Active self-treatment of a facial wound with a biologically active plant by a male Sumatran orangutan.

Although self-medication in non-human animals is often difficult to document systematically due to the difficulty of predicting its occurrence, there is widespread evidence of such behaviors as whole leaf swallowing, bitter pith chewing, and fur rubbing in African great apes, orangutans, white handed gibbons, and several other species of monkeys in Africa, Central and South America and Madagascar. To the best of our knowledge, there is only one report of active wound treatment in non-human animals, namely in chimpanzees. We observed a male Sumatran orangutan (Pongo abelii) who sustained a facial wound. Three days after the injury he selectively ripped off leaves of a liana with the common name Akar Kuning (Fibraurea tinctoria), chewed on them, and then repeatedly applied the resulting juice onto the facial wound. As a last step, he fully covered the wound with the chewed leaves. Found in tropical forests of Southeast Asia, this and related liana species are known for their analgesic, antipyretic, and diuretic effects and are used in traditional medicine to treat various diseases, such as dysentery, diabetes, and malaria. Previous analyses of plant chemical compounds show the presence of furanoditerpenoids and protoberberine alkaloids, which are known to have antibacterial, anti-inflammatory, anti-fungal, antioxidant, and other biological activities of relevance to wound healing. This possibly innovative behavior presents the first systematically documented case of active wound treatment with a plant species know to contain biologically active substances by a wild animal and provides new insights into the origins of human wound care.

Orangutan males make increased use of social learning opportunities, when resource availability is high.

Humans' colonization of diverse habitats relied on our ancestors' abilities to innovate and share innovations with others. While ecological impacts on innovations are well studied, their effect on social learning remains poorly understood. We examined how food availability affects social learning in migrant orangutan unflanged males, who may learn from local orangutans through peering (i.e., observational social learning). We analyzed 1,384 dyadic associations, including 360 peering events, among 46 wild Sumatran orangutan and 25 Bornean orangutan males, collected over 18 years. Migrants' peering rates significantly increased with higher food availability and time spent in proximity to others. Furthermore, migrants in the more sociable Sumatran population exhibited significantly higher peering rates compared to the Borneans, suggesting intrinsic and/or developmental effects of food availability on social learning. These findings emphasize the importance of investigating ecological effects on social learning on the immediate, developmental, and intrinsic levels for our understanding of cultural evolution.

Does the expensive brain hypothesis apply to amphibians and reptiles?

Vertebrate brains show extensive variation in relative size. The expensive brain hypothesis argues that one important source of this variation is linked to a species' ability to generate the energy required to sustain the brain, especially during periods of unavoidable food scarcity. Here we ask whether this hypothesis, tested so far in endothermic vertebrates, also applies to ectotherms, where ambient temperature is an additional major aspect of energy balance. Phylogenetic comparative analyses of reptiles and amphibians support the hypothesis. First, relative brain size increases with higher body temperature in those species active during the day that can gain free energy by basking. Second, relative brain size is smaller among nocturnal species, which generally face less favorable energy budgets, especially when maintaining high body temperature. However, we do not find an effect of seasonal variation in ambient temperature or food on brain size, unlike in endotherms. We conclude that the factors affecting energy balance in ectotherms and endotherms are overlapping but not identical. We therefore discuss the idea that when body temperatures are seasonally very low, cognitive benefits may be thwarted and selection on larger brain size may be rare. Indeed, mammalian hibernators may show similarities to ectotherms.

Ecological, social, and intrinsic factors affecting wild orangutans' curiosity, assessed using a field experiment.

The readiness to interact with and explore novel stimuli-i.e., curiosity-is the cornerstone of innovation. Great apes show broad and complex innovation repertoires. However, little is known about the factors that affect curiosity in wild apes. To shed light on wild apes' curiosity, we measured the reactions of wild Sumatran orangutans (Pongo abelii) to an experiment apparatus. Overall, individuals were reluctant to touch the apparatus. However, compared to adults, immatures showed higher tendencies to explore (measured through looking durations and the probability of touching the apparatus) and to approach (measured through approach latencies and approach distances) the apparatus but were more likely to show behavioral signs of agitation. The presence of conspecifics who approached the apparatus increased visual exploration and approach tendencies. Prevailing habitat food availability positively affected visual exploration but had a negative effect on approach tendencies. These findings indicate that intrinsic, social, and ecological factors affect reactions to novelty in wild orangutans and suggest that exploration, neophobia and neophilia are independently regulated. Because reactions to novelty can be an essential pathway to innovation, our results suggest that factors acting on different elements of curiosity must be considered to understand the evolution of innovative tendencies.

Alternative reproductive tactics of unflanged and flanged male orangutans revisited.

In many slowly developing mammal species, males reach sexual maturity well before they develop secondary sexual characteristics. Sexually mature male orangutans have exceptionally long periods of developmental arrest. The two male morphs have been associated with behavioral alternative reproductive tactics, but this interpretation is based on cross-sectional analyses predominantly of Northwest Sumatran populations. Here we present the first longitudinal analyses of behavioral changes of 10 adult males that have been observed in both unflanged and flanged morph. We also analyzed long-term behavioral data on an additional 143 individually identified males from two study sites, Suaq (Sumatra, Pongo abelii) and Tuanan (Borneo, Pongo pygmaeus wurmbii), to assess male mating tactics cross-sectionally in relation to population, male morph (unflanged and flanged), and other socio-ecological factors. Both our longitudinal and cross-sectional results confirm and refine previous cross-sectional accounts of the differences in mating tactics between the unflanged and the flanged male morphs. In the unflanged morph, males exhibit higher sociability, particularly with females, and higher rates of both copulation and sexual coercion than in the flanged morph. Based on our results and those of previous studies showing that females prefer flanged males, and that flanged males have higher reproductive success, we conclude that unflanged males face a trade-off between avoiding male-male contest competition and gaining mating access to females, and thus follow a "best-of-a-bad-job" mating strategy.

Extended parental provisioning and variation in vertebrate brain sizes.

Large brains provide adaptive cognitive benefits but require unusually high, near-constant energy inputs and become fully functional well after their growth is completed. Consequently, young of most larger-brained endotherms should not be able to independently support the growth and development of their own brains. This paradox is solved if the evolution of extended parental provisioning facilitated brain size evolution. Comparative studies indeed show that extended parental provisioning coevolved with brain size and that it may improve immature survival. The major role of extended parental provisioning supports the idea that the ability to sustain the costs of brains limited brain size evolution.

The economics of brain size evolution in vertebrates.

Across the animal kingdom, we see remarkable variation in brain size. This variation has even increased over evolutionary time. Traditionally, studies aiming to explain brain size evolution have looked at the fitness benefits of increased brain size in relation to its increased cognitive performance in the social and/or ecological domain. However, brains are among the most energetically expensive tissues in the body and also require an uninterrupted energy supply. If not compensated, these energetic demands inevitably lead to a reduction in energy allocation to other vital functions. In this review, we summarize how an increasing number of studies show that to fully comprehend brain size evolution and the large variation in brain size across lineages, it is important to look at the economics of brains, including the different pathways through which the high energetic costs of brains can be offset. We further show how numerous studies converge on the conclusion that cognitive abilities can only drive brain size evolution in vertebrate lineages where they result in an improved energy balance through favourable ecological preconditions. Cognitive benefits that do not directly improve the organism's energy balance can only be selectively favoured when they produce such large improvements in reproduction or survival that they outweigh the negative energetic effects of the large brain.

Orangutan mothers adjust their behaviour during food solicitations in a way that likely facilitates feeding skill acquisition in their offspring.

Immature orangutans acquire their feeding skills over several years, via social and independent learning. So far, it has remained uninvestigated to what extent orangutan mothers are actively involved in this learning process. From a fitness point of view, it may be adaptive for mothers to facilitate their offspring's skill acquisition to make them reach nutritional independence faster. Food solicitations are potential means to social learning which, because of their interactive nature, allow to investigate the degree of active involvement of the mother. To investigate the role of food solicitation and the role of the mother in immatures' foraging skill acquisition, we analysed 1390 food solicitation events between 21 immature Sumatran orangutans (Pongo abelii) and their mothers, collected over 13 years at the Suaq Balimbing orangutan population. We found that solicitation rates decreased with increasing age of the immatures and increased with increasing processing complexity of the food item. Mothers were more likely to share complex items and showed the highest likelihoods of sharing around the age at which immatures are learning most of their feeding skills. Our results indicate that immature Sumatran orangutans use food solicitation to acquire feeding skills. Furthermore, mothers flexibly adjust their behaviour in a way that likely facilitates their offspring's skill acquisition. We conclude that orangutan mothers have a more active role in the skill acquisition of their offspring than previously thought.

The development and maintenance of sex differences in dietary breadth and complexity in Bornean orangutans.

ABSTRACT: Orangutans show a pronounced sexual dimorphism, with flanged males (i.e., males with fully grown secondary sexual characteristics) reaching twice the size of adult females. Furthermore, adult orangutans show sex-specific dispersal and activity patterns. This study investigates sex differences in adult foraging behavior and sheds light on how these differences develop in immatures. We analyzed 11 years of feeding data on ten adult female, seven flanged male, and 14 immature Bornean orangutans (Pongo pygmaeus wurmbii) at Tuanan in Central Kalimantan, Indonesia. We found that the diets of the adult females were significantly broader and required more processing steps before ingestion than the diets of flanged males. We also found evidence for a similar difference in overall diet repertoire sizes. For the immatures, we found that whereas females reached 100% of their mothers' diet spectrum size by the age of weaning, males reached only around 80%. From the age of 4 years on (i.e., years before being weaned) females had significantly broader daily diets than males. We found no difference in daily or overall diet processing intensity of immature males and females but found preliminary evidence that immature males included fewer items of their mother's diet in their own diets that were processing-intensive. Overall, our results suggest that by eating a broader variety and more complex to process food items, female orangutans go to greater lengths to achieve a balanced diet than males do. These behavioral differences are not just apparent in adult foraging behavior but also reflected in immature development from an early age on. SIGNIFICANCE STATEMENT: In many species, males and females have different nutritional needs and are thus expected to show sex-specific foraging behavior. Sex differences in several aspects of foraging behavior have been found in various species, but it remains largely unclear when and how those develop during ontogeny, which is especially relevant for long-lived altricial species that learn foraging skills over many years. In our study, we analyzed a cross-sectional and longitudinal data set containing more than 750,000 feeding events of adult and immature Bornean orangutans (Pongo pygmaeus wurmbii). We found that adult females had significantly broader and more complex diets than males. We also found that these differences started to develop during infancy, suggesting that immature orangutans prepare for their sex-specific foraging niches long before those become physiologically relevant while they are still in constant association with their mothers and before being frequently exposed to other role models. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00265-021-03014-3.

Orangutans have larger gestural repertoires in captivity than in the wild-A case of weak innovation?

Whether nonhuman species can change their communicative repertoire in response to socio-ecological environments has critical implications for communicative innovativeness prior to the emergence of human language, with its unparalleled productivity. Here, we use a comparative sample of wild and zoo-housed orangutans of two species (Pongo abelii, Pongo pygmaeus) to assess the effect of the wild-captive contrast on repertoires of gestures and facial expressions. We find that repertoires on both the individual and population levels are larger in captive than in wild settings, regardless of species, age class, or sampling effort. In the more sociable Sumatran species, dominant use of signals toward single outcomes was also higher in captive settings. We thus conclude that orangutans exposed to more sociable and terrestrial conditions evince behavioral plasticity, in that they produce additional innate or innovated signals that are highly functionally specific. These findings suggest a latent capacity for innovativeness in these apes' communicative repertoires.

Immature wild orangutans acquire relevant ecological knowledge through sex-specific attentional biases during social learning.

As a part of growing up, immature orangutans must acquire vast repertoires of skills and knowledge, a process that takes several years of observational social learning and subsequent practice. Adult female and male orangutans show behavioral differences including sex-specific foraging patterns and male-biased dispersal. We investigated how these differing life trajectories affect social interest and emerging ecological knowledge in immatures. We analyzed 15 years of detailed observational data on social learning, associations, and diet repertoires of 50 immatures (16 females and 34 males), from 2 orangutan populations. Specific to the feeding context, we found sex differences in the development of social interest: Throughout the dependency period, immature females direct most of their social attention at their mothers, whereas immature males show an increasing attentional preference for individuals other than their mothers. When attending to non-mother individuals, males show a significant bias toward immigrant individuals and a trend for a bias toward adult males. In contrast, females preferentially attend to neighboring residents. Accordingly, by the end of the dependency period, immature females show a larger dietary overlap with their mothers than do immature males. These results suggest that immature orangutans show attentional biases through which they learn from individuals with the most relevant ecological knowledge. Diversifying their skills and knowledge likely helps males when they move to a new area. In sum, our findings underline the importance of fine-grained social inputs for the acquisition of ecological knowledge and skills in orangutans and likely in other apes as well.

The ontogeny of exploratory object manipulation behaviour in wild orangutans.

In human infants, exploratory object manipulation is a major vehicle for cognitive stimulation as well as an important way to learn about objects and basic physical concepts in general. The development of human infants' exploratory object manipulation follows distinct developmental patterns. So far, the degree of evolutionary continuity of this developmental process remains unclear. We investigated the development of exploratory object manipulations in wild orangutans. Our data included 3200 exploration events collected on 13 immatures between the ages of 0.5 and 13 years, at the Suaq Balimbing monitoring station in Indonesia. Our results identify several parallels between the development of exploratory behaviour in humans and orangutans: on top of a highly similar overall age trajectory, we found an increase in variability of the actions used, an increase in the number of body parts involved in each event, and an overall decrease of mouthing of the objects. All in all, our results show that orangutans progress through a developmental sequence of different aspects of exploration behaviour. In combination with previous findings from captivity, our results also provide evidence that exploratory object manipulations reflect cognitive development and might function as a means of cognitive stimulation not just in humans but across the great apes.

When ontogeny recapitulates phylogeny: Fixed neurodevelopmental sequence of manipulative skills among primates.

Neural development is highly conserved across distantly related species of different brain sizes. Here, we show that the development of manipulative complexity is equally cumulative across 36 primate species and also that its ontogeny recapitulates phylogeny. Furthermore, larger-brained species reach their adult skill levels later than smaller-brained ones, largely because they start later with the simplest techniques. These findings demonstrate that these motor behaviors are not modular and that their slow development may constrain their evolution. Complex foraging techniques therefore critically require a slow life history with low mortality, which explains the limited taxonomic distribution of flexible tool use and the unique elaboration of human technology.

Early sociability fosters later exploratory tendency in wild immature orangutans.

Exploration is essential for skill acquisition and strongly facilitates cognitive performance. In humans, it is widely known that exploration and later cognitive performance are highly dependent on early social inputs. Here, we aim to shed light on the evolutionary roots of this process by studying the effects of variation in opportunities for social learning on the exploratory tendency of immature orangutans (Pongo spp.) in nature. We based our analyses on mixed cross-sectional, longitudinal data of exploration by immatures and their mothers. Current exploration rates were correlated with levels of past experienced sociability, but not with current food abundance or with maternal condition, and only partly with genetic similarity. We conclude that the dependence of cognitive development on socially triggered exploration, which underlies the construction of cognitive skills such as intelligence, existed before the emergence of the human lineage.

The loud scratch: a newly identified gesture of Sumatran orangutan mothers in the wild.

The communicative function of primates' self-directed behaviours like scratching has gained increasing attention in recent years, but their intentional use is still debated. Here, we addressed this issue by exploring the communicative function of 'loud scratches' in wild Sumatran orangutans. Building on previous studies in chimpanzees, we examined the prediction that audio-visual loud scratches are used communicatively in mother-infant travel coordination. Specifically, we examined whether individual, social and scratch features affected the use of pre-move scratches, markers of intentional signal use and approach responses. We analysed a total of 1457 scratching bouts, produced by 17 individuals (including four mothers and their dependent offspring) observed during 305 h of focal follows. Overall, we found that scratching bouts preceded departure mainly when these were produced by mothers and showed features of exaggeration. If the scratching individual was a mother, associates were more likely to be visually attentive during pre-move scratches than in other contexts. Approach or follow responses to scratches by individuals in association were predicted by context, the relationship with the scratcher (i.e. offspring) and the associate's attentional state. We conclude that orangutan mothers use loud scratches as communicative strategies to coordinate joint travel with their infants.

Animal cultures: how we've only seen the tip of the iceberg.

For humans we implicitly assume that the way we do things is the product of social learning and thus cultural. For animals, this conclusion requires proof. Here, we first review the most commonly used procedure for documenting animal culture: the method of exclusion, which charts geographic behavioral variation between populations as evidence for culture. Using published data, we show that, whereas it is an adequate proof of principle, the method of exclusion has major deficiencies when capturing cultural diversity and complexity. Therefore, we propose a new method, namely the direct counting of socially learned skills, which we apply to previously collected data on wild orangutans. This method reveals a far greater cultural repertoire among orangutans, and a different distribution of cultural elements among behavioral domains than found by the method of exclusion, as well as clear ecological correlates for most cultural elements. The widespread occurrence of social learning ability throughout the animal kingdom suggests that these conclusions also apply to many other species. Culture is most likely more widespread and pervasive than commonly thought and an important avenue to local adaptation. The complex and normative dimensions of culture seem unique to our species, but were most likely built upon a very broad, pre-existing cultural capacity that we inherited from our ancestors.

The slow ape: High infant survival and long interbirth intervals in wild orangutans.

Orangutans (Pongo spp.) are reported to have extremely slow life histories, including the longest average interbirth intervals of all mammals. Such slow life history can be viable only when unavoidable mortality is kept low. Thus, orangutans' survivorship under natural conditions is expected to be extremely high. Previous estimates of orangutan life history were based on captive individuals living under very different circumstances or on small samples from wild populations. Here, we combine birth data from seven field sites, each with demographic data collection for at least 10 years (range 12-43 years) on wild orangutans to better document their life history. Using strict criteria for data inclusion, we calculated infant survival, interbirth intervals and female age at first reproduction, across species, subspecies and islands. We found an average closed interbirth interval of 7.6 years, as well as consistently very high pre-weaning survival for males and females. Female survival of 94% until age at first birth (at around age 15 years) was higher than reported for any other mammal species under natural conditions. Similarly, annual survival among parous females is very high, but longevity remains to be estimated. Current data suggest no major life history differences between Sumatran and Bornean orangutans. The high offspring survival is remarkable, noting that modern human populations seem to have reached the same level of survival only in the 20th century. The orangutans' slow life history illustrates what can be achieved if a hominoid bauplan is exposed to low unavoidable mortality. Their high survival is likely due to their arboreal and non-gregarious lifestyle, and has allowed them to maintain viable populations, despite living in low-productivity habitats. However, their slow life history also implies that orangutans are highly vulnerable to a catastrophic population crash in the face of drastic habitat change.

Correction to: development of foraging skills in two orangutan populations: needing to learn or needing to grow?

[This corrects the article DOI: 10.1186/s12983-016-0178-5.].

Transfusion practice in anemic, non-bleeding patients: Cross-sectional survey of physicians working in general internal medicine teaching hospitals in Switzerland.

BACKGROUND: Transfusion practice might significantly influence patient morbidity and mortality. Between European countries, transfusion practice of red blood cells (RBC) greatly differs. Only sparse data are available on transfusion practice of general internal medicine physicians in Switzerland. METHODS: In this cross-sectional survey, physicians working in general medicine teaching hospitals in Switzerland were investigated regarding their self-reported transfusion practice in anemic patients without acute bleeding. The definition of anemia, transfusion triggers, knowledge on RBC transfusion, and implementation of guidelines were assessed. RESULTS: 560 physicians of 71 hospitals (64%) responded to the survey. Anemia was defined at very diverging hemoglobin values (by 38% at a hemoglobin <130 g/L for men and by 57% at <120 g/L in non-pregnant women). 62% and 43% respectively, did not define anemia in men and in women according to the World Health Organization. Fifty percent reported not to transfuse RBC according to international guidelines. Following factors were indicated to influence the decision to transfuse: educational background of the physicians, geographical region of employment, severity of anemia, and presence of known coronary artery disease. 60% indicated that their knowledge on Transfusion-related Acute Lung Injury (TRALI) did not influence transfusion practice. 50% of physicians stated that no local transfusion guidelines exist and 84% supported the development of national recommendations on transfusion in non-acutely bleeding, anemic patients. CONCLUSION: This study highlights the lack of adherence to current transfusion guidelines in Switzerland. Identifying and subsequently correcting this deficit in knowledge translation may have a significant impact on patient care.

The effects of sociability on exploratory tendency and innovation repertoires in wild Sumatran and Bornean orangutans.

It has been hypothesized that opportunities for social learning affect the size and complexity of the adult skill set of birds and mammals, their learning ability, and thus ultimately also their innovation frequency. To test these predictions we compared rates of social learning, rates of independent exploration (independent learning) and innovation repertoires between individuals of a highly sociable population of Pongo abelii at Suaq Balimbing and a less sociable population of Pongo pygmaeus wurmbii at Tuanan. Suaq immatures showed significantly higher rates of peering, even after controlling for differences in association time and diet complexity, implying that they make disproportionally greater use of their increased opportunities for social learning. As predicted, we found that immatures and adults at Suaq also showed significantly higher rates of exploratory behaviour. The difference between the individuals of the two popuations remained when controlling for association time, suggesting persistent developmental effects, intrinsic differences, or both. Accordingly, Suaq animals had a larger set of learned skills and a higher mean dietary complexity. Our findings show that population level sociability, individual rates of exploration and population-wide repertoires of innovations are positively linked, as predicted.