An evaluation of the geographic method for recognizing innovations in nature,using zoo orangutans

Innovation and social learning are the raw materials for traditions and culture. Of these two, innovation has received far less scrutiny, largely because of difficulties assessing the innovation status of behaviors. A recent attempt proposes recognition of innovations in natural populations based on assessment of the behavior’s properties and its geographic and local prevalence. Here we examine the validity of this approach and the list of 43 potential innovations it generated for wild orangutans by extending the comparison to zoo orangutans. First, we created an inventory of the behavioral repertoire in the zoo population. Four of ten putative innovations recognized in the field and potentially present in captivity did not occur despite appropriate conditions, suggesting they are indeed innovations. Second, we experimentally produced relevant conditions to evaluate whether another five potential innovations could be elicited. Based on their continued absence or on their latencies relative to known behaviors, four of the potential innovations could be assessed as innovations and one as a modification. Because 53% of relevant innovations recognized in the field could be confirmed in this analysis, and another 27% assigned possible innovation status, we conclude that the geographic method for detecting innovation in the wild is valid. However, the experiments also yielded up to 13 additional innovations, suggesting that zoo orangutans are far more innovative than wild ones. We discuss the implications of this latter finding with regard to limiting factors for the expansion of cultural repertoires in wild orangutans.     

Experimental field studies of Asian ape social systems

The Asian apes, orangutans and gibbons, possess unusual social systems among anthropoid primates. Social groups of gibbons consist of mated adult pairs and their offspring; mature orangutans are primarily solitary. Recent experimental field research has begun to yield insights into the behavioral mechanisms employed by these animals to maintain their characteristic patterns of social dispersion. While spatial separation between female orangutans appears to be maintained passively, aggression, which is manifest during direct encounters and long-distance vocal interactions, mediates male asociality. Male-male aggression is the result of intense intrasexual competition occurring between animals for mating access to females. To reduce intrasexual competition, male orangutans have adopted alternative mating tactics. In contrast to female orangutans, female gibbons show marked agonistic tendencies toward conspecifics. Female territoriality contributes to preventing males from becoming polygynous. Male gibbons, restricted to monogamous relationships, attempt to ensure their paternity through intrasexual aggression. These observations suggest that the spatial dispersion of females constrains male mating options in both species. However, variations between orangutan and gibbon social systems can be understood as consequences of the temporal dispersion of sexually receptive females. The temporal clumping of females, due to relatively high operational sex ratios, limits the ability of male gibbons to acquire multiple mates. Conversely, an extremely low operational sex ratio in orangutans creates a strong selection pressure for intrasexual competition and polygamous mating. These considerations provide a novel framework for interpreting the social systems of the African apes.     

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.

To understand the development and evolution of cognition of our closest relatives, we need to investigate their learning behavior during every-day life. This study finds that wild orangutan males and females differ in their social learning strategies and subsequent learning outcomes from an early age, underlining the general importance of, and the effects of sex on, social learning in non-human great apes.     

Grouping behavior of Sumatran orangutans (Pongo abelii) and Tapanuli orangutans (Pongo tapanuliensis) living in forest with low fruit abundance

In contrast to the African great apes, orangutans (Pongo spp.) are semisolitary: Individuals are often on their own, but form aggregations more often than expected by chance. These temporary aggregations provide social benefits such as mating opportunities. When fruit availability is high, costs of aggregating should be lower, because competition is less pronounced. Therefore, average party size is expected to be higher when fruit availability is high. This hypothesis would also explain why orangutans in highly fruit-productive habitats on Sumatra are more gregarious than in the usually less productive habitats of Borneo. Here, we describe the aggregation behavior of orangutans in less productive Sumatran habitats (Sikundur and Batang Toru), and compare results with those of previously surveyed field sites. Orangutans in Sikundur were more likely to form parties when fruit availability was higher, but the size of daily parties was not significantly affected by fruit availability. With regard to between-site comparisons, average party sizes of females and alone time of parous females in Sikundur and Batang Toru were substantially lower than those for two previously surveyed Sumatran sites, and both fall in the range of values for Bornean sites. Our results indicate that the assessment of orangutans on Sumatra as being more social than those on Borneo needs revision. Instead, between-site differences in sociality seem to reflect differences in average fruit availability.     

Implications of body mass and predation for ape social system and biogeographical distribution

Despite the fact that all African great apes have overlapping diets, they differ substantially in both biogeographical distribution and social organisation: Gorilla lives in relatively small, cohesive groups within a small biogeographical area while Pan is much more widely distributed and lives in large, fluid groups in which the members are rarely all together. In this study we use a modelling approach to identify possible causes and consequences of these differences. We use a time budget model which is based on the relationship between time available for various activities, group size, body mass and climate. We demonstrate the importance of body mass as a critical determinant for maximum ecologically tolerable group size as well as ape distribution patterns. In addition, we show that predation pressure may play a strong role in limiting the distribution of smaller-bodied apes ( Pan ). Predation pressure appears to be especially important if the apes opt for a fission–fusion strategy because it obliges them to maintain larger (sub-) groups. In effect, the apes appear to face a tradeoff between solving the predation problem by increasing body size (at the expense of reduced ecological flexibility) and going for ecological flexibility (but at some cost in terms of how they handle predation).     

Demographic history and genetic differentiation in apes

Comparisons of genetic variation between humans and great apes are hampered by the fact that we still know little about the demographics and evolutionary history of the latter species. In addition, characterizing ape genetic variation is important because they are threatened with extinction, and knowledge about genetic differentiation among groups may guide conservation efforts. We sequenced multiple intergenic autosomal regions totaling 22,400 base pairs (bp) in ten individuals each from western, central, and eastern chimpanzee groups and in nine bonobos, and 16,000 bp in ten Bornean and six Sumatran orangutans. These regions are analyzed together with homologous information from three human populations and gorillas. We find that whereas orangutans have the highest diversity, western chimpanzees have the lowest, and that the demographic histories of most groups differ drastically. Special attention should therefore be paid to sampling strategies and the statistics chosen when comparing levels of variation within and among groups. Finally, we find that the extent of genetic differentiation among "subspecies" of chimpanzees and orangutans is comparable to that seen among human populations, calling the validity of the "subspecies" concept in apes into question.     

Does Sympathy Motivate Prosocial Behaviour in Great Apes?

Prosocial behaviours such as helping, comforting, or sharing are central to human social life. Because they emerge early in ontogeny, it has been proposed that humans are prosocial by nature and that from early on empathy and sympathy motivate such behaviours. The emerging question is whether humans share these abilities to feel with and for someone with our closest relatives, the great apes. Although several studies demonstrated that great apes help others, little is known about their underlying motivations. This study addresses this issue and investigates whether four species of great apes (Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, Pan paniscus) help a conspecific more after observing the conspecific being harmed (a human experimenter steals the conspecific’s food) compared to a condition where no harming occurred. Results showed that in regard to the occurrence of prosocial behaviours, only orangutans, but not the African great apes, help others when help is needed, contrasting prior findings on chimpanzees. However, with the exception of one population of orangutans that helped significantly more after a conspecific was harmed than when no harm occurred, prosocial behaviour in great apes was not motivated by concern for others.     

Knuckle-walking and the evolution of hominoid hands

Knuckle-walking is a pattern of digitigrade locomotion unique to African apes among Primates. Only chimpanzees and gorillas are specially adapted for supporting weight on the dorsal aspects of middle phalanges of flexed hand digits II–V. When forced to the ground, most orangutans assume one of a variety of flexed hand postures, but they cannot knuckle-walk. Some orangutans place their hands in palmigrade postures which are impossible to African apes. The knuckle-walking hands and plantigrade feet of African apes are both morphologically and adaptively distinct from those of Pongo, their nearest relative among extant apes. These features are associated with a common adaptive shift to terrestrial locomotion and support placing chimpanzees and gorillas in the same genus Pan. It is further suggested than Pan comprises the subgenera (a) Pan, including P. troglodytes and pygmy chimpanzees, and (b) Gorilla, including mountain and lowland populations of P. gorilla. African apes probably diverged from ancestral pongids that were specially adapted for distributing their weight in terminal branches of the forest canopy. Early adjustments to terrestrial locomotion may have involved fist-walking which later evolved into knuckle-walking. Orangutans continued to adapt to feeding and locomotion in the forest canopy and their hands and feet became highly specialized for four-digit prehension. Although chimpanzees retained arboreal feeding and nesting habits, they moved from tree to tree by terrestrial routes and became less restricted in habitat. While adapting to a diet of ground plants gorillas increased in size to the point that arboreal nesting is less frequent among them than among chimpanzees and orangutans. Early hominids probably diverged from pongids that had not developed prospective adaptations to knuckle-walking, and therefore did not evolve through a knuckle-walking stage. Initial adjustments to terrestrial quadrupedal locomotion and resting stance probably included palmigrade hand posturing. Their thumbs may have been already well developed as an adaptation for grasping during arboreal climbing. A combination of selection pressures for efficient terrestrial locomotor support and for object manipulation further advanced early hominid hands toward modern human configuration.     

The nature and evolution of intelligence in orangutans (Pongo pygmaeus)

Orangutans share many intellectual qualities with African great apes and humans, likely because of their recent common ancestry. They may also show unique intellectual adaptations because of their long evolutionary divergence from the African lineage. This paper assesses orangutan intelligence in light of this evolutionary history. Evidence derives from observations of juvenile ex-captive orangutans reintroduced to free forest life by the Wanariset Orangutan Reintroduction Project, East Kalimantan, Indonesia. The intellectual qualities shared by great apes and humans point to a distinct “great ape” intelligence with hierarchization as a pivotal cognitive mechanism. Evolutionary reconstructions jibe with this view and suggest that technically difficult foods may have been key selection pressures. Orangutans should then show hierarchical intelligence when obtaining difficult foods. Evidence on ex-captive orangutans' techniques for processing difficult foods concurs. Intellectual qualities distinct to orangutans may owe to arboreal travel pressures; in particular arboreality may aggravate foraging problems. Evidence confirms that ex-captive orangutans' techniques for accessing difficult foods located arboreally are intellectually complex—i.e. they show hierarchization. These findings suggest other factors probably important to understanding great ape and orangutan forms of intelligence and their evolutionary origins.     

Variation in perikymata counts between repetitive episodes of linear enamel hypoplasia among orangutans from Sumatra and Borneo

The goal of this study is to evaluate whether repetitive linear enamel hypoplasia (rLEH) in apes is ecologically informative. LEH, which appears as grooves of thinner enamel often caused by malnutrition and/or disease, is a permanent record of departures from developmental homeostasis in infant and juvenile apes. Orangutans were selected for the study as they are a threatened species, have a remarkably high prevalence of rLEH, and because Sumatra is deemed a better habitat for orangutans than is Borneo, facilitating an ecological comparison. Objectives are to determine: a) whether periodicity of rLEH in orangutans corresponds to monsoon‐mediated cycles in precipitation or food; and b) whether patterning of rLEH supports the view that Borneo is an inferior habitat. This study compares the counts of perikymata between adjacent LEH from 9 Sumatran and 26 Bornean orangutans to estimate the periodicity of rLEH. A total of 131 nonredundant inter‐LEH perikymata counts were transformed to natural log values to reveal clusters of counts in a multiplicative series. Using a value of 10 days to form one perikyma, rLEH tends to recur semiannually in both populations. However, Sumatran orangutans show significantly fewer semiannual intervals and more annually recurring episodes. Bornean orangutans show mostly semiannual intervals and are more variable in inter‐LEH perikymata counts. It is concluded that: a) developmental conditions for infant orangutans in Sumatra protect them somewhat from seasonal and environmental variation; b) temporal patterning of rLEH indicates that Borneo is the poorer habitat for orangutans; and c) the study of rLEH can be ecologically informative. Am J Phys Anthropol 154:125–139, 2014. © 2014 Wiley Periodicals, Inc.     

Genetic sex identification in orangutans

To date, no established protocol for genetic sex identification in orangutans (Pongo pygmaeus) exists. In nearly all apes (gibbons, gorillas, chimpanzees, and humans), genetic sex identification is possible using the amelogenin gene because copies located on X and Y chromosomes have different sizes. Here we report that orangutan sex identification can be resolved through multiplex polymerase chain reaction (PCR) of the Y-linked SRY locus and the amelogenin locus. PCR amplifications of orangutan amelogenin produces one fragment size in both sexes, while SRY amplifies only in males. This protocol will allow primatologists to identify the sex of orangutans through genetic analysis.     

A Comparison of Female Mating Strategies in <Emphasis Type="Italic">Pan troglodytes</Emphasis> and <Emphasis Type="Italic">Pongo</Emphasis> spp.

Orangutans and chimpanzees differ in many aspects of their mating and social systems. Nevertheless, because both great apes require enormous maternal investment in offspring and because female reproductive potential is limited, female orangutans and chimpanzees should be selective of their mates, yet expected to exhibit anti-infanticide strategies such as mating with multiple males. We review and compare mating patterns in orangutans and chimpanzees to understand how these critical pressures are filtered through the different demands of the socioecology of each species. We highlight the variation in female mating behavior as a function of the proximity of ovulation. We conclude that both genera pursue tactics for paternity confusion by mating with multiple males and by mating cooperatively or even proceptively with nonpreferred partners when conception is unlikely. Mating selectivity is suggested by variation in proceptive behavior toward particular partners and by increased resistance of nonpreferred partners during the periovulatory period. Thus, data for both species support a mixed mating strategy whereby females shift their mating behavior in accordance with ovulatory status to accommodate the competing demands of mate selectivity and paternity confusion.     

Food Neophobia and Social Learning Opportunities in Great Apes

Finding food resources and maintaining a balanced diet are major concerns for all animals. A compromise between neophobia and neophilia is hypothesised to enable animals to enlarge their diet while limiting the risk of poisoning. However, little is known about how primates respond to novel food items and whether their use is socially transmitted. By comparing how four different species of great apes respond to novel food items, we investigated how differences in physiology (digestive tract size and microbial content), habitats (predictability of food availability), and social systems (group size and composition) affect their response toward novelty. We presented two familiar foods, one novel fruit, four novel aromatic plants from herbal medicine, and kaolin to captive chimpanzees (Pan troglodytes), western gorillas (Gorilla gorilla), Bornean orangutans (Pongo pygmaeus) and Sumatran orangutans (Pongo abelii). We recorded smelling, approach-taste delays, ingestion, interindividual observations, and food transfers with continuous sampling. We found that behaviors differed between the apes: chimpanzees were the most cautious species and observed their conspecifics handling the items more frequently than the other apes. Close observations and food transfers were extremely rare in gorillas in comparison to orangutans and chimpanzees. We suggest that a low neophobia level reflects an adaptive response to digestive physiological features in gorillas and to unpredictable food availability in orangutans. Social interactions appeared to be predominant in chimpanzees and in both orangutan species to overcome food neophobia. They reflect higher social tolerance and more opportunities for social learning and cultural transmission in a feeding context.     

Evidence of leopard predation on bonobos (Pan paniscus)

Current models of social organization assume that predation is one of the major forces that promotes group living in diurnal primates. As large body size renders some protection against predators, gregariousness of great apes and other large primate species is usually related to other parameters. The low frequency of observed cases of nonhuman predation on great apes seems to support this assumption. However, recent efforts to study potential predator species have increasingly accumulated direct and indirect evidence of predation by leopards (Panthera pardus) on chimpanzees and gorillas. The following report provides the first evidence of predation by a leopard on bonobos (Pan paniscus).     

Adaptable individuals and innovative lineages

This paper suggests (i) that while work on animal innovation has made good progress in understanding some of the proximate mechanisms and selective regimes through which innovation emerges, it has somewhat neglected the role of the social environment of innovation; a neglect manifest in the fact that innovation counts are almost always counts of resource-acquisition innovations; the invention of social tools is rarely considered. The same is true of many experimental projects, as these typically impose food acquisition tasks on their experimental subjects. (ii) That neglect is important, because innovations often pose collective action problems; the hominin species were technically innovative because they were also socially adaptable. (iii) In part for this reason, there remains a disconnect between research on hominin innovation and research on animal innovation. (iv) Finally, the paper suggests that there is something of a disconnect between the theoretical work on innovation in hominin evolution (based on theories of cultural evolution) and the experimental tradition on human innovation. That disconnect is largely due to the theoretical work retreating from strong claims about the proximate mechanisms of human cultural accumulation.     

Self-awareness and the emergence of mind in primates

To date humans, chimpanzees, and orangutans are the only species which have been shown capable of recognizing themselves in mirrors. Several species of macaques have now been provided with years of continuous exposure to mirrors, but they still persist in reacting to their reflection as if they were seeing other monkeys. Even gibbons (apes) and gorillas (great apes) seem incapable of learning that their behavior is the source of the behavior depicted in the image. Most primates, therefore, appear to lack a cognitive category for processing mirrored information about themselves. The implications of these data for traditional views of consciousness are considered briefly, and a recent attempt to develop an operant analog to self-recognition is critically evaluated. Finally, an attempt is made to show that self-awareness, consciousness, and mind are not mutually exclusive cognitive categories and that the emergence of self-awareness may be equivalent to the emergence of mind. Several indices of “mind” which can be applied to nonhuman species are discussed in the context of an attempt to develop a comparative psychology of mind.     

Population history, biogeography, and taxonomy of orangutans (Genus: Pongo) based on a population genetic meta-analysis of multiple loci

This paper examines orangutan population history and evolution through a meta-analysis of seven loci collected from both Sumatran and Bornean orangutans. Within orangutans, most loci show that the Sumatran population is about twice as diverse as the Bornean population. Orangutans are more diverse than African apes and humans. Sumatran and Bornean populations show significant genetic differentiation from one another and their history does not differ significantly from an 'island model' (population splitting without gene flow). Two different methods support a divergence of Bornean and Sumatran orangutans at 2.7-5 million years ago. This suggests that Pleistocene events, such as the cyclical exposure of the Sunda shelf and the Toba volcanic eruption, did not have a major impact on the divergence of Bornean and Sumatran orangutans. Pairwise mismatch analyses, however, suggest that Bornean orangutans have undergone a recent population expansion (beginning 39,000-64,000 years ago), while Sumatran orangutan populations were stable. Pleistocene events may have contributed to these aspects of orangutan population history. These conclusions are applied to the debate on orangutan taxonomy.     

Orangutan Energetics and the Influence of Fruit Availability in the Nonmasting Peat-swamp Forest of Sabangau,Indonesian Borneo

Data on energy intake and the effects of fluctuations in fruit availability on energy intake for African apes, and orangutans in mast-fruiting habitats, indicate that orangutans may face greater energetic challenges than do their African counterparts. Comparable data on orangutans in nonmasting forests, which experience lower fluctuations in fruit availability, have been lacking, however, complicating interpretations. We conducted a 46-mo study of orangutan energetics in the nonmasting Sabangau peat-swamp forest, Indonesian Borneo. Sabangau orangutans experienced periods of negative energy balance apparently even longer than in mast-fruiting habitats, as indicated by comparisons of observed energy intake with theoretical requirements and analysis of urinary ketones. Daily energy intake was positively related to fruit availability in flanged males, but not in adult females or unflanged males. This may represent different foraging strategies between age-sex classes and suggests that fruit availability is not always an accurate indicator of ape energy intake/balance. Urinary ketone levels were not generally related to fruit availability, daily energy intake, day range, or party size. This is probably due to low energy intake, and consequently high ketone production, throughout much of the study period. Comparisons with published results on African apes support the hypothesis that orangutans are unique among hominoids in regularly experiencing prolonged periods of negative energy balance. This has important effects on orangutan behavior and socioecology, and has likely been a key factor driving the evolutionary divergence of orangutans and African apes.     

Slow loris (Nycticebus borneanus) consumption by a wild Bornean orangutan (Pongo pygmaeus wurmbii)

Primates - Vertebrate predation and consumption by wild Bornean orangutans (Pongo pygmaeus spp.) is rare. In contrast to recorded observations of slow loris consumption by Sumatran orangutans...     

Leaf Surface Roughness Elicits Leaf Swallowing Behavior in Captive Chimpanzees (Pan troglodytes) and Bonobos (P. paniscus), but not in Gorillas (Gorilla gorilla) or Orangutans (Pongo abelii)

Researchers have described apparently self-medicative behaviors for a variety of nonhuman species including birds and primates. Wild chimpanzees, bonobos, and gorillas have been observed to swallow rough leaves without chewing, a behavior proposed to be self-medicative and to aid control of intestinal parasites. Researchers have hypothesized that the presence of hairs on the leaf surface elicits the behavior. We investigated the acquisition and the underlying mechanisms of leaf swallowing. We provided 42 captive great apes (24 chimpanzees, six bonobos, six gorillas, and six orangutans) with both rough-surfaced and hairless plants. None of the subjects had previously been observed to engage in leaf swallowing behavior and were therefore assumed naïve. Two chimpanzees and one bonobo swallowed rough-surfaced leaves spontaneously without chewing them. In a social setup six more chimpanzees acquired the behavior. None of the gorillas or orangutans showed leaf swallowing. Because this behavior occurred in naïve individuals, we conclude that it is part of the behavioral repertoire of chimpanzees and bonobos. Social learning is thus not strictly required for the acquisition of leaf swallowing, but it may still facilitate its expression. The fact that apes always chewed leaves of hairless control plants before swallowing, i.e., normal feeding behavior, indicates that the surface structure of leaves is indeed a determinant for initiating leaf swallowing in apes where it occurs.