Orangutans and the evolution of sharp stone tools.

Orangutans use stone tools in a variety of modes, including cutting. This behavior appears to be learned from trusted social partners.

Metabolic acceleration and the evolution of human brain size and life history.

Humans are distinguished from the other living apes in having larger brains and an unusual life history that combines high reproductive output with slow childhood growth and exceptional longevity. This suite of derived traits suggests major changes in energy expenditure and allocation in the human lineage, but direct measures of human and ape metabolism are needed to compare evolved energy strategies among hominoids. Here we used doubly labelled water measurements of total energy expenditure (TEE; kcal day(-1)) in humans, chimpanzees, bonobos, gorillas and orangutans to test the hypothesis that the human lineage has experienced an acceleration in metabolic rate, providing energy for larger brains and faster reproduction without sacrificing maintenance and longevity. In multivariate regressions including body size and physical activity, human TEE exceeded that of chimpanzees and bonobos, gorillas and orangutans by approximately 400, 635 and 820 kcal day(-1), respectively, readily accommodating the cost of humans' greater brain size and reproductive output. Much of the increase in TEE is attributable to humans' greater basal metabolic rate (kcal day(-1)), indicating increased organ metabolic activity. Humans also had the greatest body fat percentage. An increased metabolic rate, along with changes in energy allocation, was crucial in the evolution of human brain size and life history.

Orangutan strategies for solving a visuospatial memory task.

The popular game known as Concentration (also commonly referred to as Memory), in which players search for matching pairs among a grid of face-down cards, provides a robust platform for examining visuospatial memory in a simple and nonverbal way. Five orangutans (Pongo ssp.) at the Indianapolis Zoo were given a modified version of the Concentration Game in which three cards were shown face-down on a computer screen, two of which matched each other while the third was a foil. Subjects overturned two cards at a time by touching them, with trials terminating in a food reward if the overturned cards matched, or reverting to their face-down position if they did not. A constraint was experimentally imposed on the game whereby the first two cards touched would never match, resulting in an optimal strategy composed of touching the first two cards, followed by the third, followed by the card among the first two cards that matched the third. We aimed to measure the extent to which orangutans would memorize and utilize visuospatial cues to solve the task in the optimal manner. Findings showed that three of five subjects utilized an optimal strategy more often than would be expected by chance, but also over utilized specific patterns of choices instead of adjusting their strategies to minimize the overall number of card flips. Visuospatial recall played a role in several of the participants' strategies for completing the task, but not to an extent that was necessary to achieve optimal gameplay.

Primate energy expenditure and life history.

Humans and other primates are distinct among placental mammals in having exceptionally slow rates of growth, reproduction, and aging. Primates' slow life history schedules are generally thought to reflect an evolved strategy of allocating energy away from growth and reproduction and toward somatic investment, particularly to the development and maintenance of large brains. Here we examine an alternative explanation: that primates' slow life histories reflect low total energy expenditure (TEE) (kilocalories per day) relative to other placental mammals. We compared doubly labeled water measurements of TEE among 17 primate species with similar measures for other placental mammals. We found that primates use remarkably little energy each day, expending on average only 50% of the energy expected for a placental mammal of similar mass. Such large differences in TEE are not easily explained by differences in physical activity, and instead appear to reflect systemic metabolic adaptation for low energy expenditures in primates. Indeed, comparisons of wild and captive primate populations indicate similar levels of energy expenditure. Broad interspecific comparisons of growth, reproduction, and maximum life span indicate that primates' slow metabolic rates contribute to their characteristically slow life histories.

Orangutans (Pongo spp.) have deeper, more efficient sleep than baboons (Papio papio) in captivity.

The nightly construction of arboreal sleeping platforms or "nests" has been observed among every great ape population studied to date. However, this behavior has never been reported in any other nonhuman primate and comparisons between ape and monkey sleep illuminate the link between sleeping substrates, positional behavior, and sleep efficiency. Here, we compare sleep depth and efficiency and night-time positional behavior between a large-bodied cercopithecoid (Papio papio) and a large-bodied hominoid (Pongo spp.) at the Indianapolis Zoo. We used infrared videography to assess nightly sleep and awake behavioral states, gross body movements, and postures in baboons (N = 45 nights) and orangutans (N = 128 nights). We calculated the total waking time, total sleep time, sleep fragmentation (the number of brief awakenings ≥2 min/h), sleep motor activity (number of motor activity bouts per hour), sleep efficiency (sleep duration/time in bed), and percentage of time spent in each posture. By every measure, orangutans experienced overall deeper, more efficient sleep. Baboons were more likely to sleep in guarded, upright positions (weight bearing on their ischial callosities) and never opted to use additional materials to augment sleep environments, whereas orangutans slept in insouciant, relaxed positions on constructed sleeping materials. Our results suggest that relaxed sleeping postures may have been enabled by sleeping platforms as a behavioral facilitator to sleep, which could have allowed for greater sleep depth and next-day cognitive capacities in both great apes and hominins.

Metabolic adaptation for low energy throughput in orangutans.

Energy is the fundamental currency of life--needed for growth, repair, and reproduction--but little is known about the metabolic physiology and evolved energy use strategies of the great apes, our closest evolutionary relatives. Here we report daily energy use in free-living orangutans (Pongo spp.) and test whether observed differences in energy expenditure among orangutans, humans, and other mammals reflect known differences in life history. Using the doubly labeled water method, we measured daily energy expenditure (kCal/d) in orangutans living in a large indoor/outdoor habitat at the Great Ape Trust. Despite activity levels similar to orangutans in the wild, Great Ape Trust orangutans used less energy, relative to body mass, than nearly any eutherian mammal ever measured, including sedentary humans. Such an extremely low rate of energy use has not been observed previously in primates, but is consistent with the slow growth and low rate of reproduction in orangutans, and may be an evolutionary response to severe food shortages in their native Southeast Asian rainforests. These results hold important implications for the management of orangutan populations in captivity and in the wild, and underscore the flexibility and interdependence of physiological, behavioral, and life history strategies in the evolution of apes and humans.

Orangutan (Pongo spp.) whistling and implications for the emergence of an open-ended call repertoire: a replication and extension.

One of the most apparent discontinuities between non-human primate (primate) call communication and human speech concerns repertoire size. The former is essentially fixed to a limited number of innate calls, while the latter essentially consists of numerous learned components. Consequently, primates are thought to lack laryngeal control required to produce learned voiced calls. However, whether they may produce learned voiceless calls awaits investigation. Here, a case of voiceless call learning in primates is investigated--orangutan (Pongo spp.) whistling. In this study, all known whistling orangutans are inventoried, whistling-matching tests (previously conducted with one individual) are replicated with another individual using original test paradigms, and articulatory and acoustic whistle characteristics are compared between three orangutans. Results show that whistling has been reported for ten captive orangutans. The test orangutan correctly matched human whistles with significantly high levels of performance. Whistle variation between individuals indicated voluntary control over the upper lip, lower lip, and respiratory musculature, allowing individuals to produce learned voiceless calls. Results are consistent with inter- and intra-specific social transmission in whistling orangutans. Voiceless call learning in orangutans implies that some important components of human speech learning and control were in place before the homininae-ponginae evolutionary split.

Evolution of water conservation in humans.

To sustain life, humans and other terrestrial animals must maintain a tight balance of water gain and water loss each day.1-3 However, the evolution of human water balance physiology is poorly understood due to the absence of comparative measures from other hominoids. While humans drink daily to maintain water balance, rainforest-living great apes typically obtain adequate water from their food and can go days or weeks without drinking4-6. Here, we compare isotope-depletion measures of water turnover (L/d) in zoo- and rainforest-sanctuary-housed apes (chimpanzees, bonobos, gorillas, and orangutans) with 5 diverse human populations, including a hunter-gatherer community in a semi-arid savannah. Across the entire sample, water turnover was strongly related to total energy expenditure (TEE, kcal/d), physical activity, climate (ambient temperature and humidity), and fat free mass. In analyses controlling for those factors, water turnover was 30% to 50% lower in humans than in other apes despite humans' greater sweating capacity. Water turnover in zoo and sanctuary apes was similar to estimated turnover in wild populations, as was the ratio of water intake to dietary energy intake (∼2.8 mL/kcal). However, zoo and sanctuary apes ingested a greater ratio of water to dry matter of food, which might contribute to digestive problems in captivity. Compared to apes, humans appear to target a lower ratio of water/energy intake (∼1.5 mL/kcal). Water stress due to changes in climate, diet, and behavior apparently led to previously unknown water conservation adaptations in hominin physiology.

Does early care affect joint attention in great apes (Pan troglodytes, Pan paniscus, Pongo abelii, Pongo pygmaeus, Gorilla gorilla)?

The ability to share attention with another is the foundation on which other theory of mind skills are formed. The quality of care received during infancy has been correlated with increased joint attention in humans. The purpose of this study was to assess the effects of care style (responsive or basic) and caregiver type (ape or human) during the first 6 months on joint attention in 4 great ape species (Pan troglodytes, Gorilla gorilla, Pongo spp., and Pan pansicus). Great apes engaged in joint attention with conspecifics and humans regardless of the style of early care they experienced from either a great ape mother or human caregiver. This finding suggests that joint attention is a robust ability in great apes that is resilient against at least some differences in early care. Future studies using additional measures of early care quality are recommended.

A case of spontaneous acquisition of a human sound by an orangutan.

The capacity of nonhuman primates to actively modify the acoustic structure of existing sounds or vocalizations in their repertoire appears limited. Several studies have reported population or community differences in the acoustical structure of nonhuman primate long distance calls and have suggested vocal learning as a mechanism for explaining such variation. In addition, recent studies on great apes have indicated that there are repertoire differences between populations. Some populations have sounds in their repertoire that others have not. These differences have also been suggested to be the result of vocal learning. On yet another level great apes can, after extensive human training, also learn some species atypical vocalizations. Here we show a new aspect of great ape vocal learning by providing data that an orangutan has spontaneously (without any training) acquired a human whistle and can modulate the duration and number of whistles to copy a human model. This might indicate that the learning capacities of great apes in the auditory domain might be more flexible than hitherto assumed.

Orangutans show active voicing through a membranophone.

Active voicing - voluntary control over vocal fold oscillation - is essential for speech. Nonhuman great apes can learn new consonant- and vowel-like calls, but active voicing by our closest relatives has historically been the hardest evidence to concede to. To resolve this controversy, a diagnostic test for active voicing is reached here through the use of a membranophone: a musical instrument where a player's voice flares a membrane's vibration through oscillating air pressure. We gave the opportunity to use a membranophone to six orangutans (with no effective training), three of whom produced a priori novel (species-atypical) individual-specific vocalizations. After 11 and 34 min, two subjects were successful by producing their novel vocalizations into the instrument, hence, confirming active voicing. Beyond expectation, however, within <1 hour, both subjects found opposite strategies to significantly alter their voice duration and frequency to better activate the membranophone, further demonstrating plastic voice control as a result of experience with the instrument. Results highlight how individual differences in vocal proficiency between great apes may affect performance in experimental tests. Failing to adjust a test's difficulty level to individuals' vocal skill may lead to false negatives, which may have largely been the case in past studies now used as "textbook fact" for great ape "missing" vocal capacities. Results qualitatively differ from small changes that can be caused in innate monkey calls by intensive months-long conditional training. Our findings verify that active voicing beyond the typical range of the species' repertoire, which in our species underpins the acquisition of new voiced speech sounds, is not uniquely human among great apes.

Response strategies in list learning by orangutans (Pongo pygmaeus x P. abelii).

Rhesus monkeys (Macaca mulatta) develop strategies to acquire and execute serial lists (K. B. Swartz & S. A. Himmanen, 2001). Serial probe recognition studies of list memory have demonstrated similarities across monkeys and humans (S. F. Sands & A. A. Wright, 1980). The present study extended the investigation of list learning and memory to determine whether orangutans (Pongo pygmaeus x P. abelii) would show evidence of subjective organization of photographic lists in a manner similar to that shown by humans learning a list of unrelated words (E. Tulving, 1962). No evidence for the effective use of a subjective organization strategy was found, but the orangutans developed a right-to-left spatial response strategy, which emerged during the acquisition of 5-item lists. This strategy was an effective way to reduce the load on working memory when presented with a complex array of items.

Vocal fold control beyond the species-specific repertoire in an orang-utan.

Vocal fold control was critical to the evolution of spoken language, much as it today allows us to learn vowel systems. It has, however, never been demonstrated directly in a non-human primate, leading to the suggestion that it evolved in the human lineage after divergence from great apes. Here, we provide the first evidence for real-time, dynamic and interactive vocal fold control in a great ape during an imitation "do-as-I-do" game with a human demonstrator. Notably, the orang-utan subject skilfully produced "wookies" - an idiosyncratic vocalization exhibiting a unique spectral profile among the orang-utan vocal repertoire. The subject instantaneously matched human-produced wookies as they were randomly modulated in pitch, adjusting his voice frequency up or down when the human demonstrator did so, readily generating distinct low vs. high frequency sub-variants. These sub-variants were significantly different from spontaneous ones (not produced in matching trials). Results indicate a latent capacity for vocal fold exercise in a great ape (i) in real-time, (ii) up and down the frequency spectrum, (iii) across a register range beyond the species-repertoire and, (iv) in a co-operative turn-taking social setup. Such ancestral capacity likely provided the neuro-behavioural basis of the more fine-tuned vocal fold control that is a human hallmark.

Effect of repeated exposures and sociality on novel food acceptance and consumption by orangutans.

Hundreds of rehabilitant great apes have been released into the wild, and thousands await release. However, survival rates after release can be as low as 20%. Several factors influence individuals' survival rates, one of which is the capacity to obtain an adequate diet once released. Released individuals are faced with a mixture of familiar and novel foods in an unfamiliar forest; therefore, it is important to understand how they increase acceptance and consumption of novel foods. This is especially vital for omnivorous species, such as wild great apes, which consume several hundred species of different foods. We assessed the effects of repeated exposures and sociality (i.e. co-feeding in the presence of one or more other individuals) on the acceptance and consumption of novel foods by captive orangutans (Pongo sp). Repeated exposures of food (novel, at first) did not cause an increase of acceptance of food; in other words, the orangutans did not start to eat a food item after being exposed to that food more often, but repeated exposures of food increased consumption (i.e. quantity). After repeated exposures, the orangutans also became gradually more familiar with the food, decreasing their explorative behaviour. The presence of co-feeding conspecifics resulted in an increased acceptance of the novel food by orangutans, and they ate a larger amount of said foods than when alone. Repeated exposure and sociality may benefit rehabilitant great apes in augmenting and diversifying diet and, once practiced before release, may accelerate an individuals' adaptation to their new habitat, improving survival chances. Great ape rescue, rehabilitation and reintroduction require large financial and logistic investments; however, their effectiveness may be improved at low cost and low effort through the suggested measures.

Speech-like rhythm in a voiced and voiceless orangutan call.

The evolutionary origins of speech remain obscure. Recently, it was proposed that speech derived from monkey facial signals which exhibit a speech-like rhythm of ∼5 open-close lip cycles per second. In monkeys, these signals may also be vocalized, offering a plausible evolutionary stepping stone towards speech. Three essential predictions remain, however, to be tested to assess this hypothesis' validity; (i) Great apes, our closest relatives, should likewise produce 5Hz-rhythm signals, (ii) speech-like rhythm should involve calls articulatorily similar to consonants and vowels given that speech rhythm is the direct product of stringing together these two basic elements, and (iii) speech-like rhythm should be experience-based. Via cinematic analyses we demonstrate that an ex-entertainment orangutan produces two calls at a speech-like rhythm, coined "clicks" and "faux-speech." Like voiceless consonants, clicks required no vocal fold action, but did involve independent manoeuvring over lips and tongue. In parallel to vowels, faux-speech showed harmonic and formant modulations, implying vocal fold and supralaryngeal action. This rhythm was several times faster than orangutan chewing rates, as observed in monkeys and humans. Critically, this rhythm was seven-fold faster, and contextually distinct, than any other known rhythmic calls described to date in the largest database of the orangutan repertoire ever assembled. The first two predictions advanced by this study are validated and, based on parsimony and exclusion of potential alternative explanations, initial support is given to the third prediction. Irrespectively of the putative origins of these calls and underlying mechanisms, our findings demonstrate irrevocably that great apes are not respiratorily, articulatorilly, or neurologically constrained for the production of consonant- and vowel-like calls at speech rhythm. Orangutan clicks and faux-speech confirm the importance of rhythmic speech antecedents within the primate lineage, and highlight potential articulatory homologies between great ape calls and human consonants and vowels.

Orangutans (Pongo spp.) may prefer tools with rigid properties to flimsy tools.

Preference for tools with either rigid or flexible properties was explored in orangutans (Pongo spp.) through an extension of D. J. Povinelli, J. E. Reaux, and L. A. Theall's (2000) flimsy-tool problem. Three captive orangutans were presented with three unfamiliar pairs of tools to solve a novel problem. Although each orangutan has spontaneously used tools in the past, the tools presented in this study were novel to the apes. Each pair of tools contained one tool with rigid properties (functional) and one tool with flimsy properties (nonfunctional). Solving the problem required selection of a rigid tool to retrieve a food reward. The functional tool was selected in nearly all trials. Moreover, two of the orangutans demonstrated this within the first test trials with each of the three tool types. Although further research is required to test this statistically, it suggests either a preexisting preference for rigid tools or comprehension of the relevant features required in a tool to solve the task. The results of this study demonstrate that orangutans can recognize, or learn to recognize, relevant tool properties and can choose an appropriate tool to solve a problem.

Reproductive life history traits of female orangutans (Pongo spp.).

Data from wild populations demonstrate that orangutans have the slowest life history of all the great apes. In this chapter, we provide an overview of reproduction and life history traits of female orangutans in the wild and captivity. This comparison of wild and captive data illustrates the variability that exists for orangutans. Wild orangutan females first reproduce at a mean age of 15.4 years, with an age range of 13-18 years, and they have a mean interbirth interval of 9.3 years. Wild male orangutans are conservatively estimated to live at least 58 years, and 53 years for females [1], and to date, there is no evidence to suggest that wild orangutans experience reproductive senescence. We use captive data from 2,566 individuals to show that in captivity orangutan females regularly begin reproducing at the age of 7 and have interbirth intervals that can be shorter than 1 year. We provide additional data that describe the onset and normalization of menses in a young adolescent orangutan as well as the reproductive cycles of three adult females of different ages. Although captive females routinely cycle and reproduce throughout much of their lifespan, age at last reproduction in captivity is 41, which is well before maximum female lifespan. To date, longevity in the wild and in captivity appears equivalent [2]. The reasons for the presence of a postreproductive lifespan in captivity as opposed to its absence in wild populations may be related to management issues. The above results indicate a need for more detailed comparisons between wild and captive orangutans using similar methodologies.