Timothy M. Eppley

Ape duos and trios: spontaneous cooperation with free partner choice in chimpanzees

The purpose of the present study was to push the boundaries of cooperation among captive chimpanzees (Pan troglodytes). There has been doubt about the level of cooperation that chimpanzees are able to spontaneously achieve or understand. Would they, without any pre-training or restrictions in partner choice, be able to develop successful joint action? And would they be able to extend cooperation to more than two partners, as they do in nature? Chimpanzees were given a chance to cooperate with multiple partners of their own choosing. All members of the group (N = 11) had simultaneous access to an apparatus that required two (dyadic condition) or three (triadic condition) individuals to pull in a tray baited with food. Without any training, the chimpanzees spontaneously solved the task a total of 3,565 times in both dyadic and triadic combinations. Their success rate and efficiency increased over time, whereas the amount of pulling in the absence of a partner decreased, demonstrating that they had learned the task contingencies. They preferentially approached the apparatus when kin or nonkin of similar rank were present, showing a preference for socially tolerant partners. The forced partner combinations typical of cooperation experiments cannot reveal these abilities, which demonstrate that in the midst of a complex social environment, chimpanzees spontaneously initiate and maintain a high level of cooperative behavior.

Coping with low-quality diets: a first account of the feeding ecology of the southern gentle lemur, Hapalemur meridionalis, in the Mandena littoral forest, southeast Madagascar

Malagasy primates of the genus Hapalemur are exceptional in their exhibition of specialisations allowing for a folivorous diet despite their small body size. Members of this group are well known for their preference for specific parts of woody bamboo, the primary food resource throughout much of their range. The southern gentle lemur (H.meridionalis), however, inhabits littoral forests that contain little or no woody bamboo. Similar to its closely related congener, the Alaotran gentle lemur (H. alaotrensis), the question is raised as to how these lemurs subsist in this ecological context. The aim of this study was to gain an initial understanding of the ecological niche of the southern gentle lemur in the threatened ecosystem of the littoral forest of southeastern Madagascar. Lemurs were habituated and observed over a 3-month period during the austral winter, allowing for collection of both continuous and instantaneous focal data on their feeding ecology. Preferred food species were identified and collected, and biochemical analyses determined macronutrient and secondary compound values for consumed food items. The diet of the southern gentle lemur was found to be of low nutritional quality, as evaluated through the low protein-to-fibre ratio, especially when compared with other folivores. This lemur is also unique in spending a majority of its time grazing on terrestrial grasses (family Poaceae) during the resource-poor winter months. Our data indicate that Hapalemur spp. possess a behavioural flexibility, and possibly, digestive abilities, higher than previously thought for an animal of its small body size.

How chimpanzees cooperate in a competitive world

Significance Competitive tendencies may make it hard for members of a group to cooperate with each other. Humans use many different “enforcement” strategies to keep competition in check and favor cooperation. To test whether one of our closest relatives uses similar strategies, we gave a group of chimpanzees a cooperative problem that required joint action by two or three individuals. The open-group set-up allowed the chimpanzees a choice between cooperation and competitive behavior like freeloading. The chimpanzees used a combination of partner choice and punishment of competitive individuals to reduce competition. In the end, cooperation won. Our results suggest that the roots of human cooperation are shared with other primates. Our species is routinely depicted as unique in its ability to achieve cooperation, whereas our closest relative, the chimpanzee (Pan troglodytes), is often characterized as overly competitive. Human cooperation is assisted by the cost attached to competitive tendencies through enforcement mechanisms, such as punishment and partner choice. To examine if chimpanzees possess the same ability to mitigate competition, we set up a cooperative task in the presence of the entire group of 11 adults, which required two or three individuals to pull jointly to receive rewards. This open-group set-up provided ample opportunity for competition (e.g., freeloading, displacements) and aggression. Despite this unique set-up and initial competitiveness, cooperation prevailed in the end, being at least five times as common as competition. The chimpanzees performed 3,565 cooperative acts while using a variety of enforcement mechanisms to overcome competition and freeloading, as measured by (attempted) thefts of rewards. These mechanisms included direct protest by the target, third-party punishment in which dominant individuals intervened against freeloaders, and partner choice. There was a marked difference between freeloading and displacement; freeloading tended to elicit withdrawal and third-party interventions, whereas displacements were met with a higher rate of direct retaliation. Humans have shown similar responses in controlled experiments, suggesting shared mechanisms across the primates to mitigate competition for the sake of cooperation.

The Use of an Invasive Species Habitat by a Small Folivorous Primate: Implications for Lemur Conservation in Madagascar.

The lemurs of Madagascar are among the most threatened mammalian taxa in the world, with habitat loss due to shifting cultivation and timber harvest heavily contributing to their precarious state. Deforestation often leads to fragmentation, resulting in mixed-habitat matrices throughout a landscape where disturbed areas are prone to invasion by exotic plants. Our study site, the Mandena littoral forest (southeast Madagascar), is a matrix of littoral forest, littoral swamp, and Melaleuca swamp habitats. Here, Melaleuca quinquenervia has invaded the wetland ecosystem, creating a mono-dominant habitat that currently provides the only potential habitat corridor between forest fragments. We sought to understand the role of this invasive Melaleuca swamp on the behavioral ecology of a threatened, small-bodied folivore, the southern bamboo lemur (Hapalemur meridionalis). We collected botanical and behavioral data on four groups of H. meridionalis between January and December 2013. Our results confirm Melaleuca swamp as an important part of their home range: while lemurs seasonally limited activities to certain habitats, all groups were capable of utilizing this invasive habitat for feeding and resting. Furthermore, the fact that Hapalemur use an invasive plant species as a dispersal corridor increases our knowledge of their ecological flexibility, and may be useful in the conservation management of remaining threatened populations.

Perseverance and food sharing among closely affiliated female chimpanzees

Chimpanzees (Pantroglodytes) have been frequently observed to share food with one another, with numerous hypotheses proposed to explain why. These often focus on reciprocity exchanges for social benefits (e.g., food for grooming, food for sex, affiliation, kinship, and dominance rank) as well as sharing based on begging and deterring harassment. Although previous studies have shown that each of these hypotheses has a viable basis, they have only examined situations in which males have preferential access to food whereby females are required to obtain the food from males. For example, studies on male chimpanzee food sharing take advantage of successful crop-raids and/or acquisitions of meat from hunting, situations that only leave females access to food controlled by male food possessors. This begs the question how and with whom might a female chimpanzee in sole possession of a high-quality food item choose to share? In two large captive groups of chimpanzees, we examined each of the hypotheses with female food possessors of a high-quality food item and compared these data to a previous study examining food transfers from male chimpanzees. Our results show that alpha females shared significantly more with closely affiliated females displaying perseverance, while kinship and dominance rank had no effect. This positive interaction between long-term affiliation and perseverance shows that individuals with whom the female possessor was significantly affiliated received more food while persevering more than those with neutral or avoidant relationships towards her. Furthermore, females with avoidant relationships persevered far less than others, suggesting that this strategy is not equally available to all individuals. In comparison to the mixed-sex trials, females chose to co-feed with other females more than was observed when the alpha male was sharing food. This research indicates that male and female chimpanzees (as possessors of a desired food item) share food in ways influenced by different factors and strategies.

The roles of food quality and sex in chimpanzee sharing behavior (Pan troglodytes)

Both wild and captive chimpanzees (Pan troglodytes) share food with non-relatives. Researchers have proposed several hypotheses to explain this behavior, including ‘food for sex’, ‘food for grooming or agonistic support’, and ‘sharing under pressure’. We examined food sharing in two captive groups of socially-housed chimpanzees. In contrast to previous captive studies, which only examined transfers of low-quality foods, we conducted seven trials with high-quality food and seven with low-quality food for each group to directly compare transfers of different food qualities. We recorded how male chimpanzees shared food, including active transfers, passive transfers, and co-feeding. We also noted all instances of copulations, female estrous states, benign attempts to access food (termed ‘perseverance’), and aggressive attempts (termed ‘harassment’) to examine whether any of these factors influenced food sharing. Male food possessors shared at the same rate in both food quality conditions, but seemingly for different reasons, indicating that food quality may affect the exchange of social benefits in chimpanzees. In the low-quality condition, there was an interaction with rank and perseverance: while low- and middle-ranking females received more food the more they persevered, high-ranking females received more food without perseverance and gained relatively little benefit from persevering. In the high-quality condition, there was an interaction between copulations and perseverance: females who copulated with the male food possessor received more food during that trial with less perseverance. Non-copulating females received more transfers the more they persevered. This result was only observed in the shortterm — copulations over the previous year were not correlated with food transfers. Further, the copulations observed here were unusual for these chimpanzees in that they were not confined to peak fertility, suggesting a non-conceptive function for copulations in chimpanzees. Copulations in this study may have functioned to reduce tension and increase short-term tolerance, allowing females better access to food.

An unusual case of affiliative association of a female Lemur cattain a Hapalemur meridionalissocial group

Polyspecific associations are well documented, but have rarely been observed in strepsirrhines. In this study we present a unique affiliative association between a female ring-tailed lemur ( Lemur catta) and a group of southern bamboo lemurs ( Hapalemur meridionalis) in south-east Madagascar. Our main research focused on H. meridionalis; however, due to the presence of the L. cattawe treated her as a group member, including her in the focal sampling of Hapalemursocial behaviour. We also recorded ad libitum data on all food species/items and any unique events or occurrences. Among observations, both species appeared to have a mutual understanding of vocalisations, behavioural synchronisation, dietary overlap, and possible service exchange, e.g., grooming. We also observed the L. cattaoccasionally attending to the bamboo lemur infant. This included grooming, baby-sitting, and even transporting the infant. The behavioural flexibility exhibited by both species has allowed the successful integration of the female ring-tailed lemur.

Chimpanzees Prefer African and Indian Music Over Silence

[Correction Notice: An Erratum for this article was reported in Vol 40(4) of Journal of Experimental Psychology: Animal Learning and Cognition (see record 2014-35305-001). For the article, the below files were used to create the audio used in this study. The original West African akan and North Indian raga pieces were used in their entirety and the Japanese taiko piece was used from the 0:19 second mark through the end. The tempo of each piece was adjusted so that they maintained an identical base tempo of 90 beats per minute, then looped to create 40 minutes of continuous music. Additionally, the volume of the music was standardized at 50 dB so that the all music maintained the same average amplitude. All audio manipulations were completed using GarageBand

Determinants of terrestrial feeding in an arboreal primate: The case of the southern bamboo lemur (Hapalemur meridionalis).

OBJECTIVES The proximate and ultimate determinants that may have prompted some primates to shift from an arboreal to terrestrial feeding niche, whether due to environmental change, seasonality, and/or predation pressure, are poorly understood. Within a fragmented littoral forest in southeast Madagascar, an arboreal strepsirrhine population spends a large proportion of time on the ground, thus we aimed to identify which factors influence terrestrial feeding. METHODS From January to December 2013, we conducted 103 full-day focal follows on three social groups of southern bamboo lemurs H. meridionalis. We continuously recorded feeding time on all arboreal and terrestrial items, as well as whether the focal individual was under the canopy or exposed, and the distance to their nearest conspecific neighbor. All observed food items were collected and analyzed for macronutrient content. Daily climatic variables (temperature, precipitation), resource seasonality, daily path length (DPL), along with dietary and predation risk proxies, were used as fixed effects in a linear mixed model, with the daily proportion of terrestrial feeding as the dependent variable. RESULTS Our model indicated that daily terrestrial feeding increased at cooler temperature, was associated with reduced DPL, and the intake of dietary metabolizable energy increased as terrestrial feeding increased. All other fixed effects were not significant predictors. DISCUSSION Our study provides a window into the ultimate determinants of niche expansion: ancestral primates, in absence of their primary resources, may have initially descended to the ground in peripheral population range areas where the benefits (e g., nutritional pay-off) out-weighed the costs.

Chimpanzee uses manipulative gaze cues to conceal and reveal information to foraging competitor

Tactical deception has been widely reported in primates on a functional basis, but details of behavioral mechanisms are usually unspecified. We tested a pair of chimpanzees (Pan troglodytes) in the informed forager paradigm, in which the subordinate saw the location of hidden food and the dominant did not. We employed cross‐correlations to examine temporal contingencies between chimpanzees’ behavior: specifically how the direction of the subordinates gaze and movement functioned to manipulate the dominants searching behavior through two tactics, withholding, and misleading information. In Experiment 1, not only did the informed subordinate tend to stop walking toward a single high value food, but she also refrained from gazing toward it, thus, withholding potentially revealing cues from her searching competitor. In a second experiment, in which a moderate value food was hidden in addition to the high value food, whenever the subordinate alternated her gaze between the dominant and the moderate value food, she often paused walking for 5 s; this frequently recruited the dominant to the inferior food, functioning as a “decoy.” The subordinate flexibly concealed and revealed gaze toward a goal, which suggests that not only can chimpanzees use visual cues to make predictions about behavior, but also that chimpanzees may understand that other individuals can exploit their gaze direction. These results substantiate descriptive reports of how chimpanzees use gaze to manipulate others, and to our knowledge are the first quantitative data to identify behavioral mechanisms of tactical deception.