) linked to a handling score measuring both the diversity and changes of manual postures during each sequence. We identified four techniques, used differently depending on the physical substrate on which the individual performed food manipulation and the food physical properties. Our results showed that manipulative techniques were more complex (i.e., higher handling score) for large foods and on substrates with lower stability. But the effectiveness score was not significantly lower for these items since manipulative complexity seemed to be compensated by a greater number of mouthfuls. It appeared that the techniques employed involved a trade-off between manipulative complexity and the amount of food ingested. This study allowed us to test and validate innovative analysis methods that are applicable to diverse ethological studies involving sequential events. Our results bring new data for a better understanding of the evolution of manual abilities in primates in association with different ecological contexts and both terrestrial and arboreal substrates and suggest that social and individual influences need to be explored further.

Chimpanzees select comfortable nesting tree species.

Every evening, chimpanzees build sleeping "nests" in trees. In some studied communities, individuals appear to be selective about the tree species used, which has led researchers to hypothesize whether chimpanzees prefer trees that repel troublesome insects or/and that provide comfortable and stable structures. We investigate these hypotheses, or a trade-off between both, though study of tree species preference based on their biomechanical and/or biochemical properties in the Sebitoli chimpanzee community in Kibale National Park, Uganda. The ten tree species most frequently used for nesting were compared with ten abundant in their environment but not preferred for nesting. For these 20 tree species, we determined their biomechanical and morphological characteristics such as foliar density, foliar units form (shape and size) and branch rigidity. Their spatial repellent activity, previously tested against Anopheles gambiae was incorporated into the analysis. Chimpanzees chose tree species with medium-sized and elongated foliar units, high foliar density and branch with stiffer wood. In addition, most tree species with such mechanical and morphological properties also have mosquito repellent activity. These tree properties may provide a comfortable sleeping environment enhancing sleep quality. Finally, a comparison across chimpanzee communities would be relevant to understand whether these choices are not only ecological but also cultural.

Feeling a bit peckish: Seasonal and opportunistic insectivory for wild gorillas.

OBJECTIVES: Insectivory likely contributed to survival of early humans in diverse conditions and influenced human cognitive evolution through the need to develop harvesting tools. In living primates, insectivory is a widespread behavior and frequently seasonal, although previous studies do not always agree on reasons behind this. Since western gorillas (Gorilla gorilla) diet is largely affected by seasonal variation in fruit availability, we aimed to test three non-mutually exclusive hypotheses (habitat use, frugivory and rainfall) to explain seasonality in termite feeding across age/sex classes in three habituated groups (Nindividuals = 27) in Central Africa. MATERIALS AND METHODS: We used 4 years of ranging, scan and continuous focal sampling records of gorillas (Nranging days = 883, Nscans = 12,384; Nhours = 891) in addition to 116 transects recording vegetation and termite mound distribution. RESULTS: Depending on the age/sex classes, we found support for all three hypotheses. Time spent in termite-rich vegetation positively impacted termite consumption in all age/sex classes, but subadults. Lengthier travels increased termite feeding in females but decreased it in subadults. Frugivory decreased termite consumption in adults. Daily rainfall had a positive effect on termite feeding and foraging in silverbacks and juveniles, but a negative effect in subadults. For females, rainfall had a positive effect on termite feeding, but a negative effect for termite foraging. DISCUSSION: In great apes, seasonal insectivory seems to be multifactorial and primarily opportunistic with important differences among age/sex classes. While insectivory has potentials to be traditional, it likely played a crucial role during primate evolution (including ours), allowing diet flexibility in changing environments.

Survey of ticks and tick-borne pathogens in wild chimpanzee habitat in Western Uganda.

BACKGROUND: Ticks and tick-borne pathogens significantly impact both human and animal health and therefore are of major concern to the scientific community. Knowledge of tick-borne pathogens is crucial for prescription of mitigation measures. In Africa, much research on ticks has focused on domestic animals. Little is known about ticks and their pathogens in wild habitats and wild animals like the endangered chimpanzee, our closest relative. METHODS: In this study, we collected ticks in the forested habitat of a community of 100 chimpanzees living in Kibale National Park, Western Uganda, and assessed how their presence and abundance are influenced by environmental factors. We used non-invasive methods of flagging the vegetation and visual search of ticks both on human team members and in chimpanzee nests. We identified adult and nymph ticks through morphological features. Molecular techniques were used to detect and identify tick-borne piroplasmids and bacterial pathogens. RESULTS: A total of 470 ticks were collected, which led to the identification of seven tick species: Haemaphysalis parmata (68.77%), Amblyomma tholloni (20.70%), Ixodes rasus sensu lato (7.37%), Rhipicephalus dux (1.40%), Haemaphysalis punctaleachi (0.70%), Ixodes muniensis (0.70%) and Amblyomma paulopunctatum (0.35%). The presence of ticks, irrespective of species, was influenced by temperature and type of vegetation but not by relative humidity. Molecular detection revealed the presence of at least six genera of tick-borne pathogens (Babesia, Theileria, Borrelia, Cryptoplasma, Ehrlichia and Rickettsia). The Afrotopical tick Amblyomma tholloni found in one chimpanzee nest was infected by Rickettsia sp. CONCLUSIONS: In conclusion, this study presented ticks and tick-borne pathogens in a Ugandan wildlife habitat whose potential effects on animal health remain to be elucidated.

Measuring the force of the tip of the elephants trunk.

Forces that animals can exert is of great interest in biology. Regarding the elephant trunk, the maximum mass that an elephant can lift with its trunk is known, but the pinching force of the trunk tip is unknown. We here present an original system to measure this force for an organ much coveted in soft robotics for example. It consists of:•A wooden box protecting the elephants and the measuring system with no protruding parts except the sensor. This box has an opening at the back to fill it with apples and a trap door at the front to release the apples.•Two load cells protruding from the box connected to an electronic system controlled by an Arduino card that records and sends the pinch force via Wi-Fi to a laptop while releasing a reward apple.•Depending on the threshold chosen, the elephant must pinch harder than the previous time to release the next apple. The repetition of this action allows us to approach the maximum force it can achieve.The system, tested on elephants at the Beauval Zooparc (France), has demonstrated that it is effective in measuring the pinching force of the tip of the trunk.

Repellent activity against Anopheles gambiae of the leaves of nesting trees in the Sebitoli chimpanzee community of Kibale National Park, Uganda.

BACKGROUND: Every evening, chimpanzees (Pan troglodytes) build a sleeping platform so called "nest" by intertwining branches of tree. Most of chimpanzees' communities studied have a preference for tree species in which they nest. As female mosquitoes are feeding on the blood of their host at nighttime, chimpanzees may prevent being disturbed and bitten by mosquitoes by selecting tree species having properties to repel them. METHODS: To test the hypothesis that chimpanzees choose tree species for their aromatic properties, data related to 1,081 nesting trees built between 2017 and 2019 in the Sebitoli community of Kibale National Park (Uganda) were analysed. The 10 most used trees were compared to the 10 most common trees in the habitat that were not preferred for nesting. Leaves from the 20 trees species were collected and hydro-distillated to obtain essential oils and one of the by-products for behavioural bioassays against females of the African mosquito, Anopheles gambiae. RESULTS: Sebitoli chimpanzees showed tree preferences: 10 species correspond to more than 80% of the nesting trees. Out of the essential oil obtained from the 10 nesting trees, 7 extracts for at least one concentration tested showed spatial repellency, 7 were irritant by contact and none were toxic. In the other hand, for the abundant trees in their habitat not used by chimpanzees, only 3 were repellent and 5 irritants. DISCUSSION AND CONCLUSION: This study contributes to evidence that chimpanzees, to avoid annoying mosquitoes, may select their nesting trees according to their repellent properties (linked to chemical parameters), a potential inspiration for human health.

Free hand hitting of stone-like objects in wild gorillas.

The earliest stone tool types, sharp flakes knapped from stone cores, are assumed to have played a crucial role in human cognitive evolution. Flaked stone tools have been observed to be accidentally produced when wild monkeys use handheld stones as tools. Holding a stone core in hand and hitting it with another in the absence of flaking, free hand hitting, has been considered a requirement for producing sharp stone flakes by hitting stone on stone, free hand percussion. We report on five observations of free hand hitting behavior in two wild western gorillas, using stone-like objects (pieces of termite mound). Gorillas are therefore the second non-human lineage primate showing free-hand hitting behavior in the wild, and ours is the first report for free hand hitting behavior in wild apes. This study helps to shed light on the morphofunctional and cognitive requirements for the emergence of stone tool production as it shows that a prerequisite for free hand percussion (namely, free hand hitting) is part of the spontaneous behavioral repertoire of one of humans' closest relatives (gorillas). However, the ability to combine free hand hitting with the force, precision, and accuracy needed to facilitate conchoidal fracture in free hand percussion may still have been a critical watershed for hominin evolution.

The relationship between distal trunk morphology and object grasping in the African savannah elephant (Loxodonta africana).

Background: During reach-to-grasp movements, the human hand is preshaped depending on the properties of the object. Preshaping may result from learning, morphology, or motor control variability and can confer a selective advantage on that individual or species. This preshaping ability is known in several mammals (i.e., primates, carnivores and rodents). However, apart from the tongue preshaping of lizards and chameleons, little is known about preshaping of other grasping appendages. In particular, the elephant trunk, a muscular hydrostat, has impressive grasping skills and thus is commonly called a hand. Data on elephant trunk grasping strategies are scarce, and nothing is known about whether elephants preshape their trunk tip according to the properties of their food. Methods: To determine the influence of food sizes and shapes on the form of the trunk tip, we investigated the morphology of the distal part of the trunk during grasping movements. The influence of food item form on trunk tip shape was quantified in six female African savannah elephants (Loxodonta africana). Three food item types were presented to the elephants (elongated, flat, and cubic), as well as three different sizes of cubic items. A total of 107 ± 10 grips per individual were video recorded, and the related trunk tip shapes were recorded with a 2D geometric morphometric approach. Results: Half of the individuals adjusted the shape of the distal part of their trunk according to the object type. Of the three elephants that did not preshape their trunk tip, one was blind and another was subadult. Discussion and perspectives: We found that elephants preshaped their trunk tip, similar to the preshaping of other species' hands or paws during reach-to-grasp movements. This preshaping may be influenced by visual feedback and individual learning. To confirm these results, this study could be replicated with a larger sample of elephants.

Manipulative repertoire of bonobos (Pan paniscus) in spontaneous feeding situation.

Comparative behavioral studies of hand use amongst primate species, including humans, have been central in research on evolutionary mechanisms. In particular, the manipulative abilities of our closest relatives, the chimpanzee (Pan troglodytes), have been widely described in various contexts, showing a high level of dexterity both in zoo and in natural conditions. In contrast, the study of bonobos' manipulative abilities has almost exclusively been carried out in experimental contexts related to tool use. The objective of the present study is to describe the richness of the manipulative repertoire of zoo-housed bonobos, in a spontaneous feeding context including various physical substrates to gain a larger insight into our evolutionary past. Our study describes a great variety of grasping postures and grip associations in bonobos, close to the range of manipulative repertoire in chimpanzees, confirming that the two species are not markedly different in terms of cognitive and morphological constraints associated with food manipulation. We also observed differences in manipulative behaviors between juveniles and adults, indicating a greater diversity in grip associations and grasping postures used in isolation with age, and a sex-biased use of tools with females using tools more often than males. These results are consistent with the previous results in the Pan genus and reinforce the hypothesis that the evolutionary mechanisms underlying the flexibility of manipulative behaviors are shared by both species and that these ecological strategies would have already evolved in their common ancestor.

Maternal cradling bias in baboons: The first environmental factor affecting early infant handedness development?

The most emblematic behavioral manifestation of human brain asymmetries is handedness. While the precise mechanisms behind the development of handedness are still widely debated, empirical evidences highlight that besides genetic factors, environmental factors may play a crucial role. As one of these factors, maternal cradling behavior may play a key role in the emergence of early handedness in the offspring. In the present study we followed 41 Papio anubis infants living in social groups with their mother for which direction (e.g., left- or right-arm) and degree of maternal cradling-side bias were available from a previous published study. We assessed hand preferences for an unimanual grasping task at three developmental stages: (A) 0-4, (B) 4-6, and (C) 9-10 months of age. We found that individual hand preferences for grasping exist as soon as the first months of age, with a population-level left-handedness predominance, being stable until 6 months; to wit the period during which juveniles are mainly carried by their mothers. More importantly, this early postnatal handedness is positively correlated with maternal cradling lateralization. Interestingly, hand preferences assessed later in the development, once juveniles are no longer carried (i.e., from 9 to 10 months of age), are less dependent from the maternal cradling bias and less consistent with the earlier developmental stages, especially in infants initially cradled on the right maternal side. Our findings suggest that the ontogenetic dynamics of the infant's hand preference and its changes might ultimately rely on the degree of infant dependence from the mother across development.

Analogous laterality in trunk movements in captive African elephants: A pilot study.

Lateralization of hand use in primates has been extensively studied in a variety of contexts, and starts to be investigated in other species and organs in order to understand the evolution of the laterality according to different tasks. In elephants, the orientation of the movements of the trunk has been observed mainly in feeding and social contexts, in free conditions. However, little is known about the influence of task complexity on trunk laterality. In this study, we compared the lateralization of the trunk in two conditions: standardized and free. We offered granules to six African elephants on each side of an opened trapdoor to create a constraining environment and reported the different behaviours employed and their orientation. In addition, we observed the same individuals in free conditions and noted the lateralization of the use of their trunk. We revealed a common right side preference in all our elephants, both in standardized and free conditions. This side bias was stronger in our constraining task, adding evidence for the task complexity theory. We finally described laterality in new behaviours in the literature on elephants, such as pinching, gathering or exploration with the trunk.

No evidence for female kin association, indications for extragroup paternity, and sex-biased dispersal patterns in wild western gorillas.

Characterizing animal dispersal patterns and the rational behind individuals' transfer choices is a long-standing question of interest in evolutionary biology. In wild western gorillas (Gorilla gorilla), a one-male polygynous species, previous genetic findings suggested that, when dispersing, females might favor groups with female kin to promote cooperation, resulting in higher-than-expected within-group female relatedness. The extent of male dispersal remains unclear with studies showing conflicting results. To investigate male and female dispersal patterns and extragroup paternity, we analyzed long-term field observations, including female spatial proximity data, together with genetic data (10 autosomal microsatellites) on individuals from a unique set of four habituated western gorilla groups, and four additional extragroup males (49 individuals in total). The majority of offspring (25 of 27) were sired by the group male. For two offspring, evidence for extragroup paternity was found. Contrarily to previous findings, adult females were not significantly more related within groups than across groups. Consistently, adult female relatedness within groups did not correlate with their spatial proximity inferred from behavioral data. Adult females were similarly related to adult males from their group than from other groups. Using R ST statistics, we found significant genetic structure and a pattern of isolation by distance, indicating limited dispersal in this species. Comparing relatedness among females and among males revealed that males disperse farer than females, as expected in a polygamous species. Our study on habituated western gorillas shed light on the dispersal dynamics and reproductive behavior of this polygynous species and challenge some of the previous results based on unhabituated groups.

Exploring the behavioral reactions to a mirror in the nocturnal grey mouse lemur: sex differences in avoidance.

Most mirror-image stimulation studies (MIS) have been conducted on social and diurnal animals in order to explore self-recognition, social responses, and personality traits. Small, nocturnal mammals are difficult to study in the wild and are under-represented in experimental behavioral studies. In this pilot study, we explored the behavioral reaction of a small nocturnal solitary forager-the grey mouse lemur (Microcebus murinus)-an emergent animal model in captivity. We assessed whether MIS can be used to detect a repeatable behavioral reaction, whether individuals will present a similar reaction toward a conspecific and the mirror, and whether males and females respond similarly. We tested 12 individuals (six males and six females) twice in three different contexts: with a mirror, with a live conspecific, and with a white board as a neutral control. We detected significant repeatability for the activity component of the behavioral reaction. There was a significant effect of the context and the interaction between presentation context and sex for avoidance during the first session for males but not for females. Males avoided the mirror more than they avoided a live conspecific. This pilot study opens a discussion on the behavioral differences between males and females regarding social interactions and reproduction in the nocturnal solitary species, and suggests that males are more sensitive to context of stimulation than females.

Increased performance in juvenile baboons is consistent with ontogenetic changes in morphology.

OBJECTIVES: In many primates, the greater proportion of climbing and suspensory behaviors in the juvenile repertoire likely necessitates good grasping capacities. Here, we tested whether very young individuals show near-maximal levels of grasping strength, and whether such an early onset of grasping performance could be explained by ontogenetic variability in the morphology of the limbs in baboons. MATERIAL AND METHODS: We quantified a performance trait, hand pull strength, at the juvenile and adult stages in a cross-sectional sample of 15 olive baboons (Papio anubis). We also quantified bone dimensions (i.e., lengths, widths, and heights) of the fore- (n = 25) and hind limb (n = 21) elements based on osteological collections covering the whole development of olive baboons. RESULTS: One-year old individuals demonstrated very high pull strengths (i.e., 200% of the adult performance, relative to body mass), that are consistent with relatively wider phalanges and digit joints in juveniles. The mature proportions and shape of the forelimb elements appeared only at full adulthood (i.e., ≥4.5 years), whereas the mature hind limb proportions and shape were observed much earlier during development. DISCUSSION: These changes in limb performance and morphology across ontogeny may be explained with regard to behavioral transitions that olive baboons experience during their development. Our findings highlight the effect of infant clinging to mother, an often-neglected feature when discussing the origins of grasping in primates. The differences in growth patterns, we found between the forelimb and the hind limb further illustrate their different functional roles, having likely evolved under different ecological pressures (manipulation and locomotion, respectively).

The implications of thumb movements for Neanderthal and modern human manipulation.

Much research has debated the technological abilities of Neanderthals relative to those of early modern humans, with a particular focus on subtle differences in thumb morphology and how this may reflect differences in manipulative behaviors in these two species. Here, we provide a novel perspective on this debate through a 3D geometric morphometric analysis of shape covariation between the trapezial and proximal first metacarpal articular surfaces of Neanderthals (Homo neanderthalensis) in comparison to early and recent humans (Homo sapiens). Results show a distinct pattern of shape covariation in Neanderthals, consistent with more extended and adducted thumb postures that may reflect habitual use of grips commonly used for hafted tools. Both Neanderthals and recent humans demonstrate high intraspecific variation in shape covariation. This intraspecific variation is likely the result of genetic and/or developmental differences, but may also reflect, in part, differing functional requirements imposed by the use of varied tool-kits. These results underscore the importance of holistic joint shape analysis for understanding the functional capabilities and evolution of the modern human thumb.

Behavioural variability among captive African elephants in the use of the trunk while feeding.

The Proboscideans, an order of mammals including elephants, are the largest of the Earth lands animals. One probable consequence of the rapid increase of their body size is the development of the trunk, a multitask highly sensitive organ used in a large repertoire of behaviours. The absence of bones in the trunk allows a substantial degree of freedom for movement in all directions, and this ability could underlie individual-level strategies. We hypothesised a stronger behavioural variability in simple tasks, and a correlation between the employed behaviours and the shape and size of the food. The observations of a captive group of African elephants allowed us to create a complete catalogue of trunk movements in feeding activities. We noted manipulative strategies and impact of food item properties on the performed behaviours. The results show that a given item is manipulated with a small panel of behaviours, and some behaviours are specific to a single shape of items. The study of the five main feeding behaviours emphasises a significant variability between the elephants. Each individual differed from every other individual in the proportion of at least one behaviour, and every behaviour was performed in different proportions by the elephants. Our findings suggest that during their lives elephants develop individual strategies adapted to the manipulated items, which increases their feeding efficiency.

Human-like maternal left-cradling bias in monkeys is altered by social pressure.

About 66-72% of human mothers cradle their infants on their left side. Given that left-cradling exposes the baby's face to the mother's left visual field (i.e., mainly projected to her right hemisphere) and is altered by emotional states such as stress, maternal left-cradling was interpreted as reflecting right-hemispheric dominance for emotional processing. Whether this phenomenon is unique to human evolution is still in debate. In the present study we followed 44 olive baboon (Papio anubis) mothers and their infants in different social groups. We found that a maternal cradling bias exists and is predominantly towards the left in a similar proportion as in humans, but shifts toward a right bias in mothers living in high density groups. The sensitivity of left-cradling to social pressure highlights its potential links with the mother's stress as reported in humans. Our finding clearly illustrates the phylogenetic continuity between humans and Old-World monkeys concerning this lateralization and its potential links with hemispheric specialization for emotions, inherited from a common ancestor 25-35 million years ago.