Publications by authors named "Jeroen M G Stevens"

29 Publications

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Erratum to "Bonobos and chimpanzees preferentially attend to familiar members of the dominant sex" [ 177 (2021) 193-206].

Anim Behav 2021 Jul;177:303

School of Psychology & Neuroscience, University of St Andrews, St Andrews, U.K.

[This corrects the article DOI: 10.1016/j.anbehav.2021.04.027.].
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http://dx.doi.org/10.1016/j.anbehav.2021.06.014DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8274698PMC
July 2021

Time-lag of urinary and salivary cortisol response after a psychological stressor in bonobos (Pan paniscus).

Sci Rep 2021 04 12;11(1):7905. Epub 2021 Apr 12.

Behavioural Ecology and Ecophysiology Group, Department of Biology, University of Antwerp, Antwerp, Belgium.

Cortisol is often measured as a marker for stress. Therefore, a profound validation of the time-lag between the stressor and the increase and peak in cortisol levels is needed. No study measured both the urinary and salivary cortisol time-lag after a psychological stressor. In this study, we used a frequent sampling study design to (1) describe the urinary and salivary cortisol pattern during a control day; and (2) characterize the induced excretion pattern of urinary and salivary cortisol after a psychological stressor in six zoo-housed bonobos. Liquid chromatography-tandem mass spectrometry was used to analyze 71 urine and 162 saliva samples collected on a control and a test day. We found that the time-lag between the stressor and the maximal cortisol concentration was similar in urine and saliva (160 min after the stressor). However, salivary cortisol after the stressor did show a faster and steeper increase than urinary cortisol. We also show inter-individual variation in the baseline and stress levels of cortisol, which should be considered in future cortisol studies. Our research highlights the importance of validation studies to confirm relevant sampling windows for cortisol sampling in order to obtain biologically meaningful results.
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http://dx.doi.org/10.1038/s41598-021-87163-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8041877PMC
April 2021

The Pan social brain: An evolutionary history of neurochemical receptor genes and their potential impact on sociocognitive differences.

J Hum Evol 2021 03 10;152:102949. Epub 2021 Feb 10.

Behavioral Ecology and Ecophysiology Group, Department of Biology, University of Antwerp, Universiteitsplein 1, 2610, Wilrijk, Belgium.

Humans have unique cognitive capacities that, compared with apes, are not only simply expressed as a higher level of general intelligence, but also as a quantitative difference in sociocognitive skills. Humans' closest living relatives, bonobos (Pan paniscus), and chimpanzees (Pan troglodytes), show key between-species differences in social cognition despite their close phylogenetic relatedness, with bonobos arguably showing greater similarities to humans. To better understand the evolution of these traits, we investigate the neurochemical mechanisms underlying sociocognitive skills by focusing on variation in genes encoding proteins with well-documented roles in mammalian social cognition: the receptors for vasopressin (AVPR1A), oxytocin (OXTR), serotonin (HTR1A), and dopamine (DRD2). Although these genes have been well studied in humans, little is known about variation in these genes that may underlie differences in social behavior and cognition in apes. We comparatively analyzed sequence data for 33 bonobos and 57 chimpanzees, together with orthologous sequence data for other apes. In all four genes, we describe genetic variants that alter the amino acid sequence of the respective receptors, raising the possibility that ligand binding or signal transduction may be impacted. Overall, bonobos show 57% more fixed substitutions than chimpanzees compared with the ancestral Pan lineage. Chimpanzees, show 31% more polymorphic coding variation, in line with their larger historical effective population size estimates and current wider distribution. An extensive literature review comparing allelic changes in Pan with known human behavioral variants revealed evidence of homologous evolution in bonobos and humans (OXTR rs4686301(T) and rs237897(A)), while humans and chimpanzees shared OXTR rs2228485(A), DRD2 rs6277(A), and DRD2 rs11214613(A) to the exclusion of bonobos. Our results offer the first in-depth comparison of neurochemical receptor gene variation in Pan and put forward new variants for future behavior-genotype association studies in apes, which can increase our understanding of the evolution of social cognition in modern humans.
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http://dx.doi.org/10.1016/j.jhevol.2021.102949DOI Listing
March 2021

Exploring the Utility of Hair Endocannabinoids for Monitoring Homeostasis in Bonobos.

Physiol Biochem Zool 2021 Mar-Apr;94(2):83-98

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 (-palmitoylethanolamine [PEA], -oleoylethanolamine [OEA], -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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http://dx.doi.org/10.1086/712658DOI Listing
August 2021

Food preference and nutrient composition in captive bonobos (Pan paniscus).

Primates 2020 Sep 3;61(5):661-671. Epub 2020 Apr 3.

Behavioural Ecology and Ecophysiology Group, Department of Biology, University of Antwerp, Antwerp, Belgium.

Food preference has been studied in a range of Hominoidea in the wild and in captivity, allowing for interspecific comparisons. Chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla gorilla) prefer low-fibre, high-sugar foods, suggesting that frugivory and their dietary overlap are a result of their shared preference for the same nutrients. Comparable tests of the nutritional preference of bonobos do not exist. In this study we examined food preferences of five captive bonobos for 23 familiar and ten novel food items. We performed paired-choice food tests, resulting in a clear rank order in food preference, with minor individual differences. Fruits were more preferred than vegetables. We correlated nutritional composition of the food items with the bonobos' preference. We found that preferences for familiar food items were positively correlated with total energy and carbohydrate content and negatively correlated with water and micronutrient (sodium, calcium, phosphorus, iron, zinc, manganese, selenium) content. Food preference for the novel food items also showed a significant positive correlation with total energy and carbohydrate content. Our study supports the idea that food preference among bonobos follows the pattern of the other great apes and that the shared frugivorous diets may be the result of a common preference for the same nutrients. In the wild, these preferences may be less clear due to the interference of preferred nutrients with secondary compounds. Combining food preference data and nutritional information can help in providing a healthy diet with a balanced nutrient composition in captivity. Individual food preferences can help in optimizing food choice for positive reinforcement training and food-related tasks in future research.
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http://dx.doi.org/10.1007/s10329-020-00813-6DOI Listing
September 2020

Social culture in bonobos.

Curr Biol 2020 03;30(6):R261-R262

Behavioral Ecology and Ecophysiology Group, Department of Biology, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium; Centre for Research and Conservation, Royal Zoological Society of Antwerp, K. Astridplein 26, B 2018 Antwerp, Belgium. Electronic address:

Van Leeuwen et al. found that two peculiar interactive behaviors (social scratching and groom slapping) transmitted socially through bonobo networks across six European zoos.
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http://dx.doi.org/10.1016/j.cub.2020.02.038DOI Listing
March 2020

Bonobo personality predicts friendship.

Sci Rep 2019 12 17;9(1):19245. Epub 2019 Dec 17.

Behavioural Ecology and Ecophysiology Group, Department of Biology, University of Antwerp, Antwerp, Belgium.

In bonobos, strong bonds have been documented between unrelated females and between mothers and their adult sons, which can have important fitness benefits. Often age, sex or kinship similarity have been used to explain social bond strength variation. Recent studies in other species also stress the importance of personality, but this relationship remains to be investigated in bonobos. We used behavioral observations on 39 adult and adolescent bonobos housed in 5 European zoos to study the role of personality similarity in dyadic relationship quality. Dimension reduction analyses on individual and dyadic behavioral scores revealed multidimensional personality (Sociability, Openness, Boldness, Activity) and relationship quality components (value, compatibility). We show that, aside from relatedness and sex combination of the dyad, relationship quality is also associated with personality similarity of both partners. While similarity in Sociability resulted in higher relationship values, lower relationship compatibility was found between bonobos with similar Activity scores. The results of this study expand our understanding of the mechanisms underlying social bond formation in anthropoid apes. In addition, we suggest that future studies in closely related species like chimpanzees should implement identical methods for assessing bond strength to shed further light on the evolution of this phenomenon.
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http://dx.doi.org/10.1038/s41598-019-55884-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6917795PMC
December 2019

Higher fundamental frequency in bonobos is explained by larynx morphology.

Curr Biol 2018 10;28(20):R1188-R1189

Department of Primatology, Max-Planck-Institute for Evolutionary Anthropology, Leipzig, Germany. Electronic address:

Acoustic signals, shaped by natural and sexual selection, reveal ecological and social selection pressures [1]. Examining acoustic signals together with morphology can be particularly revealing. But this approach has rarely been applied to primates, where clues to the evolutionary trajectory of human communication may be found. Across vertebrate species, there is a close relationship between body size and acoustic parameters, such as formant dispersion and fundamental frequency (f0). Deviations from this acoustic allometry usually produce calls with a lower f0 than expected for a given body size, often due to morphological adaptations in the larynx or vocal tract [2]. An unusual example of an obvious mismatch between fundamental frequency and body size is found in the two closest living relatives of humans, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although these two ape species overlap in body size [3], bonobo calls have a strikingly higher f0 than corresponding calls from chimpanzees [4]. Here, we compare acoustic structures of calls from bonobos and chimpanzees in relation to their larynx morphology. We found that shorter vocal fold length in bonobos compared to chimpanzees accounted for species differences in f0, showing a rare case of positive selection for signal diminution in both bonobo sexes.
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http://dx.doi.org/10.1016/j.cub.2018.09.030DOI Listing
October 2018

Segmental morphometrics of bonobos (Pan paniscus): are they really different from chimpanzees (Pan troglodytes)?

J Anat 2018 12 7;233(6):843-853. Epub 2018 Oct 7.

Behavioural Ecology and Ecophysiology Group, University of Antwerp, Wilrijk, Belgium.

The inertial properties of body segments reflect performance and locomotor habits in primates. While Pan paniscus is generally described as more gracile, lighter in body mass, and as having relatively longer and heavier hindlimbs than Pan troglodytes, both species exhibit very similar patterns of (quadrupedal and bipedal) kinematics, but show slightly different locomotor repertoires. We used a geometric model to estimate the inertial properties for all body segments (i.e. head, trunk, upper and lower arms, hand, thigh, shank and foot) using external length and diameter measurements of 12 anaesthetized bonobos (eight adults and four immatures). We also calculated whole limb inertial properties. When we compared absolute and relative segment morphometric and inertial variables between bonobos and chimpanzees, we found that adult bonobos are significantly lighter than adult chimpanzees. The bonobo is also shorter in head length, upper and lower arm lengths, and foot length, and is generally lighter in most absolute segment mass values (except head and hand). In contrast, the bonobo has a longer trunk. When scaled relative to body mass, most differences disappear between the two species. Only the longer trunk and the shorter head of the bonobo remain apparent, as well as the lighter thigh compared with the chimpanzee. We found similar values of natural pendular periods of the limbs in both species, despite differences in absolute limb lengths, masses, mass centres (for the hindlimb) and moments of inertia. While our data contradict the commonly accepted view that bonobos have relatively longer and heavier hindlimbs than chimpanzees, they are consistent with the observed similarities in the quadrupedal and bipedal kinematics between these species. The morphological differences between both species are more subtle than those previously described from postcranial osteological materials.
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http://dx.doi.org/10.1111/joa.12894DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6231171PMC
December 2018

Does the MHC Confer Protection against Malaria in Bonobos?

Trends Immunol 2018 10 17;39(10):768-771. Epub 2018 Aug 17.

Biomedical Primate Research Centre, Department of Comparative Genetics and Refinement, Rijswijk, The Netherlands; Department of Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, The Netherlands. Electronic address:

The immunological factors that could explain the near absence of malaria parasites in bonobos are not yet understood. The MHC class I system, however, may play an important role, as particular bonobo allotypes show functional similarities to HLA-B*53/B*78, which are considered to confer protection against malaria in humans.
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http://dx.doi.org/10.1016/j.it.2018.07.004DOI Listing
October 2018

Insights into the musculature of the bonobo hand.

J Anat 2018 Jun 25. Epub 2018 Jun 25.

Muscles & Movement, Biomedical Sciences Group, University of Leuven Campus Kulak, Kortrijk, Belgium.

The human hand is well known for its unique dexterity which is largely facilitated by a highly mobile, long and powerful thumb that enables both tool manufacturing and use, a key component of human evolution. The bonobo (Pan paniscus), the closest extant relative to modern humans together with the chimpanzee (Pan troglodytes), also possesses good manipulative capabilities but with a lower level of dexterity compared with modern humans. Despite the close phylogenetic relationship between bonobos and humans, detailed quantitative data of the bonobo forelimb musculature remains largely lacking. To understand how morphology may influence dexterity, we investigated the functional anatomy of the bonobo hand using a unique sample of eight bonobo cadavers, along with one chimpanzee and one human (Homo sapiens) cadaver. We performed detailed dissections of unembalmed specimens to collect quantitative datasets of the extrinsic and intrinsic hand musculature, in addition to qualitative descriptions of the forelimb muscle configurations, allowing estimation of force-generating capacities for each functional group. Furthermore, we used medical imaging to quantify the articular surface of the trapeziometacarpal joint to estimate the intra-articular pressure. Our results show that the force-generating capacity for most functional groups of the extrinsic and intrinsic hand muscles in bonobos is largely similar to that of humans, with differences in relative importance of the extensors and rotators. The bonobo thumb musculature has a lower force-generating capacity than observed in the human specimen, but the estimated maximal intra-articular pressure is higher in bonobos. Most importantly, bonobos show a higher degree of functional coupling between the muscles of the thumb, index and lateral fingers than observed in humans. It is conceivable that differentiation and individualization of the hand muscles rather than relative muscle development explain the higher level of dexterity of humans compared with that of bonobos.
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http://dx.doi.org/10.1111/joa.12841DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6081514PMC
June 2018

Hand pressures during arboreal locomotion in captive bonobos ().

J Exp Biol 2018 04 19;221(Pt 8). Epub 2018 Apr 19.

Animal Postcranial Evolution (APE) Lab, Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury CT2 7NR, UK

Evolution of the human hand has undergone a transition from use during locomotion to use primarily for manipulation. Previous comparative morphological and biomechanical studies have focused on potential changes in manipulative abilities during human hand evolution, but few have focused on functional signals for arboreal locomotion. Here, we provide this comparative context though the first analysis of hand loading in captive bonobos during arboreal locomotion. We quantify pressure experienced by the fingers, palm and thumb in bonobos during vertical locomotion, suspension and arboreal knuckle-walking. The results show that pressure experienced by the fingers is significantly higher during knuckle-walking compared with similar pressures experienced by the fingers and palm during suspensory and vertical locomotion. Peak pressure is most often experienced at or around the third digit in all locomotor modes. Pressure quantified for the thumb is either very low or absent, despite the thumb making contact with the substrate during all suspensory and vertical locomotor trials. Unlike chimpanzees, bonobos do not show a rolling pattern of digit contact with the substrate during arboreal knuckle-walking - instead, we found that digits 3 and 4 typically touch down first and digit 5 almost always made contact with the substrate. These results have implications for interpreting extant and fossilized hand morphology; we expect bonobo (and chimpanzee) bony morphology to primarily reflect the biomechanical loading of knuckle-walking, while functional signals for arboreal locomotion in fossil hominins are most likely to appear in the fingers, particularly digit 3, and least likely to appear in the morphology of the thumb.
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http://dx.doi.org/10.1242/jeb.170910DOI Listing
April 2018

Limited MHC class I intron 2 repertoire variation in bonobos.

Immunogenetics 2017 10 16;69(10):677-688. Epub 2017 Jun 16.

Biomedical Primate Research Centre, Department of Comparative Genetics & Refinement, Rijswijk, The Netherlands.

Common chimpanzees (Pan troglodytes) experienced a selective sweep, probably caused by a SIV-like virus, which targeted their MHC class I repertoire. Based on MHC class I intron 2 data analyses, this selective sweep took place about 2-3 million years ago. As a consequence, common chimpanzees have a skewed MHC class I repertoire that is enriched for allotypes that are able to recognise conserved regions of the SIV proteome. The bonobo (Pan paniscus) shared an ancestor with common chimpanzees approximately 1.5 to 2 million years ago. To investigate whether the signature of this selective sweep is also detectable in bonobos, the MHC class I gene repertoire of two bonobo panels comprising in total 29 animals was investigated by Sanger sequencing. We identified 14 Papa-A, 20 Papa-B and 11 Papa-C alleles, of which eight, five and eight alleles, respectively, have not been reported previously. Within this pool of MHC class I variation, we recovered only 2 Papa-A, 3 Papa-B and 6 Papa-C intron 2 sequences. As compared to humans, bonobos appear to have an even more diminished MHC class I intron 2 lineage repertoire than common chimpanzees. This supports the notion that the selective sweep may have predated the speciation of common chimpanzees and bonobos. The further reduction of the MHC class I intron 2 lineage repertoire observed in bonobos as compared to the common chimpanzee may be explained by a founding effect or other subsequent selective processes.
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http://dx.doi.org/10.1007/s00251-017-1010-xDOI Listing
October 2017

Validation of a Method for the Assessment of Urinary Neopterin Levels to Monitor Health Status in Non-human-primate Species.

Front Physiol 2017 6;8:51. Epub 2017 Feb 6.

Department for Primatology, Max Planck Institute for Evolutionary Anthropology Leipzig, Germany.

Determining individual health status is of great importance for a better understanding of life history trade-offs between growth, reproduction, and maintenance. However, existing immunological methods are invasive and therefore not suitable for investigating health status in wild populations. Thus, there is an urgent need for non-invasive methods to assess the immune status of animals. Neopterin is involved in the cell-mediated pathway of the immune response (Th1-type), secreted during the activation of monocytes and macrophages. We investigated if urinary neopterin could serve as a biomarker of health status in bonobos and chimpanzees. First, we performed a chemical validation of a commercial neopterin enzyme immune assay (EIA) for bonobo and chimpanzee urine. We then examined if urinary neopterin levels in bonobos increase during the acute period of respiratory infections. We found that neopterin levels can be reliably measured in urine of the two species with a commercial EIA. Stability experiments revealed considerable changes in urinary neopterin levels in relation to multiple freeze-thaw cycles and extended exposure to room temperature. Exposure to sunlight led to a degradation of urinary neopterin, whereas sample storage up to 2 years did not affect urinary neopterin levels. There was no detectable diurnal variation in neopterin levels, and levels remained very stable across several days in healthy individuals. While urinary neopterin levels were independent of sex, non-adult individuals had higher urinary neopterin levels than adults. Most importantly, there was a significant increase in urinary neopterin levels during a period of respiratory infection. Our results demonstrate that regular urine sample collection would allow for the monitoring of individual health status and disease progression with minimal disturbance of the subjects. In combination with behavioral, life history, and endocrinological parameters, the method can be used to investigate questions related to immunocompetence handicaps or life history trade-offs.
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http://dx.doi.org/10.3389/fphys.2017.00051DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5292569PMC
February 2017

Bonobo personality traits are heritable and associated with vasopressin receptor gene 1a variation.

Sci Rep 2016 12 2;6:38193. Epub 2016 Dec 2.

Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium.

Despite being closely related, bonobos and chimpanzees show remarkable behavioral differences, the proximate origins of which remain unknown. This study examined the link between behavioral variation and variation in the vasopressin 1a receptor gene (Avpr1a) in bonobos. Chimpanzees are polymorphic for a ~360 bp deletion (DupB), which includes a microsatellite (RS3) in the 5' promoter region of Avpr1a. In chimpanzees, the DupB deletion has been linked to lower sociability, lower social sensitivity, and higher anxiety. Chimpanzees and bonobos differ on these traits, leading some to believe that the absence of the DupB deletion in bonobos may be partly responsible for these differences, and to the prediction that similar associations between Avpr1a genotypes and personality traits should be present in bonobos. We identified bonobo personality dimensions using behavioral measures (Sociability, Boldness, Openness, Activity) and trait ratings (Assertiveness, Conscientiousness, Openness, Agreeableness, Attentiveness, Extraversion). In the present study we found that all 10 dimensions have nonzero heritabilities, indicating there is a genetic basis to personality, and that bonobos homozygous for shorter RS3 alleles were lower in Attentiveness and higher in Openness. These results suggest that variations in Avpr1a genotypes explain both within and between species differences in personality traits of bonobos and chimpanzees.
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http://dx.doi.org/10.1038/srep38193DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5133571PMC
December 2016

Sex Differences in Age-Related Decline of Urinary Insulin-Like Growth Factor-Binding Protein-3 Levels in Adult Bonobos and Chimpanzees.

Front Endocrinol (Lausanne) 2016 23;7:118. Epub 2016 Aug 23.

Department of Primatology, Max Planck Institute for Evolutionary Anthropology , Leipzig , Germany.

There is increasing interest in the characterization of normative senescence in humans. To assess to what extent aging patterns in humans are unique, comparative data from closely related species, such as non-human primates, can be very useful. Here, we use data from bonobos and chimpanzees, two closely related species that share a common ancestor with humans, to explore physiological markers that are indicative of aging processes. Many studies on aging in humans focus on the somatotropic axis, consisting of growth hormone (GH), insulin-like growth factors (IGFs), and IGF binding proteins (IGFBPs). In humans, IGFBP-3 levels decline steadily with increasing age. We used urinary IGFBP-3 levels as an alternative endocrine marker for IGF-I to identify the temporal pattern known to be related with age-related changes in cell proliferation, growth, and apoptosis. We measured urinary IGFBP-3 levels in samples from 71 bonobos and 102 chimpanzees. Focusing on samples from individuals aged 10 years or older, we found that urinary IGFBP-3 levels decline in both ape species with increasing age. However, in both species, females start with higher urinary IGFBP-3 levels than males, experience a steeper decline with increasing age, and converge with male levels around the age of 30-35 years. Our measurements of urinary IGFBP-3 levels indicate that bonobos and chimpanzees mirror human patterns of age-related decline in IGFBP-3 in older individuals (<10 years) of both sexes. Moreover, such as humans, both ape species show sex-specific differences in IGFBP-3 levels with females having higher levels than males, a result that correlates with sex differences in life expectancy. Using changes in urinary IGFBP-3 levels as a proxy for changes in GH and IGF-I levels that mark age-related changes in cell proliferation, this approach provides an opportunity to investigate trade-offs in life-history strategies in cross-sectional and in longitudinal studies, both in captivity and in the wild.
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http://dx.doi.org/10.3389/fendo.2016.00118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4994059PMC
September 2016

Within arm's reach: Measuring forearm length to assess growth patterns in captive bonobos and chimpanzees.

Am J Phys Anthropol 2016 09 3;161(1):37-43. Epub 2016 May 3.

Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Objectives: Bonobos and chimpanzees are known to differ in various morphological traits, a dichotomy that is sometimes used as an analogy for evolutionary splits during human evolution. The aim of our study was to measure the forearm length of immature and adult bonobos and adult chimpanzees to assess the extent of age-related changes of forearm length in bonobos and sex-dimorphism in bonobos and chimpanzees.

Materials And Methods: As a proxy of somatic growth we measured forearm length of captive bonobos and chimpanzees ranging in age from 1 to 55 years. Measures were taken from subjects inserting their arms into a transparent Plexiglas® tube, a novel technique facilitating repeated measures of nonanesthetized apes in captivity.

Results: Measures from adult females (>12 years) showed that bonobos exceed chimpanzees in terms of forearm length and that sexual dimorphism in forearm length is pronounced in chimpanzees, but not in bonobos. Forearm length increased significantly with chronological age in bonobos. Validation tests revealed that the device generates useful data on morphometric dimensions.

Discussion: In most primates, sexual dimorphism in body size is male-biased and the differences in forearm length in chimpanzees follow this trend. Given that males of the two species did not differ in forearm length, the absence/presence of sexual dimorphism of this trait must be due to differences in somatic growth in females. Our novel method offers an alternative to obtain morphometric measures and facilitates longitudinal studies on somatic growth. Am J Phys Anthropol 161:37-43, 2016. © 2016 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/ajpa.23004DOI Listing
September 2016

Patterns of Behaviour, Group Structure and Reproductive Status Predict Levels of Glucocorticoid Metabolites in Zoo-Housed Ring-Tailed Lemurs, Lemur catta.

Folia Primatol (Basel) 2015 30;86(6):506-24. Epub 2016 Jan 30.

Department of Biological Sciences, University of Chester, Chester, UK.

In ring-tailed lemurs, Lemur catta, the factors modulating hypothalamic-pituitary-adrenal (HPA) activity differ between wild and semi-free-ranging populations. Here we assess factors modulating HPA activity in ring-tailed lemurs housed in a third environment: the zoo. First we validate an enzyme immunoassay to quantify levels of glucocorticoid (GC) metabolites in the faeces of L. catta. We determine the nature of the female-female dominance hierarchies within each group by computing David's scores and examining these in relation to faecal GC (fGC). Relationships between female age and fGC are assessed to evaluate potential age-related confounds. The associations between fGC, numbers of males in a group and reproductive status are explored. Finally, we investigate the value of 7 behaviours in predicting levels of fGC. The study revealed stable linear dominance hierarchies in females within each group. The number of males in a social group together with reproductive status, but not age, influenced fGC. The 7 behavioural variables accounted for 68% of the variance in fGC. The amounts of time an animal spent locomoting and in the inside enclosure were both negative predictors of fGC. The study highlights the flexibility and adaptability of the HPA system in ring-tailed lemurs.
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http://dx.doi.org/10.1159/000442587DOI Listing
October 2016

Chimpanzee sociability is associated with vasopressin (Avpr1a) but not oxytocin receptor gene (OXTR) variation.

Horm Behav 2015 Sep 20;75:84-90. Epub 2015 Aug 20.

Centre for Research and Conservation, Royal Zoological Society of Antwerp, B-2018 Antwerp, Belgium; University of Antwerp, Department of Biology, B-2610 Antwerp, Belgium. Electronic address:

The importance of genes in regulating phenotypic variation of personality traits in humans and animals is becoming increasingly apparent in recent studies. Here we focus on variation in the vasopressin receptor gene 1a (Avpr1a) and oxytocin receptor gene (OXTR) and their effects on social personality traits in chimpanzees. We combine newly available genetic data on Avpr1a and OXTR allelic variation of 62 captive chimpanzees with individual variation in personality, based on behavioral assessments. Our study provides support for the positive association of the Avpr1a promoter region, in particular the presence of DupB, and sociability in chimpanzees. This complements findings of previous studies on adolescent chimpanzees and studies that assessed personality using questionnaire data. In contrast, no significant associations were found for the single nucleotide polymorphism (SNP) ss1388116472 of the OXTR and any of the personality components. Most importantly, our study provides additional evidence for the regulatory function of the 5' promoter region of Avpr1a on social behavior and its evolutionary stable effect across species, including rodents, chimpanzees and humans. Although it is generally accepted that complex social behavior is regulated by a combination of genes, the environment and their interaction, our findings highlight the importance of candidate genes with large effects on behavioral variation.
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http://dx.doi.org/10.1016/j.yhbeh.2015.08.006DOI Listing
September 2015

Personality in Bonobos.

Psychol Sci 2015 Sep 24;26(9):1430-9. Epub 2015 Jul 24.

Centre for Research and Conservation, Royal Zoological Society of Antwerp.

To better understand human and chimpanzee personality evolution, we obtained trait ratings of personality for 154 captive bonobos (~80% of the U.S. and European population). We found factors that we labeled Assertiveness, Conscientiousness, Openness, Agreeableness, Attentiveness, and Extraversion. The interrater reliabilities and test-retest reliabilities for these factors were comparable to those found in humans and other species. Using orthogonal targeted Procrustes rotations, we compared the bonobo dimensions with those of three samples of captive chimpanzees. Overall congruence coefficients indicated a fair degree of similarity; at the factor level, there was good evidence for Assertiveness, Conscientiousness, Openness, and Agreeableness in the chimpanzee samples; evidence for Attentiveness and Extraversion was poor. These findings suggest that, as expected given their close phylogenetic relationship, bonobo personality structure resembles chimpanzee personality structure in some respects. However, divergent evolution, perhaps as a result of socioecological differences between bonobos and chimpanzees, also appears to have shaped personality structure in these species.
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http://dx.doi.org/10.1177/0956797615589933DOI Listing
September 2015

Bonobos show limited social tolerance in a group setting: a comparison with chimpanzees and a test of the relational model.

Folia Primatol (Basel) 2015 28;86(3):164-77. Epub 2015 Apr 28.

Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, The Netherlands.

Social tolerance is a core aspect of primate social relationships with implications for the evolution of cooperation, prosociality and social learning. We measured the social tolerance of bonobos in an experiment recently validated with chimpanzees to allow for a comparative assessment of group-level tolerance, and found that the bonobo group studied here exhibited lower social tolerance on average than chimpanzees in this paradigm. Furthermore, following the Relational Model of de Waal, we investigated whether bonobos responded to an increased potential for social conflict with tolerance, conflict avoidance or conflict escalation, and found that only behaviours indicative of conflict escalation differed across conditions. Taken together, these findings contribute to the current debate over the level of social tolerance of bonobos and lend support to the position that the social tolerance of bonobos may not be notably high compared with other primates.
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http://dx.doi.org/10.1159/000373886DOI Listing
January 2016

Oxytocin and vasopressin receptor gene variation as a proximate base for inter- and intraspecific behavioral differences in bonobos and chimpanzees.

PLoS One 2014 18;9(11):e113364. Epub 2014 Nov 18.

University of Antwerp, Department of Biology, Ethology research group, 2610, Antwerp, Belgium.

Recent literature has revealed the importance of variation in neuropeptide receptor gene sequences in the regulation of behavioral phenotypic variation. Here we focus on polymorphisms in the oxytocin receptor gene (OXTR) and vasopressin receptor gene 1a (Avpr1a) in chimpanzees and bonobos. In humans, a single nucleotide polymorphism (SNP) in the third intron of OXTR (rs53576 SNP (A/G)) is linked with social behavior, with the risk allele (A) carriers showing reduced levels of empathy and prosociality. Bonobos and chimpanzees differ in these same traits, therefore we hypothesized that these differences might be reflected in variation at the rs53576 position. We sequenced a 320 bp region surrounding rs53576 but found no indications of this SNP in the genus Pan. However, we identified previously unreported SNP variation in the chimpanzee OXTR sequence that differs from both humans and bonobos. Humans and bonobos have previously been shown to have a more similar 5' promoter region of Avpr1a when compared to chimpanzees, who are polymorphic for the deletion of ∼ 360 bp in this region (+/- DupB) which includes a microsatellite (RS3). RS3 has been linked with variation in levels of social bonding, potentially explaining part of the interspecies behavioral differences found in bonobos, chimpanzees and humans. To date, results for bonobos have been based on small sample sizes. Our results confirmed that there is no DupB deletion in bonobos with a sample size comprising approximately 90% of the captive founder population, whereas in chimpanzees the deletion of DupB had the highest frequency. Because of the higher frequency of DupB alleles in our bonobo population, we suggest that the presence of this microsatellite may partly reflect documented differences in levels of sociability found in bonobos and chimpanzees.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0113364PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4236177PMC
January 2016

Testing the effect of medical positive reinforcement training on salivary cortisol levels in bonobos and orangutans.

PLoS One 2014 24;9(9):e108664. Epub 2014 Sep 24.

Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

The management of captive animals has been improved by the establishment of positive reinforcement training as a tool to facilitate interactions between caretakers and animals. In great apes, positive reinforcement training has also been used to train individuals to participate in simple medical procedures to monitor physical health. One aim of positive reinforcement training is to establish a relaxed atmosphere for situations that, without training, might be very stressful. This is especially true for simple medical procedures that can require animals to engage in behaviours that are unusual or use unfamiliar medical devices that can be upsetting. Therefore, one cannot exclude the possibility that the training itself is a source of stress. In this study, we explored the effects of medical positive reinforcement training on salivary cortisol in two groups of captive ape species, orangutans and bonobos, which were familiar to this procedure. Furthermore, we successfully biologically validated the salivary cortisol assay, which had already been validated for bonobos, for orangutans. For the biological validation, we found that cortisol levels in orangutan saliva collected during baseline conditions were lower than in samples collected during three periods that were potentially stressful for the animals. However, we did not find significant changes in salivary cortisol during medical positive reinforcement training for either bonobos or orangutans. Therefore, for bonobos and orangutans with previous exposure to medical PRT, the procedure is not stressful. Thus, medical PRT provides a helpful tool for the captive management of the two species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0108664PLOS
December 2015

Age-related changes in thyroid hormone levels of bonobos and chimpanzees indicate heterochrony in development.

J Hum Evol 2014 Jan 22;66:83-8. Epub 2013 Nov 22.

Max Planck Institute for Evolutionary Anthropology, Department of Primatology, Deutscher Platz 6, D-04103 Leipzig, Germany.

We present information on age related changes of thyroid hormone levels in bonobos (N = 96) and chimpanzees (N = 100) ranging between one and 56 years of age. Fresh urine samples were used for hormone measurements with a commercial competitive total triiodothyronine (T3) ELISA. In both species, immature individuals had higher TT3 levels than adults and there was a marked decrease in TT3 levels between age classes. The two species differed in terms of the timing of TT3 level changes, with chimpanzees experiencing a significant decline in TT3 levels after 10 years of age and bonobos after 20 years of age. The decline of TT3 in chimpanzees appears to coincide with the time when somatic growth terminates while TT3 values in bonobos decrease much later. This temporal asymmetry in urinary thyroid hormone levels indicates heterochrony in the ontogenetic changes of the two sister species and developmental delay in bonobos. The prolongation of high TT3 levels in bonobos, which is characteristic of immatures of both Pan species may affect the behavior of bonobos; namely, the low intensity of aggression they display. Given that developmental studies are often based on post-mortem analyses of skeletons, measures of urinary thyroid hormones offer a non-invasive tool for exploring ontogenetic changes in living wild and captive hominoids.
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http://dx.doi.org/10.1016/j.jhevol.2013.09.008DOI Listing
January 2014

Group size of a permanent large group of agile mangabeys (Cercocebus agilis) at Bai Hokou, Central African Republic.

Folia Primatol (Basel) 2013 20;84(2):67-73. Epub 2013 Mar 20.

Behavioural Biology Unit, University of Liège, Liège, Belgium.

White-eyelid mangabeys (genus Cercocebus) live in groups of highly variable size. Because of their semi-terrestrial behaviour and preference for dense forest habitats, re-liable data on group size are scarce. During a 5-month study, we collected 17 group counts on a habituated group of agile mangabeys (C. agilis) at Bai Hokou in the Central African Republic. We found a stable group size of approximately 135 individuals. This permanent large grouping pattern is known to occur among several populations of white-eyelid mangabeys and is congruent with extreme group sizes reported in mandrills at Lopé in Gabon.
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http://dx.doi.org/10.1159/000346964DOI Listing
January 2014

Adrenarche in bonobos (Pan paniscus): evidence from ontogenetic changes in urinary dehydroepiandrosterone-sulfate levels.

J Endocrinol 2012 Jul 4;214(1):55-65. Epub 2012 May 4.

Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany.

Adrenarche is characterized by the onset of adrenal secretions of increasing amounts of dehydroepiandrosterone-sulfate (DHEA-S). While the function of adrenarche remains a matter of speculation, evidence suggests that the morphological and physiological changes related to it are restricted to humans and closely related primates. Within the primate order, adrenarche has been described only in humans and chimpanzees, but bonobos, the sister species of chimpanzees, have not yet been studied regarding the early ontogenetic changes such as adrenarche. While bonobos and chimpanzees share many morphological and behavioral characteristics, they differ in a number of behavioral traits, and there is a growing interest in terms of the physiological differences that can be linked to species-specific patterns of social behavior. In this study, we measured urinary DHEA-S levels to determine whether bonobos experience physiological changes that are indicative of adrenarche. We measured DHEA-S in urine using ELISA and analyzed its levels in the samples from 53 bonobos aged 1-18 years. Our results show that bonobos experience an increase in DHEA-S levels after 5 years of age, which is comparable with the patterns observed in humans and chimpanzees. This indicates that bonobos do undergo adrenarche and that the timing of onset is similar to that of the two Pan species. The extraction procedures described in this report demonstrate the use of urine for monitoring ontogenetic changes in DHEA-S excretion. If applicable to other species, the technique would facilitate more research on the evolutionary origin of adrenarche and other developmental processes.
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http://dx.doi.org/10.1530/JOE-12-0103DOI Listing
July 2012

Tolerant food sharing and reciprocity is precluded by despotism among bonobos but not chimpanzees.

Am J Phys Anthropol 2010 Sep;143(1):41-51

Anthropological Institute and Museum, University of Zurich, Winterthurerstr. 190, Zürich 8057, Switzerland.

Tolerant food sharing among human foragers can largely be explained by reciprocity. In contrast, food sharing among chimpanzees and bonobos may not always reflect reciprocity, which could be explained by different dominance styles: in egalitarian societies reciprocity is expressed freely, while in more despotic groups dominants may hinder reciprocity. We tested the degree of reciprocity and the influence of dominance on food sharing among chimpanzees and bonobos in two captive groups. First, we found that chimpanzees shared more frequently, more tolerantly, and more actively than bonobos. Second, among chimpanzees, food received was the best predictor of food shared, indicating reciprocal exchange, whereas among bonobos transfers were mostly unidirectional. Third, chimpanzees had a shallower and less linear dominance hierarchy, indicating that they were less despotic than bonobos. This suggests that the tolerant and reciprocal sharing found in chimpanzees, but not bonobos, was made possible by the absence of despotism. To investigate this further, we tested the relationship between despotism and reciprocity in grooming using data from an additional five groups and five different study periods on the main groups. The results showed that i) all chimpanzee groups were less despotic and groomed more reciprocally than bonobo groups, and ii) there was a general negative correlation between despotism and grooming reciprocity across species. This indicates that an egalitarian hierarchy may be more common in chimpanzees, at least in captivity, thus fostering reciprocal exchange. We conclude that a shallow dominance hierarchy was a necessary precondition for the evolution of human-like reciprocal food sharing.
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http://dx.doi.org/10.1002/ajpa.21288DOI Listing
September 2010

Social structures in Pan paniscus: testing the female bonding hypothesis.

Primates 2006 Jul 28;47(3):210-7. Epub 2006 Feb 28.

Department of Biology, University of Antwerp, Universiteitsplein 1, 2610, Wilrijk, Belgium.

Based on previous research in captivity, bonobos, Pan paniscus, have been called a female-bonded species. However, genetic and behavioural data indicate that wild females migrate. Bonding between these unrelated females would then be in contradiction with socio-ecological models. It has been argued that female bonding has been overemphasized in captive bonobos. We examine patterns of proximity, grooming and support behaviour in six well established captive groups of bonobos. We find that female bonding was not a typical characteristic of all captive bonobo groups. In only two groups there was a trend for females to prefer proximity with other females over association with males. We found no evidence that following or grooming between females was more frequent than between males and unrelated females or between males. Only in coalitions, females supported each other more than male-female or male-male dyads. We also investigated five mother-son pairs. Grooming was more frequent among mothers and sons than in any other dyad, but sons did not groom their mothers more than males groomed unrelated females. Mothers groomed their sons, or provided more support to them than females groomed or supported unrelated males. Thus, while bonds between females were clearly present, intersexual relations between males and either unrelated females or their mothers are of more, or equal importance.
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http://dx.doi.org/10.1007/s10329-005-0177-1DOI Listing
July 2006

Peering is not a formal indicator of subordination in bonobos (Pan paniscus).

Am J Primatol 2005 Mar;65(3):255-67

Department of Biology, University of Antwerp, Wilrijk, Belgium.

It has been suggested that peering behavior in bonobos is a formal signal acknowledging social dominance status. We investigated whether peering meets the published criteria for a formal signal of subordination in five captive groups of bonobos. The degree of linearity in the set of peering relationships was significantly high in all study groups, and a linear rank order was found. However, unidirectionality was low, and there was little correspondence between the peering order and the agonistic dominance rank. Therefore, peering does not satisfy the criteria of a formal subordination indicator. We also studied the relation between peering and agonistic dominance rank, age, and sex. Animals directed peering significantly more often at high-ranking animals in four of the groups. We suggest that peering is indirectly related to dominance rank by the resource-holding potential of individuals. In contexts where dominant individuals can monopolize resources, peerers may direct their attention at those high-ranking animals. When resources are distributed more evenly, high-ranking animals may peer down the hierarchy. We speculate on the reasons why a formal dominance or subordination signal appears to be absent in bonobos.
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http://dx.doi.org/10.1002/ajp.20113DOI Listing
March 2005
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