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.

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.

The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates.

Life history, brain size and energy expenditure scale with body mass in mammals but there is little conclusive evidence for a correlated evolution between life history and energy expenditure (either basal/resting or daily) independent of body mass. We addressed this question by examining the relationship between primate free-living daily energy expenditure (DEE) measured by doubly labeled water method (n = 18 species), life history variables (maximum lifespan, gestation and lactation duration, interbirth interval, litter mass, age at first reproduction), resting metabolic rate (RMR) and brain size. We also analyzed whether the hypometabolic primates of Madagascar (lemurs) make distinct energy allocation tradeoffs compared to other primates (monkeys and apes) with different life history traits and ecological constraints. None of the life-history traits correlated with DEE after controlling for body mass and phylogeny. In contrast, a regression model showed that DEE increased with increasing RMR and decreasing reproductive output (i.e., litter mass/interbirth interval) independent of body mass. Despite their low RMR and smaller brains, lemurs had an average DEE remarkably similar to that of haplorhines. The data suggest that lemurs have evolved energy strategies that maximize energy investment to survive in the unusually harsh and unpredictable environments of Madagascar at the expense of reproduction.

Energy (Im-)Balance in Frugivorous Lemurs in Southern Madagascar: A Preliminary Study in Lemur catta and Eulemur rufifrons × collaris.

The reproductive cycle of several lemur species is synchronized by photoperiodic changes and it is attuned to the seasonal fluctuations in food supply. Nevertheless, irregular periods of food shortage occur in Madagascar, which can result in a negative energy balance and reduced fitness, especially in frugivorous species. Here, we tested whether ring-tailed lemurs (Lemur catta) and brown lemurs (Eulemur rufifrons × collaris) use fat stores to maintain their energy balance in a gallery forest of Madagascar (Berenty Reserve). We assessed the energy intake from weight-based estimates of food intake (mouthful count) and macronutrient contents in the diet during dry and wet months. The metabolizable energy ingested by these frugivorous/folivorous species was high during the late wet season, but it was insufficient to meet their energy requirements during the dry season. These preliminary data suggest that these lemurs must store sufficient amount of fat mass during the period of food abundance to meet their maintenance requirements and to cope with the energetic burden of the mating season. Estimates based on models assuming no fiber digestibility during the dry season are consistent with the prediction that brown lemurs should supplement their daytime diet with nighttime feeding in addition to the use of body fat stores.

Primate energy input and the evolutionary transition to energy-dense diets in humans.

Humans and other large-brained hominins have been proposed to increase energy turnover during their evolutionary history. Such increased energy turnover is plausible, given the evolution of energy-rich diets, but requires empirical confirmation. Framing human energetics in a phylogenetic context, our meta-analysis of 17 wild non-human primate species shows that daily metabolizable energy input follows an allometric relationship with body mass where the allometric exponent for mass is 0.75 ± 0.04, close to that reported for daily energy expenditure measured with doubly labelled water in primates. Human populations at subsistence level (n = 6) largely fall within the variation of primate species in the scaling of energy intake and therefore do not consume significantly more energy than predicted for a non-human primate of equivalent mass. By contrast, humans ingest a conspicuously lower mass of food (-64 ± 6%) compared with primates and maintain their energy intake relatively more constantly across the year. We conclude that our hominin hunter-gatherer ancestors did not increase their energy turnover beyond the allometric relationship characterizing all primate species. The reduction in digestive costs due to consumption of a lower mass of high-quality food, as well as stabilization of energy supply, may have been important evolutionary steps enabling encephalization in the absence of significantly raised energy intakes.

The importance of protein in leaf selection of folivorous primates.

Protein limitation has been considered a key factor in hypotheses on the evolution of life history and animal communities, suggesting that animals should prioritize protein in their food choice. This contrasts with the limited support that food selection studies have provided for such a priority in nonhuman primates, particularly for folivores. Here, we suggest that this discrepancy can be resolved if folivores only need to select for high protein leaves when average protein concentration in the habitat is low. To test the prediction, we applied meta-analyses to analyze published and unpublished results of food selection for protein and fiber concentrations from 24 studies (some with multiple species) of folivorous primates. To counter potential methodological flaws, we differentiated between methods analyzing total nitrogen and soluble protein concentrations. We used a meta-analysis to test for the effect of protein on food selection by primates and found a significant effect of soluble protein concentrations, but a non-significant effect for total nitrogen. Furthermore, selection for soluble protein was reinforced in forests where protein was less available. Selection for low fiber content was significant but unrelated to the fiber concentrations in representative leaf samples of a given forest. There was no relationship (either negative or positive) between the concentration of protein and fiber in the food or in representative samples of leaves. Overall our study suggests that protein selection is influenced by the protein availability in the environment, explaining the sometimes contradictory results in previous studies on protein selection. Am. J. Primatol. 79:e22550, 2017. © 2016 Wiley Periodicals, Inc.

Intestinal Helminths of Wild Bonobos in Forest-Savanna Mosaic: Risk Assessment of Cross-Species Transmission with Local People in the Democratic Republic of the Congo.

Phylogenetic and geographic proximities between humans and apes pose a risk of zoonotic transmission of pathogens. Bonobos (Pan paniscus) of the Bolobo Territory, Democratic Republic of the Congo, live in a fragmented forest-savanna mosaic setting, a marginal habitat for this species used to living in dense forests. Human activities in the forest have increased the risk of contacts between humans and bonobos. Over 21 months (September 2010-October 2013), we monitored intestinal parasites in bonobo (n = 273) and in human (n = 79) fecal samples to acquire data on bonobo parasitology and to assess the risk of intestinal helminth transmission between these hosts. Coproscopy, DNA amplification, and sequencing of stored dried feces and larvae were performed to identify helminths. Little difference was observed in intestinal parasites of bonobos in this dryer habitat compared to those living in dense forests. Although Strongylids, Enterobius sp., and Capillaria sp. were found in both humans and bonobos, the species were different between the hosts according to egg size or molecular data. Thus, no evidence of helminth transmission between humans and bonobos was found. However, because humans and this threatened species share the same habitat, it is essential to continue to monitor this risk.

Energy management in crowned sifakas (Propithecus coronatus) and the timing of reproduction in a seasonal environment.

OBJECTIVES: Little is known about the absolute pool of energy primates use in the wild and how this pool varies seasonally. It is also not fully understood why some species facing unpredictable changes in food supply and risks of energy imbalance show high breeding seasonality. We examined these issues in a folivorous gregarious lemur (Propithecus coronatus) in a dry forest of Madagascar. METHODS: We assessed energy input and activity budget in males and females from three groups during dry and wet months. Diet composition and daily food intake were determined using focal animal sampling and continuous recording of mouthfuls. Locomotion types and daily distances traveled were recorded. Time budget was determined using scan sampling, supplemented with a preliminary analysis of the energy budget using the factorial method. RESULTS: The macronutrient composition of the diet did not change markedly between seasons but a large increase in energy input arose during the early wet season. Activity was highest at this period but entailed only moderate increase in energy expenditure. Females did not ingest more energy than males despite female dominance. Both sexes exhibited a thrifty energy strategy and, possibly, fat storage. CONCLUSIONS: Seasonal increase of daily energy input was likely related to male-male mating competition and females' need to reach physical condition prior to the dry season sufficient for reproducing. Sifakas may time their reproductive cycle according to the seasonal variation in day-length because recurrent patterns of low (dry season) versus high (wet season) food production occur despite years of food shortage. Am J Phys Anthropol, 2015. © 2015 Wiley Periodicals, Inc. Am J Phys Anthropol 158:269-278, 2015. © 2015 Wiley Periodicals, Inc.

Bonobo habituation in a forest-savanna mosaic habitat: influence of ape species, habitat type, and sociocultural context.

Habituation is the term used to describe acceptance by wild animals of a human observer as a neutral element in their environment. Among primates, the process takes from a few days for Galago spp. to several years for African apes. There are also intraspecies differences reflecting differences in habitat, home range, and ape-human relationship history. Here, we present the first study of the process of bonobo habituation in a fragmented habitat, a forest-savanna mosaic in the community-based conservation area led by the Congolese nongovernmental organization Mbou-Mon-Tour, Democratic Republic of the Congo. In this area, local people use the forest almost every day for traditional activities but avoid bonobos because of a traditional taboo. Because very few flight reactions were observed during habituation, we focused on quantitative parameters to assess the development of ape tolerance and of the tracking efficiency of observer teams. During the 18-month study period (May 2012-October 2013), 4043 h (319 days) were spent in the forest and bonobos were observed for a total of 405 h (196 contacts on 134 days). The average contact duration was stable over time (124 min), but the minimal distance during a contact decreased with habituation effort. Moreover, bonobo location and tracking efficiency, daily ratio of contact time to habituation effort, and the number of observations at ground level were positively correlated with habituation effort. Our observations suggest that bonobos become habituated relatively rapidly. These results are discussed in relation to the habitat type, ape species, and the local sociocultural context of villagers. The habituation process involves changes in ape behavior toward observers and also more complex interactions concerning the ecosystem, including the building of an efficient local team. Before starting a habituation process, knowledge of the human sociocultural context is essential to assess the balance between risks and benefits.

Scaling of free-ranging primate energetics with body mass predicts low energy expenditure in humans.

Studies of how a mammal's daily energy expenditure scales with its body mass suggest that humans, whether Westerners, agro-pastoralists, or hunter-gatherers, all have much lower energy expenditures for their body mass than other mammals. However, non-human primates also differ from other mammals in several life history traits suggestive of low energy use. Judging by field metabolic rates of free-ranging strepsirhine and haplorhine primates with different lifestyle and body mass, estimated using doubly labeled water, primates have lower energy expenditure than other similar-sized eutherian mammals. Daily energy expenditure in humans fell along the regression line of non-human primates. The results suggest that thrifty energy use could be an ancient strategy of primates. Although physical activity is a major component of energy balance, our results suggest a need to revise the basis for establishing norms of energy expenditure in modern humans.

Leaf chemistry as a predictor of primate biomass and the mediating role of food selection: a case study in a folivorous lemur (Propithecus verreauxi).

Folivorous primate biomass has been shown to positively correlate with the average protein-to-fiber ratio in mature leaves of tropical forests. However, studies have failed to explain the mismatch between dietary selection and the role of the protein-to-fiber ratio on primate biomass; why do not folivores always favor mature leaves or leaves with the highest protein-to-fiber ratio? We examined the effect of leaf chemical characteristics and plant abundance (using transect censuses; 0.37 ha, 233 trees) on food choices and nutrient/toxin consumption in a folivorous lemur (Propithecus verreauxi) in a gallery forest in southern Madagascar. To assess the nutritional quality of the habitat, we calculated an abundance-weighted chemical index for each chemical variable. Food intake was quantified using a continuous count of mouthfuls during individual full-day follows across three seasons. We found a significant positive correlation between food ranking in the diet and plant abundance. The protein-to-fiber ratio and most other chemical variables tested had no statistical effect on dietary selection. Numerous chemical characteristics of the sifaka's diet were essentially by-products of generalist feeding and "low energy input/low energy crop" strategy. The examination of feeding behavior and plant chemistry in Old World colobines and folivorous prosimians in Madagascar suggests that relative lack of feeding selectivity and high primate biomass occur when the average protein-to-fiber ratio of mature leaves in the habitat exceeds a threshold at 0.4.

Total energy expenditure and body composition in two free-living sympatric lemurs.

BACKGROUND: Evolutionary theories that account for the unusual socio-ecological traits and life history features of group-living prosimians, compared with other primates, predict behavioral and physiological mechanisms to conserve energy. Low energy output and possible fattening mechanisms are expected, as either an adaptive response to drastic seasonal fluctuations of food supplies in Madagascar, or persisting traits from previously nocturnal hypometabolic ancestors. Free ranging ring-tailed lemurs (Lemur catta) and brown lemurs (Eulemur sp.) of southern Madagascar have different socio-ecological characteristics which allow a test of these theories: Both gregarious primates have a phytophagous diet but different circadian activity rhythms, degree of arboreality, social systems, and slightly different body size. METHODOLOGY AND RESULTS: Daily total energy expenditure and body composition were measured in the field with the doubly labeled water procedure. High body fat content was observed at the end of the rainy season, which supports the notion that individuals need to attain a sufficient physical condition prior to the long dry season. However, ring-tailed lemurs exhibited lower water flux rates and energy expenditure than brown lemurs after controlling for body mass differences. The difference was interpreted to reflect higher efficiency for coping with seasonally low quality foods and water scarcity. Daily energy expenditure of both species was much less than the field metabolic rates predicted by various scaling relationships found across mammals. DISCUSSION: We argue that low energy output in these species is mainly accounted for by low basal metabolic rate and reflects adaptation to harsh, unpredictable environments. The absence of observed sex differences in body weight, fat content, and daily energy expenditure converge with earlier investigations of physical activity levels in ring-tailed lemurs to suggest the absence of a relationship between energy constraints and the evolution of female dominance over males among lemurs. Nevertheless, additional seasonal data are required to provide a definitive conclusion.

Taste acuity of obese adolescents and changes in food neophobia and food preferences during a weight reduction session.

The relationship between taste acuity and food neophobia, food familiarity and liking has been studied in the context of a residential weight reduction session (WRS; mean duration: 10 months) in 39 obese adolescents. Taste acuity was assessed using recognition thresholds for sucrose, citric acid, sodium chloride and 6-n propylthiouracil (PROP) and supra-threshold perceived intensities for sucrose, sodium chloride and PROP. Food neophobia was assessed by using the food neophobia scale at the beginning and at the end of the WRS. At these time points we used also a food familiarity and liking questionnaire to assess changes in food familiarity and likes or dislikes for different food categories. Taste acuity appeared to mediate behavioural food-related changes during the WRS. High taste acuity was associated with limited reductions in food neophobia; less sensitive subjects showed greater increases in the acceptability of healthy foods, especially fruits and vegetables. Therefore, taste perception (and particularly PROP perception) appears to be a predictor of the magnitude of food-related behavioural change achieved during a WRS.

Taste perception in massively obese and in non-obese adolescents.

OBJECTIVE: The purpose is to determine whether taste functions are different in massively obese adolescents as compared with non-obese adolescents, and to what extent metabolic disorders may interfere with taste perception, as suggested by the results of recent animal studies. RESEARCH METHOD AND PROCEDURES: We compared taste sensitivity and hedonic responses of 39 adolescents with severe early onset obesity (mean BMI: 39.5; min-max: 30.9-51.6) and 48 non-obese adolescents (mean BMI: 21.0; min-max: 16.5-27.9) of both sexes. We measured recognition thresholds for fructose, sucrose, citric acid and sodium chloride. Supra-threshold perceived intensity and hedonic responses were assessed for solutions of sucrose and sodium chloride. In obese subjects, the occurrence of the metabolic syndrome was assessed by measuring blood pressure and, in blood samples, fasting glycemia and insulinemia, the concentration of triglycerides and HDL cholesterol. HOMA modelling was used to assess insulin resistance. RESULTS: Massively obese adolescents present a higher sensitivity to sucrose and sodium chloride than non-obese adolescents, with significantly lower recognition thresholds, and higher perceived intensities at supra-threshold levels for sucrose and salt. Hedonic responses are significantly lower for sodium chloride in the obese subjects. Among obese subjects, a significant positive correlation between taste responsiveness and the number of obesity-related metabolic disturbances is observed only in girls. CONCLUSION: Massively obese subjects have higher taste sensitivity than control subjects, especially for sucrose and salt. This can be explained, to some extent, by the influence of obesity-related metabolic disorders, which appears to be gender-specific.

Food neophobia in the context of a varied diet induced by a weight reduction program in massively obese adolescents.

Previous studies in humans have shown that short to middle-term pre-exposure to multiple foods can reduce the negative response to novel foods (neophobia). In order to explore the effects of a long-term exposure to varied foods on food neophobia, we studied a population of obese adolescents observed in a longitudinal protocol in which the multiple food experiences are induced by a residential weight reduction program (WRP) that encourages the consumption of a wide variety of foods. Seventy-two massively obese adolescents (22 boys) filled the food neophobia scale (FNS, [Pliner, P., & Hobden, K. (1992). Development of a scale to measure the trait of food neophobia in humans. Appetite 19, 105-120]) and an ad hoc food familiarity and liking questionnaire at the beginning and at the end of the program (mean duration: 8.9 months). Their scores were compared to those of a control group of 51 adolescents (14 boys) tested within a similar period. FNS results show a decrease of food neophobia, without significant difference between the control group and the WRP subjects, although only WRP have encountered new foods experiences as attested by the familiarity and liking results. Methodological considerations, concerning the characteristics of the participants, the nature of the multiple food exposure and the food neophobia measurements, will be proposed to explain differences among studies.

Relationship between taste thresholds and hunger under debate.

We determined taste recognition thresholds for six compounds (sucrose, fructose, sodium chloride, quinine sulphate, PROP and liquorice) in fasting students and, in the same subjects, after a meal. The testing procedure was the staircase-method in blind conditions. Although taste sensitivity may vary with hormonal status, our results did not show any significant difference in taste recognition thresholds between hunger and satiety. Our Bayesian analysis did not corroborate the hypothesis of increased sensitivity to nutrition-related tastants in the fasting state that was recently supported by data obtained with the two-alternative forced-choice method.

Demography, range use, and behavior in black lemurs (Eulemur macaco macaco) at Ampasikely, northwest Madagascar.

We studied a black lemur population over a 2-year period (1992-1993) and 8 years later (2000) in a 50-ha secondary forest in northwest Madagascar. All of the animals were marked to investigate population dynamics and seasonal variation in ranging and behavior, and new data on black lemurs were obtained. Our data on demographic characteristics were expanded to include other forest sites and contrasted with those collected in other Eulemur macaco macaco field studies, in relation to human activity and the presence of introduced and cultivated plant species. Density is affected by deforestation and hunting. Group size and home range depend on the composition of the forest and probably food patches. Sex ratio at birth varies according to the number of females per group, a result that fits the local resource competition model. Groups are multimale-multifemale, and adult females form the core of the groups. Reproductive parameters indicate sharply defined seasonal breeding, a high female reproductive rate, and birth synchrony. Changes in group composition reveal male and female juvenile dispersal, male transfer between groups at the time of mating, and adult female transfer and group fission when groups exceed a critical size. At mating and birth, intergroup agonistic encounters occurred at home-range boundaries, and larger groups were dominant over smaller groups. Patterns of intragroup interactions suggest that males compete for access to groups of females during the mating season, and that females may compete for food resources during the birth season. Our study also reports female social dominance and lack of sexual weight dimorphism in this species.

A comparison of taste thresholds for sweet and astringent-tasting compounds in great apes.

Taste responses to fructose and tannic acid were compared between great apes using the 'two-bottle test' with tests of brief duration. The taste thresholds for fructose were [10-20] mM in Pongo pygmaeus, [40-50] mM in Pan troglodytes, and [70-80] mM in Gorilla gorilla. Inhibition thresholds for tannic acid were [2.9-3.5] mM in Pongo and [2.9-5.9] mM in Pan. Gorillas apparently significantly preferred tannins at low concentrations ([0.59-5.9] mM) but rejected concentrations above [8.8-14.7] mM. These results are discussed in relation to the effects of phylogenetic inertia and biological adaptation.