Robert W. Shumaker

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.

Primate energy expenditure and life history

Significance Measurements of daily energy expenditure indicate that primates, including humans, expend only half of the calories expected for mammals of similar body size. As energy expenditure is central to organismal biology, these results hold important implications for life history, evolutionary biology, and foraging ecology for primates and other mammals. Specifically, we show that primates’ remarkably low metabolic rates account for their distinctively slow rates of growth, reproduction, and aging. 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.

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.

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 820u2009kcal 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.

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.

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.

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.

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.

Documenting orang-utan sleep architecture: sleeping platform complexity increases sleep quality in captive Pongo

Of the extant primates, only 20 non-human species have been studied by sleep scientists. Notable sampling gaps exist, including large-bodied hominoids such as gorillas (Gorilla gorilla), orang-utans (Pongo spp.) and bonobos (Pan paniscus), for which data have been characterized as high priority. Here, we report the sleep architecture of three female and two male orang-utans housed at the Indianapolis Zoo. Sleep states were identified by scoring correlated behavioural signatures (e.g., respiration, gross body movement, muscle atonia, random eye movement, etc.). The captive orang-utans were focal subjects for a total of 70 nights (1013 h) recorded. We found that orang-utans slept an average of 9.11 h (range 5.85–11.2 h) nightly and were characterized by an average NREM of 8.03 h (range 5.47–10.2 h) and REM of 1.11 (range: 0.38–2.2 h) per night. In addition, using a sleeping platform complexity index (SPCI) we found that individuals that manufactured and slept in more complex beds were characterized by higher quality sleep. Sleep fragmentation (the number of brief awakenings greater than 2 min per hour), arousability (number of motor activity bouts per hour), and total time awake per night were reduced by greater quality sleep environments. Therefore, comfortable sleeping environments reduced arousability and improve sleep quality in captive orang-utans. These results support Fruth & Hohmann’s (1996) hypothesis, which purported that the tree-limb-to-sleeping platform transition in Miocene apes improved sleep quality.

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.