Intra-and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool use

Tool manufacture and use have been described for wild orangutans (Pongo pygmaeus), with appreciable interpopulational differences in tool complexes. The ecological factors that contribute to these differences require investigation. Significant interpopulational differences in diet suggest that ecological factors contribute to variation in tool-based insect foraging. Using 4 years of behavioral data from the Suaq Balimbing Research Station (Sumatra, Indonesia), we tested predictions of two ecological hypotheses for the invention of tool use for insect foraging. We found limited evidence for inter- and intrasexual differences, as well as temporal variation, in activity budget and diet. However, differences did not correspond to variation in either rate of tool use or specialization on tool-based insectivory. Compared to other populations, orangutans at Suaq Balimbing ate significantly more insects. Low temporal variation in insectivory and an abundance of social insects at Suaq Balimbing suggest that insects formed a staple in the diet rather than a fallback food. Our findings do not support the hypothesis that tool use is a response to the low availability of primary food sources. Rather, greater opportunities for invention likely contributed to insect-extraction tool use at Suaq Balimbing.     

The conditions for tool use in primates: implications for the evolution of material culture

In order to identify the conditions that favored the flourishing of primate tool use into hominid technology, we examine inter- and intraspecific variation in manufacture and use of tools in extant nonhuman primates, and develop a model to account for their distribution. We focus on tools used in acquiring food, usually by extraction. Any model for the evolution of the use of feeding tools must explain why tool use is found in only a small subset of primate species, why many of these species use tools much more readily in captivity, why routine reliance on feeding tools is found in only two species of ape, and why there is strong geographic variation within these two species. Because ecological factors alone cannot explain the distribution of tool use in the wild, we develop a model that focuses on social and cognitive factors affecting the invention and transmission of tool-using skills. The model posits that tool use in the wild depends on suitable ecological niches (especially extractive foraging) and the manipulative skills that go with them, a measure of intelligence that enables rapid acquisition of complex skills (through both invention and, more importantly, observational learning), and social tolerance in a gregarious setting (which facilitates both invention and transmission). The manipulative skills component explains the distribution across species of the use of feeding tools, intelligence explains why in the wild only apes are known to make and use feeding tools routinely, and social tolerance explains variation across populations of chimpanzees and orangutans. We conclude that strong mutual tolerance was a key factor in the explosive increase in technology among hominids, probably intricately tied to a lifestyle involving food sharing and tool-based processing or the acquisition of large, shareable food packages.     

Individual variation in the rate of use of tree-hole tools among wild orang-utans: implications for hominin evolution

Primate tool use varies among species, populations, and individuals. Individual variation is especially poorly understood. Orang-utans in the Sumatran swamp forest of Suaq Balimbing varied widely in rates of tool use to extract honey, ants or termites from tree holes and in the degree to which they specialized on this tree-hole tool use. We tested whether individual variation was best explained by effects of social dominance, habitat differences, or by opportunities for socially learning the skills during ontogeny. There was no evidence for the first two hypotheses. However, we found a strong relationship between tool use specialization and mean female party size, which was used as a proxy for the opportunities for socially mediated learning in a foraging context during their development. This use was justified because females are rather philopatric and their mean party size remained stable over time, thus reflecting long-term tendencies. The correlation was not an artifact of a direct effect of party size on tool use tendencies, and did not hold for males, the dispersing sex. Thus, variation in the number of opportunities for social learning explains tool use variation within populations, corroborating hypotheses for between-population variation. The emergence of human culture was accompanied by vastly improved mechanisms of social learning. In order for these improvements to be favored by natural selection, the cultural potential must have actually been expressed. Thus, a combination of strong sociability and a reliance on tool-using or other technical skills acquired through social learning must have characterized early hominins.     

The socioecology of fission-fusion sociality in Orangutans

Fission-fusion systems can have the group or the individual as their primary unit. In group-based fission-fusion systems, predation risk reduction is the major benefit to grouping, in the individual-based ones the benefits are likely to be primarily social. Orangutans, like chimpanzees, are examples of an individual-based fission-fusion species. The orangutans inhabiting a Sumatran swamp forest (Suaq Balimbing) are more likely than elsewhere to form travel parties. As elsewhere, the main benefits of grouping are social: mating opportunities, protection from harassment and socialization of infants. Most animals also incur costs, but these are relatively low at Suaq Balimbing due to the high productivity of the swamp. Costs seem to be disproportionately high for females with mid-sized infants, who avoid parties.     

Forest Structure and Support Availability Influence Orangutan Locomotion in Sumatra and Borneo

The influence of habitat structure and support availability on support use is an important aspect of understanding locomotor behavior in arboreal primates. We compared habitat structure and support availability in three orangutan study sites—two on Sumatra (Pongo abelii) in the dry‐lowland forest of Ketambe and peat swamp forest of Suaq Balimbing, and one on Borneo (Pongo pygmaeus wurmbii) in the disturbed peat swamp forest of Sabangau—to better understand orangutan habitat use. Our analysis revealed vast differences in tree and liana density between the three sites. Sabangau had a much higher overall tree density, although both Sumatran sites had a higher density of larger trees. The two peat swamp forests were more similar to each other than to Ketambe, particularly with regard to support availability. Ketambe had a wider variety of supports of different sizes and types, and a higher density of larger lianas than the two peat swamps. Orangutans in all three sites did not differ substantially in terms of their preferred supports, although Sumatran orangutans had a strong tendency to use lianas, not observed in Sabangau. Differences in observed frequencies of locomotor behavior suggest the homogeneous structure of Sabangau limits the locomotor repertoire of orangutans, with high frequencies of fewer behaviors, whereas the wider range of supports in Ketambe appears to have facilitated a more varied locomotor repertoire. There were no differences among age‐sex classes in the use of arboreal pathways in Suaq Balimbing, where orangutans selected larger trees than were typically available. This was less apparent in Sabangau, where orangutans generally used trees in relation to their environmental abundance, reflecting the homogeneous nature of disturbed peat swamp forest. These results demonstrate that forest architecture has an important influence on orangutan locomotion, which may become increasingly important as the structure of orangutan habitat continues to be altered through human disturbance. Am. J. Primatol. 74:1128‐1142, 2012. © 2012 Wiley Periodicals, Inc.     

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

Background

Orangutans have one of the slowest-paced life histories of all mammals. Whereas life-history theory suggests that the time to reach adulthood is constrained by the time needed to reach adult body size, the needing-to-learn hypothesis instead suggests that it is limited by the time needed to acquire adult-level skills.To test between these two hypotheses, we compared the development of foraging skills and growth trajectories of immature wild orangutans in two populations: at Tuanan (Pongo pygmaeus wurmbii), Borneo, and Suaq Balimbing (Pongo abelii), Sumatra. We collected behavioral data on diet repertoire, feeding rates and ranging competence during focal follows, and estimated growth through non-invasive laser photogrammetry.

Results

We found that adult-like diet repertoires are attained around the age of weaning and that female immatures increase their repertoire size faster than their male peers. Adult-level feeding rates of easy techniques are reached just after weaning, but several years later for more difficult techniques, albeit always before adulthood (i.e. age at first reproduction). Independent immatures had faster feeding rates for easy to process items than their mothers, with male immatures achieving faster feeding rates earlier in development relative to females. Sumatran immatures reach adult-level feeding rates 2–3 years later than their Bornean peers, in line with their higher dietary complexity and later weaning. The range-use competence of independently ranging and weaned immatures is similar to that of adult females. Body size measurements showed, immatures grow until female age of first reproduction.

Conclusions

In conclusion, unlike in humans, orangutan foraging skills are in place prior to reproduction. Growth trajectories suggest that energetic constraints, rather than skills, best explain the length of immaturity. However, skill competence for dietary independence is reached later where the adult niche is more complex, which is consistent with the relatively later weaning age with increasing brain size found generally in primates, and apes in particular.

     

The development of wild immature Sumatran orangutans (Pongo abelii) at Ketambe

Orangutans have the longest immature period and inter-birth interval of all ape species. This may be explained by a slow life history, the need to develop skills or by their relatively solitary lifestyle, which prevents a mother from associating with two offspring. This study of wild immature orangutans at the Ketambe Research Station, Indonesia, describes, with partly cross-sectional, partly longitudinal data, their development to independence. The study subjects ranged from 1 to 11 years of age. Data on their activity budget, diet, mother–offspring proximity and maintenance of proximity, association with conspecifics and play behavior were collected. The results indicate that immature orangutans can provide for their own food and transport, and therefore were independent of direct maternal care, at an age of possibly 3 but more clearly 6 years. This is similar to chimpanzees, and refutes the slow life history hypothesis. Immature orangutans remain within their mother’s vicinity until the age of 8 years, indicating a dependence on indirect maternal care, and this coincides with the period during which the mother does not produce another offspring. A female orangutan seems unable to associate with an older immature while caring for a new infant. This is consistent with the solitary-lifestyle hypothesis and corroborates the results obtained with the Sumatran orangutan population at Suaq Balimbing. However, why an immature depends indirectly on its mother for such a long period remains unclear. It is possible that it needs to develop ecological or social skills or needs the protection of its mother. Unfortunately, no data were available to distinguish between these possibilities.     

New tool use by wild Sumatran orangutans (Pongo pygmaeus abelii)

Two forms of tool use by wild Sumatran orangutans are reported from the Agusan Monitoring Station, a new research site in Indonesia. One form, a branch "hook" used in locomotion, has not been reported previously in wild orangutans. The second form, a leaf "pad" used to protect the hands and feet from thorns while feeding, shares similarities in form and function with a tool type used by orangutans at Ketambe, a nearby research site. Both instances of tool use occurred in areas of disturbance, and appear to be spontaneous inventions under novel conditions, although habitual use of the tool in other ecological contexts is plausible. A summary of the distribution of tool use types in wild orangutans is presented.     

Culture and geographic variation in orangutan behavior

Although geographic variation in an organism's traits is often seen as a consequence of selection on locally adaptive genotypes accompanied by canalized development [1], developmental plasticity may also play a role [2, 3], especially in behavior [4]. Behavioral plasticity includes both individual learning and social learning of local innovations ("culture"). Cultural plasticity is the undisputed and dominant explanation for geographic variation in human behavior. It has recently also been suggested to hold for various primates and birds [5], but this proposition has been met with widespread skepticism [6-8]. Here, we analyze parallel long-term studies documenting extensive geographic variation in behavioral ecology, social organization, and putative culture of orangutans [9] (genus Pongo). We show that genetic differences among orangutan populations explain only very little of the geographic variation in behavior, whereas environmental differences explain much more, highlighting the importance of developmental plasticity. Moreover, variation in putative cultural variants is explained by neither genetic nor environmental differences, corroborating the cultural interpretation. Thus, individual and cultural plasticity provide a plausible pathway toward local adaptation in long-lived organisms such as great apes and formed the evolutionary foundation upon which human culture was built.     

Effects of nest-site availability and distribution on density-dependent clutch size and laying date in the Chough Pyrrhocorax pyrrhocorax

We compared the breeding phenology and clutch size of Choughs Pyrrhocorax pyrrhocorax in three Spanish areas that differed in feeding habitat, breeding environmental conditions and the distribution and availability of different nesting sites (cliffs or artefacts). The variation in the timing of laying seemed to be related to differences in climatic conditions determined by the altitude. The variation in clutch size was associated with the different use that Choughs made of the feeding areas because of the contrasting availability and distribution of their nesting sites. Within southeastern Madrid, clutch size of the Chough decreased and its variance increased at high nest densities on cliff sites, suggesting that density dependence in fecundity arises from habitat heterogeneity rather than by interference. At high densities, individuals, territories, nest sites or a combination of these may differ in quality, thus promoting differences and increasing the variance in the initial investment of reproductive effort. The syncronization of the onset of laying at increased breeding densities suggests that social influences arising from communal foraging or avoidance of predation by early warning and predator swamping may be acting also. We suggest that nest-site availability and distribution have a major influence on the social organization of Choughs through their breeding and foraging strategies.     

The influence of demography,population structure and selection on molecular diversity in the selfing freshwater snail Biomphalaria pfeifferi

Several forces may affect the distribution of genetic diversity in natural populations when compared to what is expected in a random-mating, constant size population of neutral genes. One solution for unravelling their respective influence is to study several genes at once in order to better reflect the true genealogy. Here we reconstruct the evolutionary history of the freshwater snail Biomphalaria pfeifferi over its entire distribution, using eight African populations, and three congeneric species as outgroups. A phylogenetic analysis was conducted using amplified fragment length polymorphism markers, and sequences at eight nuclear non-coding loci and one mitochondrial gene were used to analyse population structure. The geographic distribution of variation suggests greater affinities within than among regions. The pattern of variability at both the nuclear and mitochondrial DNA (mtDNA) loci is consistent with a bottleneck, although population structure may also partly explain our results. Our results are also indicative of the role of selection, whether positive or purifying, in the mtDNA. This highlights the fact that the interfering influences of population structure, demography and selection on molecular variation are not easily distinguished.     

Does geography or ecology best explain 'cultural' variation among chimpanzee communities?

Much attention has been paid to geographic variation in chimpanzee behavior, but few studies have applied quantitative techniques to explain this variation. Here, we apply methods typically utilized in macroecology to explain variation in the putative cultural traits of chimpanzees. We analyzed published data containing 39 behavioral traits from nine chimpanzee communities. We used a canonical correspondence analysis to examine the relative importance of environmental characteristics and geography, which may be a proxy for inter-community gene flow and/or social transmission, for explaining geographic variation in chimpanzee behavior. We found that geography, and longitude in particular, was the best predictor of behavioral variation. Chimpanzee communities in close longitudinal proximity to each other exhibit similar behavioral repertoires, independent of local ecological factors. No ecological variables were significantly related to behavioral variation. These results support the idea that inter-community dispersal patterns have played a major role in structuring behavioral variation. We cannot be certain whether behavioral variation has a genetic basis, is the result of innovation and diffusion, or a combination of the two.     

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.     

The Macaque Social Responsiveness Scale (mSRS): A Rapid Screening Tool for Assessing Variability in the Social Responsiveness of Rhesus Monkeys (Macaca mulatta)

Understanding the biological mechanisms underlying human neuropsychiatric disorders, such as autism spectrum disorder (ASD), has been hindered by the lack of a robust, translational animal model. Rhesus monkeys (Macaca mulatta) display many of the same social behaviors that are affected in ASD, making them an excellent animal species in which to model social impairments. However, the social impairments associated with ASD may reflect extreme ends of a continuous distribution of traits. Thus, to validate the rhesus monkey as an animal model for studying social impairments that has strong translational relevance for ASD, researchers need an easily-implemented measurement tool that can quantify variation in social behavior dimensionally. The Social Responsiveness Scale (SRS) is a 65-item survey that identifies both typical and atypical social behaviors in humans that covary with ASD symptom severity. A chimpanzee SRS has already been validated and the current study adapted this tool for use in the rhesus monkey (mSRS). Fifteen raters completed the mSRS for 105 rhesus monkeys living at the Yerkes National Primate Research Center. The mSRS scores showed a unimodal distribution with a positive skew that identified 6 statistical outliers. Inter-rater reliability was very strong, but only 17 of the 36 questions showed positive intra-item reliability. The results of an exploratory factor analysis identified 3 factors that explained over 60% of the variance, with 12 items significantly loading onto the primary factor. These items reflected behaviors associated with social avoidance, social anxiety or inflexibility and social confidence. These initial findings are encouraging and suggest that variability in the social responsiveness of rhesus monkeys can be quantified using the mSRS: a tool that has strong translational relevance for human disorders. With further modification, the mSRS may provide an promising new direction for research on the biological mechanisms underlying social impairments.     

The nature of culture: technological variation in chimpanzee predation on army ants revisited

Chimpanzee (Pan troglodytes) predation on army ants (Dorylus, subgenus Anomma) is an impressive example of skillful use of elementary technology, and it has been suggested to reflect cultural differences among chimpanzee communities. Alternatively, the observed geographic diversity in army-ant-eating may represent local behavioral responses of the chimpanzees to the anti-predator traits of the army ant species present at the different sites. We examined assemblages of available prey species, their behavior and morphology, consumption by chimpanzees, techniques employed, and tool lengths at 14 sites in eastern, central, and western Africa. Where army ants are eaten, tool length and concomitant technique are a function of prey type. Epigaeically foraging species with aggressive workers that inflict painful bites are harvested with longer tools and usually by the "pull-through" technique; species foraging in leaf-litter with less aggressive workers that inflict less painful bites are harvested with short tools and by the "direct-mouthing" technique. However, prey species characteristics do not explain several differences in army-ant-eating between Bossou (Guinea) and Ta? (Ivory Coast), where the same suite of prey species is available and is consumed. Moreover, the absence of army-ant-eating at five sites cannot be explained by the identity of available prey species, as all the species found at these sites are eaten elsewhere. We conclude that some of the observed variation in the predator-prey relationship of chimpanzees and army ants reflects environmental influences driven by the prey, while other variation is not linked to prey characteristics and may be solely sociocultural.     

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.     

Cognitive requirements for tool use by New Caledonian crows (Corvus moneduloides)

Abstract

Cumulative technological evolution has been suggested to explain the existence of different pandanus tool designs manufactured by New Caledonian crows. Circumstantial evidence from the distribution of the three tool designs that they manufacture suggests transmission of the designs probably involves accurate social learning, a characteristic considered essential for the cumulative evolution of tools. Recently, Kenward et al. (2005) reported that four hand‐raised crows developed basic stick tool use without social learning. This finding cast doubt on the importance of social learning in the evolution of crows’ pandanus tools in the wild. Here, we report that a naïve male crow at Parc Zoo‐Forestier, Nouméa, developed proficient stick tool use without social input in 2002. In 2004, four captive crows, including the naïve male, that were inexperienced with pandanus material were given an opportunity to use and/or manufacture pandanus tools. Only two of the four birds used the tools but none manufactured tools. Our preliminary findings and the work with the four hand‐raised crows keep open the possibility that the evolution of crows’ pandanus tool designs is based on social learning. We propose that social learning and a disposition to develop basic tool use without social input are both essential cognitive requirements for cumulative technological evolution.     

Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts

Spatial variation in parasitism is commonly observed in intermediate host populations. However, the factors that determine the causes of this variation remain unclear. Increasing evidence has suggested that spatial heterogeneity in parasitism among intermediate hosts may result from variation in recruitment processes initiated by definitive hosts. I studied the perching and habitat use patterns of wading birds, the definitive hosts in this system, and its consequences for the recruitment of parasites in snail intermediate hosts. Populations of the mangrove snail, Cerithidea scalariformis, collected from mangrove swamps on the east coast of central Florida are parasitized by a diverse community of trematode parasites. These parasites are transmitted from wading birds, which frequently perch on dead mangrove trees. I tested the hypothesis that mangrove perches act as transmission foci for trematode infections of C. scalariformis and that the spatial variation of parasitism frequently observed in this system is likely to emanate from the distribution of wading birds. On this fine spatial scale, definitive host behaviors, responding to a habitat variable, influenced the distribution, abundance and species composition of parasite recruitment to snails. This causal chain of events is supported by regressions between perch density, bird abundance, bird dropping density and ultimately parasite prevalence in snails. Variation between prevalence of parasites in free-ranging snails versus caged snails shows that while avian definitive hosts initiate spatial patterns of parasitism in snails through their perching behaviors, these patterns may be modified by the movement of snail hosts. Snail movement could disperse their associated parasite populations within the marsh, which may potentially homogenize or further increase parasite patchiness initiated by definitive hosts.     

Geographic variation in feeding preference of a generalist herbivore: the importance of seaweed chemical defenses

The ecological impacts of generalist herbivores depend on feeding preferences, which can vary across and within herbivore species. Among mesoherbivores, geographic variation in host use can occur because host plants have a more restricted geographic distribution than does the herbivore, or there is local evolution in host preference, or both. We tested the role of local evolution using the marine amphipod Ampithoe longimana by rearing multiple amphipod populations from three regions (subtropical Florida, warm-temperate North Carolina and cold-temperate New England) and assaying their feeding preferences toward ten seaweeds that occur in some but not all regions. Six of the ten seaweeds produce anti-herbivore secondary metabolites, and we detected geographic variation in feeding preference toward five (Dictyota menstrualis, Dictyota ciliolata, Fucus distichus, Chondrus crispus and Padina gymnospora, but not Caulerpa sertularioides). Amphipod populations that co-occur with a chemically-rich seaweed tended to have stronger feeding preferences for that seaweed, relative to populations that do not co-occur with the seaweed. A direct test indicated that geographic variation in feeding preference toward one seaweed (D. ciliolata) is mediated by feeding tolerance for lipophilic secondary metabolites. Among the four seaweeds that produce no known secondary metabolites (Acanthophora, Ectocarpus, Gracilaria and Hincksia/Feldmannia spp.), we detected no geographic variation in feeding preference. Thus, populations are more likely to evolve greater feeding preferences for local hosts when those hosts produce secondary metabolites. Microevolution of feeding behaviors of generalist marine consumers likely depends on the availability and identity of local hosts and the strength of their chemical defenses.