PRIMATES

Maternal exploitation: impact of maternal food snatching behaviour on the growth of their offspring in Japanese macaques
Kurita H
There is little information on maternal behaviour that deprives offspring of food, but some Japanese macaque, Macaca fuscata, mothers have been observed to snatch food from their offspring and eat it. This study investigated maternal food snatching behaviour (MFSB) and its impact on the growth of their offspring in provisioned, free-ranging Japanese macaques. The amount of food a mother snatched from her offspring was estimated to be 51.2% by dry weight compared to the amount of solid food an infant of the same age took in. Body mass growth of affected infants indicated a below-average mass gain. The study suggests that MFSB might be a pathological behaviour and provides the first detailed account of parental exploitation in animals.
Mantled howler monkeys (Alouatta palliata) alter activity and spatial cohesion across a continuous forest and forest fragment in Costa Rica
Miller RL, Kaser FVE, Belmont RE, Ennis M, Voss KA, Bolt LM and Schreier AL
Habitat loss due to deforestation is a primary threat to global biodiversity. Clearing tropical rainforests for agriculture or development leads to forest fragmentation. Forest fragments contain fewer large trees and provide lower food availability for primates compared to continuous forests. Mantled howler monkeys (Alouatta palliata) inhabit fragmented rainforests and may need to alter their activity budgets and spatial cohesion to mitigate competition and conserve energy in fragments where food quality is lower. We compared howler monkey activity and spatial cohesion across a small forest fragment (La Suerte Biological Research Station, LSBRS) and a large, continuous forest (La Selva Research Station) in Costa Rica. We predicted that monkeys at LSBRS would rest more, feed more, travel less, and be less spatially cohesive compared to La Selva to contend with fewer resources in the small fragment. Using instantaneous scan sampling at 2-min intervals during 30-min focal samples, we recorded activity and the number of individuals within 5 m of the focal animal. We collected 1505 h of data from 2017-2024. Monkey activity and spatial cohesion differed significantly across sites. As predicted, monkeys at LSBRS spent more time feeding than at La Selva, but contrary to our predictions, they rested less and traveled more. The mean number of individuals within 5 m was significantly lower at LSBRS compared to La Selva. The ability to modify their activity and spatial cohesion in response to fragmentation provides insight into how primates can contend with fewer resources and higher competition in changing ecosystems worldwide.
Urinary health indicators in folivorous-frugivorous primates with and without food supplementation
Back JP and Bicca-Marques JC
Food supplementation by humans in peri-urban and urban landscapes can lead to excessive intake of energy and certain macronutrients, and affect animal health. In this study, we evaluated the influence of food supplementation on urinary health indicators in brown howler monkeys (Alouatta guariba) by comparing supplemented and non-supplemented free-ranging peri-urban groups. We also evaluated the effect of sex, day shift, and season of sampling. Between August 2021 and August 2022, we non-invasively collected 61 samples (43 from females and 18 from males) from adult individuals (N = 10) in three supplemented groups and 56 samples (25 from females and 31 from males) from adults (N = 7) in three non-supplemented groups. The supplements, mostly raw foods (e.g., fruits, vegetables, and tubers) and bread, represented 18% of the total fresh mass ingested by the supplemented groups. We assessed pH, density, and the presence of eight urine components (glucose, bilirubin, ketones, protein, urobilinogen, nitrite, blood, and leukocytes) using reagent urine strips. Season of sampling predicted urine density (mean = 1.022), while both season and day shift predicted pH (mean = 6.5). The occurrence of supplementation was a weak predictor of these parameters. Finally, we detected leukocytes in 21% of the 117 samples. We did not identify any visible signs of disease in any individual throughout the study and found no clinical changes in urine under the conditions studied. We urge validation of the results with urine strips to facilitate monitoring of the health of howler monkeys living in anthropogenic landscapes in the presence or absence of dietary supplementation.
Using occupancy modeling to provide insights into suitable habitat characteristics for the already restricted and critically endangered Olalla's titi monkey (Plecturocebus olallae)
Martínez J, Márquez R, Reinaga A, Campera M, Nijman V and Wallace RB
Knowledge about changes in wildlife populations over time is essential for making informed decisions regarding their conservation. We evaluated the influence of distinct habitat factors on the occupancy of Olalla's titi monkey (Plecturocebus olallae), a Critically Endangered primate endemic to Bolivia. We assessed the presence of titi monkey groups using the playback technique, employing point counts in 582 quadrants of approximately 6.25 hectares. Utilizing single-species and single-season occupancy models, we estimated an occupancy (ψ) of 0.21 and found that the presence of P. olallae groups was positively related to heterogenous plant composition forests which indicates they may be more likely to occur in areas of high floristic diversity. We also found that groups of this already range restricted species do not occur in all the forest coverage within their distributional range. This complements previous considerations regarding the habitat in which P. olallae occurs based on its natural history knowledge and highlights the limited suitable habitat for this species. From our sampling effort, we calculated a power of 81% to detect a population change of 30%, showing the potential of occupancy modeling for population monitoring of P. olallae. Thus, we provide an information baseline that will be useful in further population monitoring actions for the conservation of these endemic Bolivian titi monkeys.
A case report on ranging pattern of a solitary male macaque in urban area
Tsuji Y and Kawazoe T
Information on the life histories of male macaques after leaving their natal troops is limited. A solitary male Japanese macaque (Macaca fuscata), estimated to be 5 years old, appeared in the urban area of Ishinomaki City, Miyagi Prefecture, northern Japan, where no troops are distributed, in May 2023. Because the animal was habituated to and fed frequently on garden crops, it likely came from the western part of the prefecture, where multiple crop-feeding troops are distributed. The male stayed in the hilly area in the central part of the city until June and then moved north in July. The male moved south to the tip of the Oshika Peninsula and returned to the urban area in August, after which the location of the male was unknown. This study demonstrated that (1) male macaques can move > 40 km from their natal troop, (2) the daily travel distance (average: 0.9 km) of solitary males was similar to that of troop animals, whereas the home-range size of solitary males was much bigger than that for single animals, and (3) the home-range location of solitary males changes quickly. These results implied that solitary males in novel environments prioritize finding new troops to join. Our study sheds light on aspects of male life history after dispersal.
Male adoption in the black and gold howler monkey (Alouatta caraya)
Gilles DR, Bay-Jouliá R, Sánchez-Gavier F and Kowalewski MM
Infant adoption is an association that occurs between an adult individual and a dependent infant and occurs most often when lactating females care for a nutritionally dependent infant that is not her offspring. Adult females are often involved in adoption; while, direct infant care by males occurs in less than 5% of all mammalian species. We report the first record of adoption by wild male adults of Alouatta caraya, a platyrrhine primate species that does not typically participate in parental care. We observed two independent cases of adoption, in two different groups (G1, G2) at the Corrientes Biological Station, Argentina. After the death of two adult females with dependent infants, one adult male adopted an orphan in each group. We recorded the activity of the adoptive males and the two infants. During this period, adoptive males expressed parental care behaviors toward infants. However, after 38 days in G1 and 53 days in G2, both infants died. Based on our continuous monitoring of study groups, we suggest that adoptive males are the biological parents of the orphaned infants. As such, kin selection may explain the care of the infants. However, another explanation could be group familiarity, which refers to the social bonds and cohesion that develop among individuals within a group, even if they are not genetically related. An adult male, although not genetically related to the infants, may take care of them due to the cohesion and relationships established within the group during his period of residence. The study of these rare parental behaviors taken by A. caraya adult males provide insights into the knowledge of group social cohesion and structure.
The relationship of coping style and social support variation to glucocorticoid metabolites in wild olive baboons (Papio anubis)
Pritchard AJ, Vogel ER, Blersch RA and Palombit RA
Social support, via investment in relationships of importance with others, is often emphasized as a pathway towards mediating stress. The effectiveness of social support, however, can be altered by personality differences, but the physiological consequences of such covariation are still poorly explored. How do individual differences in the functioning of the stress response system mediate access to, and use of, social support? To examine this dynamic, we investigated glucocorticoids as a biomarker of energetic activation that may also be activated by chronic psychosocial stress. For this purpose, we studied a wild anthropoid primate, i.e. the olive baboon (Papio anubis), for 17 months, in Laikipia District, Kenya. We measured biomarkers of energetic activation, i.e., fecal glucocorticoid metabolites (fGCms), to address whether individual differences in stress coping and social support were associated with variation in hormone levels across a period from 2018 to 2019. We found evidence for an association between social support and fGCm concentrations. This association had a discernable interaction between sex and social support: we found a negative association in male baboons, relative to females-who did not have a pronounced effect. Our findings emphasize the importance of social support in male baboons. The cost of not having diverse bonds, has been downplayed in male baboons.
Metacognition in nonhuman primates: a review of current knowledge
Subias L, Katsu N and Yamada K
Metacognition, the ability to monitor and control one's own cognitive processes, has long been considered a hallmark of human cognition. However, two decades of research have provided compelling evidence of metacognitive-like abilities in some nonhuman primates. This review synthesizes current knowledge on the subject, highlighting key experimental paradigms and empirical findings, with an emphasis on the latest studies. Thanks to advances in methods and efforts to counter alternative explanations, there is now a consensus that great apes and some macaque species can monitor and control some of their cognitive processes. Despite numerous investigations, however, whether capuchin monkeys are metacognitive remains unclear. Critical gaps persist in our understanding of metacognition across species. We discuss the importance of expanding research to include a wider range of primate species and the potential role of ecological factors in shaping metacognitive capacities. In addition, we consider some promising avenues for future research, including neurophysiological approaches, studies of metacognitive errors, and field experiments.
From stones to sketches: investigating tracing behaviours in Japanese macaques
Sueur C
The use of complex technologies by humans (Homo sapiens) and their ancestors is a key feature of our evolution, marked by the appearance of stone tools 3.3-million years ago. These technologies reflect cognitive complexity and an advanced understanding of materials and mechanics. Studying current primates, especially those that use stones, offers insights into the evolution of human behaviours. In particular, stone manipulation by macaques suggests that some complex behaviours in humans, such as creation of cutting and biface tools, could have emerged unintentionally. The Japanese macaques (Macaca fuscata) of Shodoshima were observed to leave marks on the ground with stones and chalk. By analysing this manipulation of stones, I suggest that drawing in humans could have appeared unintentionally; these unintentional origins of mark-making behaviours may represent early precursors to human drawing.
Nest raiding by bonnet macaques (Macaca radiata) and the response of nest guarding birds in a suburban habitat
Govindharaj V, Herald Victor MBB, Garber PA and Parthasarathy TN
In many primate species, nest raiding is a form of opportunistic foraging behavior designed to acquire protein-rich eggs and nestlings. In urban environments, this is a significant cause of nest failure in birds. Here, we describe nest raiding and egg predation in bonnet macaques (Macaca radiata) inhabiting a suburban area of Salem, Tamil Nadu, India. During nest raiding, large-billed crows (Corvus macrorhynchos) and house crows (Corvus splendens), actively defended their nest from the macaques. When several macaque foragers jointly raided the nest, they were successful in obtaining and consuming the eggs. In contrast, when a solitary macaque attempted to raid the nest, it was unsuccessful. Bird size appeared to play an important role in nest defense. Small birds, such as the scaly breasted munia (Lonchura punctulata) and the purple sunbird (Cinnyris asiaticus) were not able to protect their nests from lone bonnet macaques. These observations indicate that in urban landscapes, bonnet macaques are egg predators of many bird species. When macaques coordinate their actions and forage in small subgroups, they were more successful in preying on the eggs of larger-bodied bird species.
A three-dimensional kinematic analysis of bipedal walking in a white-handed gibbon (Hylobates lar) on a horizontal pole and flat surface
Fujiwara T, Ito K, Shitara T and Nakano Y
Gibbons, a type of lesser ape, are brachiators but also walk bipedally and without forelimb assistance, not only on the ground but also on tree branches. The arboreal bipedal walking strategy of the gibbons has been studied in previous studies in relation to two-dimensional (2D) kinematic analysis. However, because tree branches and the ground differ greatly in width, leading to a constrained foot contact point on the tree branches, gibbons must adjust their 3D joint motions of trunk and hindlimb on the tree branches. Furthermore, these motor adjustments could help minimize the center of mass (CoM) mediolateral displacement. This study investigated the kinematic adjustment mechanism necessary to enable a gibbon to walk bipedally on an arboreal-like substrate using 3D measurements. Trials were recorded with eight video cameras that were placed around the substrate. The CoM position on the body, the Cardan angles of the hindlimb joints and trunk, and spatiotemporal parameters were calculated. Asymmetry of thorax, pelvis, trunk, and left and right hindlimb joint motion was observed in the pole and flat conditions. In the pole condition, the narrower step width and the smaller range of motion of the mediolateral CoM displacement were observed with increased hip adduction and knee eversion angles. These kinematic adjustments might place the knee and foot directly under the body during the single support phase, producing a reduced step width and the amount of the mediolateral CoM displacement of a gibbon.
The presence of experienced individuals enhance the behavior and survival of reintroduced woolly monkeys in Colombia
Gómez-Muñoz M, Ramírez MA, Pérez-Torres J and Stevenson PR
Primate populations are under threat due to human activities, like illegal trafficking, requiring conservation efforts such as reintroduction programs. However, these initiatives often encounter challenges, such as aspects of individual behavior related to movement and foraging. The presence of experienced conspecifics has been suggested to improve the success of these programs. This study focuses on woolly monkeys and examines how the presence of experienced conspecifics influences the performance of reintroduced individuals. Focal animal sampling was used to collect data on proximity, diet composition, home range, and use of vertical strata of three groups of reintroduced woolly monkeys. Data was analyzed for the first 2 and 6 months after release of individuals. The results reveal that the involvement of experienced conspecifics speeds up the process of adaptation, particularly in terms of diet diversity and spatial utilization; however, differences in individual responses were also prevalent. Our findings highlight the importance of incorporating individuals with prior wild experience into reintroduction groups for improving the likelihood of success. Additionally, the study underscores the role of social learning in captive management practices, aiding in post-release behavioral adaptation and survival. This research offers valuable insights for primate conservation, emphasizing the significance of considering the presence of experienced individuals and possible social learning processes in the planning and execution of effective reintroduction efforts.
Dance displays in gibbons: biological and linguistic perspectives on structured, intentional, and rhythmic body movement
Coye C, Caspar KR and Patel-Grosz P
Female crested gibbons (genus Nomascus) perform conspicuous sequences of twitching movements involving the rump and extremities. However, these dances have attracted little scientific attention and their structure and meaning remain largely obscure. Here we analyse close-range video recordings of captive crested gibbons, extracting descriptions of dance in four species (N. annamensis, N. gabriellae, N. leucogenys and N. siki). In addition, we report results from a survey amongst relevant professionals clarifying behavioural contexts of dance in captive and wild crested gibbons. Our results demonstrate that dances in Nomascus represent a common and intentional form of visual communication restricted to sexually mature females. Whilst primarily used as a proceptive signal to solicit copulation, dances occur in a wide range of contexts related to arousal and/or frustration in captivity. A linguistically informed view of this sequential behaviour demonstrates that movement within dances is organized in groups and follows an isochronous rhythm - patterns not described for visual displays in other non-human primates. We argue that applying the concept of dance to gibbons allows us to expand our understanding of communication in non-human primates and to develop hypotheses on the rules and regularities characterising it. We propose that crested gibbon dances likely evolved from less elaborate rhythmic proceptive signals, similar to those found in siamangs. Although dance displays in humans and crested gibbons share a number of key characteristics, they cannot be assumed to be homologous. Nevertheless, gibbon dances represent a striking model behaviour to investigate the use of complex gestural signals in hominoid primates.
Domestic chicken predation and prey sharing by urban capuchin monkeys (Sapajus sp.)
Bender D and Aguiar LM
Capuchin monkeys are omnivorous platyrrhines with a high frequency of faunivory and can survive in urban forest fragments. Predation of wild vertebrates (high-quality foods) by capuchin monkeys has been frequently reported in many species of Cebus and Sapajus. However, predation of domestic animals is unknown. We describe a rare episode of predation, consumption, and sharing of an adult domestic chicken (Gallus gallus domesticus) by individuals from a social group of robust capuchin monkeys (Sapajus sp.) living in a small urban park in the city of Foz do Iguaçu, southern Brazil. This relatively large prey is freely farmed at the study site. The capture, slaughter, preparation (removal of feathers from the body), and consumption of the prey by the capuchins lasted 22 min. The dominant adult male ate the chicken's head and tolerated the approach of two juveniles. The juveniles shared the remainder of the prey after the adult abandoned it. These juveniles scared other group members that approached the carcass. We recorded an opportunistic hunt for easily accessible domestic prey, a case of human resource use by urban primates that shared passively the atypical and valuable food. Though a rare event, the predation on a domestic animal indicates a potential source of conflict with humans that can have negative impacts on urban primates.
Influence of ecological and social factors on huddling behaviour and cluster organisation in Japanese macaques (Macaca fuscata)
Herbrich M, Sands E, Ishizuka S, Kaigaishi Y, Yamamoto S and Sueur C
Huddling behaviour is present in many animal species. This behaviour involves maintaining close physical contact with conspecifics to minimise heat loss and, in general, reduce energy expenditure. Additionally, this behaviour also facilitates complex social interactions within a population. In Japanese macaques, this behaviour is observed in many populations across Japan, including Shodoshima, where huddling clusters can reach up to 100 individuals in winter. Based on several studies on this species, it appears that huddling, or sarudango in Japanese, is influenced by both meteorological factors and social relationships between individuals. The objective of this study is to understand the determinants that drive the expression (presence or absence) and the organisation (number of individuals and identities) of huddling clusters. Two hypotheses were formulated. The first hypothesis posits that the formation and variations in the size and number of clusters are influenced by meteorological factors, while the second hypothesis suggests that the number and position of individuals within a cluster are related to existing relationships between individuals. To test these, data on the number, size, and individuals composing a cluster were collected, allowing building huddling social networks. Simultaneously, meteorological measurements were taken, along with observations on dominance and grooming interactions between individuals. This allowed us to create several statistical models and social networks for comparison. Our results suggest that the probability for observing huddling is mainly related to solar radiation energy, while variations in number and size could be explained by temperature. Moreover, the organisation within a cluster is not random but reflects relationships between individuals. The ones sharing more grooming and having similar dominance ranks have more probabilities to be in the same huddling cluster.
Monkey-deer rodeo: exploring the mounting behaviours of Japanese macaques (Macaca fuscata) on Sika deer (Cervus nippon)
Depret L, Ohshima A, Allanic M, Leca JB, Gunst N and Sueur C
Interspecies interactions present diverse forms and functions, contributing significantly to ecological and social dynamics. This study focuses on the mounting behaviours of Japanese macaques (Macaca fuscata) towards Sika deer (Cervus nippon), a rare and still unexplained phenomenon, with minimal emphasis on the behaviour of the deer. Using video data from two distinct sites, Yakushima and Minoh, Japan, we documented 45 sequences of macaque-deer interactions and analysed macaques' behaviours and deer behaviours using focal and behavioural sampling techniques. We identified four primary activities performed by macaques during mountings-sexual, play, grooming, and resting-with resting being predominant. The study evaluates six hypotheses regarding the functions of these mounting behaviours: (1) interactions are sex-specific, (2) macaques use deer for transportation, (3) mutual warming through physical contact occurs, (4) deer provide support for resting, (5) macaques engage in grooming to consume parasites or play to strengthen interspecies bonds, and (6) aggressive signals relate to resource disputes or rejection of mounting behaviour. Statistical analyses using the Kruskal-Wallis test and Dunn's post-hoc test revealed significant differences between resting and other active behaviours, but no significant differences in behaviour duration between lying and sitting positions. Adults engaged in mounting for longer periods than juveniles, suggesting potential age-related differences in social and reproductive roles. These findings enhance our understanding of interspecies interactions by focusing on macaque behaviours and emphasise the need for longitudinal studies to clarify the ecological and social implications of these interactions.
A brief history of primate research in the Ndoki forest
Morgan D, Malonga R, Agnagna M, Onononga JR, Yako V, Mokoko Ikonga J, Stokes EJ, Eyana Ayina C, Funkhouser JA, Judson K, Villioth J, Nishihara T and Sanz C
The Nouabalé-Ndoki National Park (NNNP) in Republic of Congo has become a beacon for conservation in Central Africa. This manuscript documents the arrival of primatologists, the establishment of field stations and major discoveries in primate behavior and ecology. Field stations were strategically established to study primate behavior in a variety of different contexts from stationary platforms to forest follows of habituated groups. The implementation of new technologies and analyses have also been a hallmark of research at Ndoki. Scientists are shaping a new era in primatology at NNNP by building on past successes and promoting the next generation of Congolese conservationists to address environmental challenges. Results have proven crucial in discussions with government and industry and led to conservation gains such as the inclusion of the intact forests of the Goualougo and Djéké Triangles into the NNNP. The research stations have also become essential for developing a long-term certified sustainable international gorilla tourism program. Despite the many advancements for conservation such as increased protection of forests, development of internationally recognized protocols and large-scale capacity building initiatives, there are reasons for considerable concern in the near- and long-term for primates and their forest habitats in the Ndoki landscape. To address these concerns, we emphasize the long history of forming partnerships with local communities. We also discuss shared overlap featuring multicultural and environmental use of forest resources that is likely to be crucial in championing the conservation of the Ndoki forests for the next 25 years and beyond.
Acknowledgements
Twenty-five years of primate research in the Ndoki forest, Republic of Congo
Morgan D, Stephan C and Sanz C
Chimpanzees employ context-specific behavioral strategies within fission-fusion societies
Funkhouser JA, Musgrave S, Morgan D, Kialiema SN, Ngoteni D, Brogan S, McElmurray P and Sanz C
Fission-fusion social systems allow individuals to make flexible choices about where, with whom, and in what contexts to spend their time in response to competing social and ecological pressures. The ability for fission-fusion societies to support individual behavioral strategies that vary across contexts has been suggested, but the potential function of such context-specific social choices remains largely understudied. We adopted the concept of social niche construction to explore possible differences in social complexity at the individual and group level across feeding contexts. Specifically, we examined patterns of co-attendance across two common ecological contexts in wild Central African chimpanzees (Pan troglodytes troglodytes) in the Goualougo Triangle, Republic of Congo. From data compiled over 6 years, we used multidimensional social network analysis to study the patterns of co-attendance generated from 436 group scans at Ficus and 4527 visits to termite mounds. These two contexts were chosen, because they are both fixed spatial features across the landscape that serve as well-defined points to compare association patterns. We identified context-specific social niche construction in a fission-fusion chimpanzee society that produce different patterns of relationships and social complexity that are consistent in their expression over many years, and offer functional benefits. While enhancing our understanding of chimpanzee behavioral strategies, culture, and conservation, our investigation also indicates that the social niche construction framework aids in elucidating the evolutionary advantages of fission-fusion sociality by accounting for intra- and interindividual variability, cognition, and choice in newfound ways.
Great ape surveys and the implications of long-term monitoring in the Djéké Triangle, Republic of Congo
Mayoukou W, Morgan D, Strindberg S, McElmurray P, Abedine C and Sanz C
Existing protected areas are anchors for conservation. Safeguarding flora and fauna within their peripheral areas is essential to maintaining their integrity and to potential increases to the area under effective conservation. With the decline in tropical forests, initiatives to increase the area of undisturbed forests under strict protection, particularly those neighboring protected areas, is of critical importance. Applied research has informed such land-management decisions for areas surrounding the Nouabalé-Ndoki National Park (NNNP) in Republic of Congo since the park's inception three decades ago. Here, we present results of the first systematic line transect survey of great ape nests conducted in the Djéké Triangle, a 100 km unlogged continuous forest in the Kabo Forestry Management Unit adjacent to the NNNP. Distance sampling methods applied along 26 line transects on two different occasions (2016 and 2018, with total effort of 69.4 km) provided density estimates of 0.75 (95% confidence interval (CI) 0.52-1.09) and 0.61 (95% CI 0.40-0.92) chimpanzees/km and 2.15 (95% CI 1.36-3.40) and 1.19 (95% CI 0.78-1.82) gorillas/km for each of the two surveys, respectively. Estimated ape densities were compared to others across the landscape. The findings provide a unique baseline in an area that supports ongoing behavioral research and future gorilla tourism opportunities in the Djéké Triangle. More importantly, results provided empirical evidence of the environmental value and strategic conservation importance supporting inclusion of the Djéké Triangle into the NNNP in 2023. These long-term monitoring results inform best-practice standards and ape tourism certification.