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Although considered a hallmark in early ontogeny, weaning from breastmilk is difficult to monitor in wild primates and weaning ages remain unknown for wild bonobos (Pan Paniscus). Here, we calculated inter-birth intervals from demographic data and measured the isotopic offsets (Δ15N and Δ13C) between mother (n = 17) and offspring (n = 28) fecal sample pairs (n = 131, total n = 246) in the LuiKotale bonobos to assess nutritional weaning for the first time. We tested the effects of infant age, female parity, and sibling competition on Δ15N and Δ13C values. We found bonobo inter-birth intervals ranging from 2.2 to 7.3 years (xÌ = 4.7 ± 1.3 years) at LuiKotale. The Δ15N and Δ13C values suggested nutritional weaning on average by 6.6 and 7.0 years of age respectively, considerably exceeding weaning ages reported for chimpanzees (P. troglodytes) using the same approach. Our Δ13C data suggested that the number of offspring present affected nursing, with first-time mothers nursing more and possibly longer. The Δ15N and Δ13C values decreased with the arrival of the next sibling, suggesting sibling competition reduces milk access. Nevertheless, offspring may continue nursing 2.5-3 years after the birth of the next sibling, corresponding well with observations on low infant mortality. In conclusion, bonobo mothers provide remarkably enduring materna l support in the form of nursing concurrently to several offspring.
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Tool use diversity is often considered to differentiate our two closest living relatives: the chimpanzee (Pan troglodytes) and the bonobo (P. paniscus). Chimpanzees appear to have the largest repertoire of tools amongst nonhuman primates, and in this species, many forms of tool use enhance food and water acquisition. In captivity, bonobos seem as adept as chimpanzees in tool use complexity, including in the foraging context. However, in the wild, bonobos have only been observed engaging in habitual tool use in the contexts of comfort, play, self-directed behaviour and communication, whilst no tool-assisted food acquisition has been reported. Whereas captive bonobos use tools for drinking, so far, the only report from the wild populations comes down to four observations of moss sponges used at Lomako. Here, we present the first report of tool use in the form of water scooping by a wild bonobo at LuiKotale. An adult female was observed and videotaped whilst using an emptied Cola chlamydantha pod to scoop and drink water from a stream. We discuss the conditions for such observations and the importance of looking out for rare behaviours and attempt to put the observation into the context of the opportunity versus necessity hypotheses. By adding novel information on tool use, our report contributes to the ongoing efforts to differentiate population-specific traits in the behavioural ecology of the bonobo.
Assuntos
Hominidae , Comportamento de Utilização de Ferramentas , Animais , Feminino , Pan paniscus , Pan troglodytes , AlimentosRESUMO
Adolescent growth spurts (GSs) in body length seem to be absent in non-human primates and are considered a distinct human trait. However, this distinction between present and absent length-GSs may reflect a mathematical artefact that makes it arbitrary. We first outline how scaling issues and inappropriate comparisons between length (linear) and weight (volume) growth rates result in misleading interpretations like the absence of length-GSs in non-human primates despite pronounced weight-GSs, or temporal delays between length- and weight-GSs. We then apply a scale-corrected approach to a comprehensive dataset on 258 zoo-housed bonobos that includes weight and length growth as well as several physiological markers related to growth and adolescence. We found pronounced GSs in body weight and length in both sexes. Weight and length growth trajectories corresponded with each other and with patterns of testosterone and insulin-like growth factor-binding protein 3 levels, resembling adolescent GSs in humans. We further re-interpreted published data of non-human primates, which showed that aligned GSs in weight and length exist not only in bonobos. Altogether, our results emphasize the importance of considering scaling laws when interpreting growth curves in general, and further show that pronounced, human-like adolescent length-GSs exist in bonobos and probably also many other non-human primates.
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Pan paniscus , Primatas , Feminino , Masculino , Animais , Artefatos , Fenótipo , TestosteronaRESUMO
In mammals, the costs of reproduction are biased towards females. Lactation is particularly energetically expensive, and behavioral and physiological data indicate that maternal effort during lactation induces energetic stress. Another source of stress in females is male aggression directed towards them when they are cycling. Evaluating the costs of reproduction in wild and mobile animals can be a challenging task, and requires detailed information on state-dependent parameters such as hormone levels. Glucocorticoid (GC) levels are indicative of nutritional and social stress, and are widely used to assess the costs of reproduction. We investigated variation in urinary levels of cortisol, the main GC in female bonobos (Pan paniscus), between and within reproductive stages. Female chimpanzees (Pan troglodytes), the closest living relative of the bonobos, are often exposed to intense aggression from males, which causes a significant rise in their cortisol levels during the phase of their maximum fecundity. In bonobos, males compete for access to fertile females, but aggressive male mating strategies are absent in this species. Therefore, we expected that GC levels of cycling female bonobos would be lower than those of lactating females. Due to the long period of offspring care in bonobos, we expected that GC levels would remain elevated into the late stage of lactation, when immatures gain body weight but may still be nursed and carried by their mothers. We found elevated urinary GC levels only during the early stage of lactation. The GC levels of cycling females did not differ from those in the mid or late lactation stage. Behavioral strategies of female bonobos may allow them to compensate for the elevated energetic demands of lactation and prolonged maternal care.
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Lactação , Pan paniscus , Feminino , Masculino , Animais , Pan paniscus/fisiologia , Hidrocortisona , Agressão/fisiologia , Reprodução/fisiologia , Pan troglodytes/fisiologia , Glucocorticoides , MamíferosRESUMO
Habitat destruction and over-hunting are increasingly threatening the arboreal primates of Central Africa. To establish effective conservation strategies, accurate assessments of primate density, abundance, and spatial distribution are required. To date, the method of choice for primate density estimation is line transect distance sampling. However, primates fleeing human observers violate methodological assumptions, biasing the accuracy of resulting estimates. In this study, we used line transect distance sampling to study five primate species along 378 km of transects in Salonga National Park, Democratic Republic of the Congo. We tested the effect of different levels of survey-inherent disturbance (i.e., cutting) on the number of observed (i) primate groups, and (ii) individuals within groups, by counting groups at three different time lags after disturbance of the transect, (i) a minimum of 3 h, (ii) 24 h, (iii) a minimum of 3 days. We found that survey-inherent disturbance led to underestimated densities, affecting both the number of encountered groups and of observed individuals. However, the response varied between species due to species-specific ecological and behavioral features. Piliocolobus tholloni and Colobus angolenis resumed an unaltered behavior only 24 h after disturbance, while Lophocebus aterrimus, Cercopithecus ascanius, and Cercopithecus wolfi required a minimum of 10 days. To minimize bias in density estimates, future surveys using line transect distance sampling should be designed considering survey-inherent disturbance. We recommend evaluating the factors driving primate response, including habitat type, niche occupation, and hunting pressure, peculiar to the survey-specific area and primate community under study.
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Colobinae , Ecologia , Ecossistema , Animais , Colobus , Densidade Demográfica , Árvores , Ecologia/métodosRESUMO
Feces are a treasure trove in the study of animal behavior and ecology. Stable carbon and nitrogen isotope analysis allows to assess the dietary niches of elusive primate species and primate breastfeeding behavior. However, some fecal isotope data may unwillingly be biased toward the isotope ratios of undigested plant matter, requiring more consistent sample preparation protocols. We assess the impact of this potential data skew in 114 fecal samples of wild bonobos (Pan paniscus) by measuring the isotope differences (Δ13 C, Δ15 N) between bulk fecal samples containing larger particles (>1 mm) and filtered samples containing only small particles (<1 mm). We assess the influence of fecal carbon and nitrogen content (ΔC:N) and sample donor age (subadult, adult) on the resulting Δ13 C, Δ15 N values (n = 228). Additionally, we measure the isotope ratios in three systematically sieved fecal samples of chimpanzees (Pan troglodytes verus), with particle sizes ranging from 20 µm to 8 mm (n = 30). We found differences in fecal carbon and nitrogen content, with the smaller fecal fraction containing more nitrogen on average. While the Δ13 C values were small and not affected by age or ΔC:N, the Δ15 N values were significantly influenced by fecal ΔC:N, possibly resulting from the differing proportions of undigested plant macroparticles. Significant relationships between carbon stable isotope ratios (δ13 C) values and %C in large fecal fractions of both age groups corroborated this assessment. Δ15 N values were significantly larger in adults than subadults, which should be of concern in isotope studies comparing adult females with infants to assess breastfeeding. We found a random variation of up to 3.0 in δ13 C and 2.0 in nitrogen stable isotope ratios within the chimpanzee fecal samples separated by particle sizes. We show that particle size influences isotope ratios and propose a simple, cost-effective filtration method for primate feces to exclude larger undigested food particles from the analysis, which can easily be adopted by labs worldwide.
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Hominidae , Nitrogênio , Feminino , Animais , Isótopos de Nitrogênio/análise , Isótopos de Carbono/análise , Carbono , Pan troglodytes , Pan paniscus , Fezes/química , ViésRESUMO
Herbivorous animals that regularly consume tannin-rich food are known to secrete certain tannin-binding salivary proteins (TBSPs), especially proline-rich proteins and histidine-rich proteins, as an effective measure to counteract the antinutritive effects of dietary tannins. Due to their high binding capacity, TBSPs complex with tannins in the oral cavity, and thereby protect dietary proteins and digestive enzymes. Although the natural diet of great apes (Hominidae) is biased toward ripe fruits, analyses of food plants revealed that their natural diet contains considerable amounts of tannins, which is raising the question of possible counter-measures to cope with dietary tannins. In our study, we investigated the salivary amino acid profiles of zoo-housed Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo abelii, and compared their results with corresponding data from Homo sapiens. Individual saliva samples of 42 apes and 17 humans were collected and quantitated by amino acid analysis, using cation-exchange chromatography with postcolumn derivatization, following acid hydrolysis. We found species-specific differences in the salivary amino acid profiles with average total salivary protein concentration ranging from 308.8 mg/dL in Po. abelii to 1165.6 mg/dL in G. gorilla. Total salivary protein was consistently higher in ape than in human saliva samples (174 mg/dL). All apes had on average also higher relative proline levels than humans did. Histidine levels had the highest concentration in the samples from Po. abelii followed by P. paniscus. In all ape species, the high salivary concentrations of proline and histidine are considered to be indicative of high concentrations of TBSPs in hominids. Given that the species differences in salivary composition obtained in this study correspond with overall patterns of secondary compound content in the diet of wild populations, we assume that salivary composition is resilient to acute and long-lasting changes in diet composition in general and tannin content in particular.
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Aminoácidos , Gorilla gorilla , Pan paniscus , Pan troglodytes , Pongo abelii , Animais , Humanos , Aminoácidos/análise , Gorilla gorilla/metabolismo , Histidina/análise , Pan paniscus/metabolismo , Pan troglodytes/metabolismo , Pongo abelii/metabolismo , Prolina/análise , Saliva/química , Saliva/metabolismo , Proteínas e Peptídeos Salivares/análise , Taninos/análise , Taninos/metabolismo , DietaRESUMO
In most animals, males are considered more aggressive, in terms of frequency and intensity of aggressive behaviors, than their female peers. However, in several species this widespread male-biased aggression pattern is either extenuated, absent, or even sex-reversed. Studies investigating potential neuro-physiological mechanisms driving the selection for female aggression in these species have revealed an important, but not exclusive role of androgens in the expression of the observed sex-specific behavioral patterns. Two very closely related mammalian species that markedly differ in the expression and degree of sex-specific aggression are the two Pan species, where the chimpanzee societies are male-dominated while in bonobos sex-biased aggression patterns are alleviated. Using liquid chromatography-mass spectrometry (LC-MS) methods, we measured levels of plasma testosterone and androstenedione levels in male and female zoo-housed bonobos (N = 21; 12 females, 9 males) and chimpanzees (N = 41; 27 females, 14 males). Our results show comparable absolute and relative intersexual patterns of blood androgen levels in both species of Pan. Plasma testosterone levels were higher in males (bonobos: females: average 0.53 ± 0.30 ng/mL; males 6.70 ± 2.93 ng/mL; chimpanzees: females: average 0.40 ± 0.23 ng/mL; males 5.84 ± 3.63 ng/mL) and plasma androstenedione levels were higher in females of either species (bonobos: females: average 1.83 ± 0.87 ng/mL; males 1.13 ± 0.44 ng/mL; chimpanzees: females: average 1.84 ± 0.92 ng/mL; males 1.22 ± 0.55 ng/mL). The latter result speaks against a role of androstenedione in the mediation of heightened female aggression, as had been suggested based on studies in other mammal species where females are dominant and show high levels of female aggressiveness.
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In animals with slow ontogeny and long-term maternal investment, immatures are likely to experience the birth of a younger sibling before reaching maturity. In these species, the birth of a sibling marks a major event in an offspring's early life as the older siblings experience a decrease in maternal support. The transition to siblinghood (TTS) is often considered to be stressful for the older offspring, but physiological evidence is lacking. To explore the TTS in wild bonobos, we investigated physiological changes in urinary cortisol (stress response), neopterin (cell-mediated immunity), and total triiodothyronine (T3, metabolic rate), as well as changes in behaviors that reflect the mother-offspring relationship. Following a sibling's birth, urinary cortisol levels of the older offspring increased fivefold, independent of their age, and remained elevated for 7 months. The cortisol level increase was associated with declining neopterin levels; however, T3 levels and behavioral measures did not change. Our results indicate that the TTS is accompanied by elevated cortisol levels and that this change does not coincide with nutritional weaning and attainment of physical independence. Our results suggest that bonobos and humans experience TTS in similar ways and that this developmental event may have emerged in the last common ancestor.
Assuntos
Hidrocortisona , Pan paniscus , Animais , Hidrocortisona/urina , Neopterina , Irmãos , Tri-IodotironinaRESUMO
As an integral part of the immune response, testosterone secretion is inhibited when an individual is confronted with an immune challenge. Testosterone-mediated physiological, morphological, and behavioral traits are compromised at times of impaired health. Nevertheless, males of some species seem to maintain high levels of testosterone when confronted with an immune challenge, upholding competitive strength but compromising their immune response. It has been argued that this phenomenon will occur only in species living in social systems with high degrees of male-male competition over mating opportunities. Male chimpanzees contest over access to fertile females and dominants sire the majority of offspring. This male mating pattern makes chimpanzees a candidate species where we could expect males to maintain high testosterone levels, compromising their immune response, to ensure immediate reproductive success. We measured blood testosterone levels in male and female chimpanzees, who expressed clinical symptoms (symptomatic) or showed no evidence of clinical disease on assessment (asymptomatic). For females, we expected to find lower testosterone levels in symptomatic individuals than in asymptomatic subjects. In males, we would predict lower testosterone levels in symptomatic individuals than in asymptomatic males, if the immune response leads to a decrease in testosterone secretion. Alternatively, males could have equal levels of testosterone when symptomatic and asymptomatic, upholding competitive strength. Our results show that male chimpanzees exhibit lower levels of testosterone when confronted with an immune challenge than when being asymptomatic. This suggests that male testosterone secretion is suppressed as part of the immune response, which potentially increases survival and lifetime reproductive success. It will, however, negatively impact momentary competitive ability. Also, males may employ different mating strategies, some of which are less testosterone-driven (e.g., affiliative strategies). Consequently, in some individuals, the costs of maintaining high testosterone levels may not outweigh the potential gain in reproductive success.
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Pan troglodytes , Comportamento Sexual Animal , Animais , Feminino , Humanos , Masculino , Pan troglodytes/fisiologia , Reprodução/fisiologia , Comportamento Sexual Animal/fisiologia , Testosterona/fisiologiaRESUMO
Here we show that sexual signaling affects patterns of female spatial association differently in chimpanzees and bonobos, indicating its relevance in shaping the respective social systems. Generally, spatial association between females often mirrors patterns and strength of social relationships and cooperation within groups. While testing for proposed differences in female-female associations underlying female coalition formation in the species of the genus Pan, we find only limited evidence for a higher female-female gregariousness in bonobos. While bonobo females exhibited a slightly higher average number of females in their parties, there is neither a species difference in the time females spent alone, nor in the number of female party members in the absence of sexually attractive females. We find that the more frequent presence of maximally tumescent females in bonobos is associated with a significantly stronger increase in the number of female party members, independent of variation in a behavioural proxy for food abundance. This indicates the need to look beyond ecology when explaining species differences in female sociality as it refutes the idea that the higher gregariousness among bonobo females is driven by ecological factors alone and highlights that the temporal distribution of female sexual receptivity is an important factor to consider when studying mammalian sociality.
Assuntos
Preferência de Acasalamento Animal , Pan paniscus/psicologia , Pan troglodytes/psicologia , Comportamento Social , Animais , FemininoRESUMO
OBJECTIVES: Existing data on bonobo and chimpanzee dental eruption timing are derived predominantly from captive individuals or deceased wild individuals. However, recent advances in noninvasive photographic monitoring of living, wild apes have enabled researchers to characterize dental eruption in relatively healthy individuals under naturalistic conditions. At present, such data are available for only one population of wild chimpanzees. We report data for an additional population of wild chimpanzees and the first dental eruption data for wild bonobos. MATERIALS AND METHODS: We collected photographs and video footage of teeth from the open mouths of wild bonobos and East African chimpanzees of known age from LuiKotale, Democratic Republic of the Congo, and Gombe National Park, Tanzania, respectively. We scored the presence and absence of deciduous teeth from photographs and video footage to characterize deciduous dental eruption timing in these two populations. RESULTS: Deciduous dental eruption ages in our sample fall within the range of variation previously documented for captive chimpanzees, but eruption ages are later in wild than in captive contexts. We found substantial variation in deciduous canine eruption timing, particularly among bonobos. One bonobo had a deciduous canine present by 227 days old while another did not have a deciduous canine present at 477 days old. DISCUSSION: Our data indicate that deciduous teeth erupt later in wild individuals than in captive individuals. We also found that deciduous dental eruption timing varies considerably between individuals within our study populations, a pattern that is consistent with previous studies. Future studies should consider sources of variation in deciduous canine eruption timing and relationships with other aspects of life history as additional data become available.
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Hominidae , Pan troglodytes , Animais , Humanos , Pan paniscus , Tanzânia , Erupção DentáriaRESUMO
Predation is a major cause of mortality in non-human primates, and considered a selective force in the evolution of primate societies. Although larger body size is considered as protection against predation, evidence for predation on great apes by carnivores comes from chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla), and orangutans (Pongo spp.). Here, we describe the first encounter between wild bonobos (Pan paniscus) and a leopard (Panthera pardus). A single leopard was confronted by a group of habituated bonobos for three hours. Two adult males and one adolescent female bonobo actively harassed the leopard, which remained still for most of the encounter and reacted only to close approaches by bonobos. While no predation was observed, their behaviours confirm that bonobos perceive leopards as potential predators. Our report adds novel information to descriptions from other African ape species, and sheds light on the behavioural repertoire of bonobos' anti-predation strategies. For future investigations, we suggest tagging leopards to remotely monitor their movements and allow assessment of encounter rates as one of several factors influencing predation pressure.
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Pan paniscus , Panthera/fisiologia , Comportamento Predatório , Animais , República Democrática do Congo , Feminino , MasculinoRESUMO
Fission-fusion dynamics have evolved in a broad range of animal taxa and are thought to allow individuals to mitigate feeding competition. While this is the principal benefit of fission-fusion, few studies have evaluated its costs. We compared gregariousness, foraging budgets, and social budgets between lactating bonobos and chimpanzees from wild populations to evaluate potential costs. Both species exhibit fission-fusion dynamics, but chimpanzees, particularly in East African populations, appear to experience higher feeding competition than bonobos. We expected lactating chimpanzees to be less gregarious than lactating bonobos; reduced gregariousness should allow lactating chimpanzees to mitigate the costs of higher feeding competition without requiring more foraging effort. However, we expected the reduced gregariousness of lactating chimpanzees to limit their time available for affiliative interactions. Using long-term data from LuiKotale bonobos and Gombe chimpanzees, we found that lactating chimpanzees were indeed less gregarious than lactating bonobos, while feeding and travel time did not differ between species. Contrary to our predictions, lactating females did not differ in social interaction time, and lactating chimpanzees spent proportionately more time interacting with individuals other than their immature offspring. Our results indicate that lactating chimpanzees can maintain social budgets comparable to lactating bonobos despite reduced gregariousness and without incurring additional foraging costs. We discuss potential explanations for why lactating bonobos are more gregarious.
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OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.
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Alimentos Fermentados , Animais , Dieta , Ecossistema , Frutas , PrimatasRESUMO
AbstractQuantifying physiological challenges has gained increasing importance in evolutionary biology, behavioral physiology, and conservation. One matrix that is particularly useful for obtaining long-term records of physiological changes in mammals is hair. Potential markers are components of the endocannabinoid (EC) system, which regulates homeostasis of the brain as well as the endocrine and immune systems. Here, we present results from the first study to measure ECs (anandamide [AEA], 2-archidonyl glycerol [2-AG]) and EC-like compounds (N-palmitoylethanolamine [PEA], N-oleoylethanolamine [OEA], N-stearoylethanolamine [SEA]) in the hair of a nonhuman primate. We found that AEA, SEA, PEA, and OEA can be reliably measured in hair samples. When comparing the measurements of hair from different body parts, we found that variations of some analytes suggest that hair location is likely to affect results. For changes in health status, measurements of ECs and EC-like compounds reflected differences at both intra- and interindividual levels. We concluded that the EC system potentially provides novel tools to assess well-being, health status, and metabolic stress-not only in the hair of humans but also in that of domestic and wild animals. Measuring changes in ECs and EC-like compounds may improve the long-term monitoring of health status in captive and wild primates and may serve as a useful measure in animal welfare programs.
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Endocanabinoides/metabolismo , Cabelo/química , Homeostase/fisiologia , Pan paniscus/fisiologia , Animais , Biomarcadores/química , Endocanabinoides/química , Feminino , Cabelo/fisiologia , MasculinoRESUMO
Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.
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Hidrocortisona/urina , Pan paniscus/metabolismo , Pan troglodytes/metabolismo , Animais , Feminino , Masculino , Pan paniscus/crescimento & desenvolvimento , Pan troglodytes/crescimento & desenvolvimento , Especificidade da EspécieRESUMO
Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The 'interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the 'social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability.
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Comportamento Animal , Pan paniscus/fisiologia , Pan troglodytes/fisiologia , Comportamento Social , Animais , Cognição , Comportamento Cooperativo , SerpentesRESUMO
OBJECTIVES: Primates exhibit variation in rates of growth and development. Variation in female growth and development across ape species appears to be explained by the Ecological Risk Aversion Hypothesis (ERAH). Indeed, existing data on variation in somatic growth and reproductive maturation between humans' closest living ape relatives, bonobos and chimpanzees, appear to be consistent with this hypothesis. However, existing data on behavioral maturation between the two species appear to contradict this hypothesis. We present novel behavioral data on infant and juvenile females from wild populations of both species in order to further evaluate predictions of the ERAH as it relates to the speed of behavioral maturation. MATERIALS AND METHODS: We analyzed 3 years of behavioral data on 17 female bonobos (<8 years of age) from LuiKotale, Democratic Republic of the Congo and 40 years of behavioral data on 30 age-matched female chimpanzees from Gombe, Tanzania. We compared the timing of (a) the attainment of independence from mothers and (b) the development of social skills using the following proxies: proximity between females and their mothers and the time that females spent engaged in eating, suckling, social play, social grooming, and riding on their mothers. RESULTS: We did not find species differences in the proportion of time that females spent in contact with their mothers or engaged in eating, suckling, social play, or social grooming. Female bonobos spent more time riding on their mothers than did female chimpanzees. Female bonobos spent more time at distances greater than 5 m from their mothers during the ages of 3-8 years, but females did not differ during the ages of 0-3 years. DISCUSSION: Behavioral maturation is largely similar between females of the two species based on the ages and proxies considered herein. We propose alternative explanations for the differences that we found in proximity and riding that do not invoke differences in underlying rates of maturation.
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Comportamento Animal , Pan paniscus/psicologia , Pan troglodytes/psicologia , Comportamento Social , Animais , República Democrática do Congo , Feminino , Pan paniscus/crescimento & desenvolvimento , Pan troglodytes/crescimento & desenvolvimento , TanzâniaRESUMO
Monitoring metabolic activity in wild living animals has become of particular interest in the field of ecological research. Methods for the repeated non-invasive sampling of individuals are needed. Thyroid hormones (TH) are involved in the regulation of metabolic activity, and their measurement can be used as a proxy to monitor metabolic changes. During periods of low energy intake, serum TH levels are reduced, leading to a decrease in metabolic activity. Using urine samples collected during a food restriction experiment in captive bonobos we validated a total triiodthyronin (TT3) enzyme immunoassay (EIA) for the monitoring of metabolic changes. We found that the majority of immune reactivity of the assay in the urine samples could be explained through immunoreactivity to T3. Furthermore, urinary T3 was stable through repeated freeze-thaw cycles but prolonged exposure to room temperature lead to degradation. Most importantly, we found that for all animals urinary total T3 levels were higher when more digestible energy was consumed. We concluded that urinary total T3 measurements are a suitable method for monitoring metabolic changes in bonobos and potentially in a wide range of animal species.