Flanged males have higher reproductive success in a completely wild orangutan population.

Male orangutans (Pongo spp.) exhibit bimaturism, an alternative reproductive tactic, with flanged and unflanged males displaying two distinct morphological and behavioral phenotypes. Flanged males are larger than unflanged males and display secondary sexual characteristics which unflanged males lack. The evolutionary explanation for alternative reproductive tactics in orangutans remains unclear because orangutan paternity studies to date have been from sites with ex-captive orangutans, provisioning via feeding stations and veterinary care, or that lack data on the identity of mothers. Here we demonstrate, using the first long-term paternity data from a site free of these limitations, that alternative reproductive tactics in orangutans are condition-dependent, not frequency-dependent. We found higher reproductive success by flanged males than by unflanged males, a pattern consistent with other Bornean orangutan (Pongo pygmaeus) paternity studies. Previous paternity studies disagree on the degree of male reproductive skew, but we found low reproductive skew among flanged males. We compare our findings and previous paternity studies from both Bornean and Sumatran orangutans (Pongo abelii) to understand why these differences exist, examining the possible roles of species differences, ecology, and human intervention. Additionally, we use long-term behavioral data to demonstrate that while flanged males can displace unflanged males in association with females, flanged males are unable to keep other males from associating with a female, and thus they are unable to completely mate guard females. Our results demonstrate that alternative reproductive tactics in Bornean orangutans are condition-dependent, supporting the understanding that the flanged male morph is indicative of good condition. Despite intense male-male competition and direct sexual coercion by males, female mate choice is effective in determining reproductive outcomes in this population of wild orangutans.

Mother-offspring proximity maintenance as an infanticide avoidance strategy in bornean orangutans (Pongo pygmaeus wurmbii).

Sexually-selected infanticide by males is widespread across primates. Maternal protection is one of many infanticide avoidance strategies employed by female primates. Bornean orangutan (Pongo pygmaeus wurmbii) mothers with younger offspring are less social with males than mothers with older offspring. Additionally, the distance between a mother and offspring decreases in the presence of male conspecifics, but not female conspecifics. We hypothesized that mothers are responsible for the change in mother-offspring proximity when males are present. Using a year of behavioral data from orangutans in Gunung Palung National Park, we tested whether the Hinde Index, a ratio of the number of approaches and leaves between two individuals, was indicative of mother or offspring proximity maintenance across different social groupings. The semi-solitary social organization of orangutans allows us to observe different social groupings. We found that the mother-offspring Hinde Index was typically indicative of offspring maintenance of proximity. However, the presence of male conspecifics was associated with an increase in the Hinde Index which indicates that mothers are responsible for the decrease in mother-offspring distance when males are present. The decrease in mother-offspring distances and increase in Hinde Index when males are present indicates that mothers react to the presence of males in a protective manner. We suggest this may be an infanticide avoidance behavior by mother orangutans.

A composite menstrual cycle of captive orangutans, with associated hormonal and behavioral variability.

Knowledge of species-typical reproductive endocrinology profiles is crucial for testing hypotheses pertaining to the evolutionary history, reproductive parameters, and life history of a species, and for managing the well-being of individual animals in human care. Large-scale empirical measurements of ovarian hormones, however, are rare for most primate species, including orangutans. In this study, we used enzyme immunoassays (EIA) to quantify estrogen (estrone conjugates; E1 C) and progesterone (pregnanediol-3-glucuronide; PdG) levels for 98 cycles in 7 cycling zoo-housed female orangutans (10-43 years old). We use a subset of these cycles (N = 44) to create the first composite menstrual cycle for orangutans, which serves as a valuable baseline for future comparative analyses and veterinary considerations. Similar to previous studies, we determined the mean ovarian cycle length of orangutans to be 29.7 days (N = 98 cycles), although we illustrate evidence of both intra- and interindividual variation in ovarian steroid production. Given that this study took place in captivity, we consider how energetic and psychosocial aspects of the zoo environment, such as greater food availability and potential stress, may affect the reproductive physiology and sexual behavior of these females. Furthermore, we discuss the role that age and genetic background may play in producing variability. Finally, we test whether ovarian hormone levels correlate with the reproductive behaviors of these female orangutans using associated behavioral data. Our results suggest that matings are more common during the periovulatory period than outside of it, but do not support a consistent link between hormonal indices of fecundability and mating behaviors in these individuals.

Application of a parallel laser apparatus to measure forearms and flanges of wild Bornean orangutans (Pongo pygmaeus wurmbii).

We constructed a parallel laser photogrammetry apparatus constructed from commercially available parts, and measured forearm lengths and flange widths of 16 wild Bornean orangutans. Our objectives were to validate our method and apparatus, discuss issues encountered, and construct preliminary growth curves. For adult males, we also compared flange width to forearm length as a way to investigate the relationship between body size and flange development. We used a camera cage around a DSLR camera, on top of which we attached two parallel green lasers. We estimated error with repeatability, accuracy, and interobserver reliability measures, and measured forearm lengths in three different ways to see which was most consistent. The longest forearm measure was the most repeatable (CV = 1.64%), and was similar to flange repeatability (3.50%). Accuracy measurements of a known object were high (error = 0.25%), and Interobserver discrepancy low (3.74%). Laser spacing increased with distance to the subject, but we corrected for this using calibration photos after each session. We transparently discuss the issues we encountered with the aim that this accessible method can help expand the use of laser photogrammetry. Preliminary measurements show that male flange widths and forearm length do not reliably increase in tandem, and that female growth plateaus at around the age at first birth (15 years old). We conclude with suggested improvements to the apparatus and method to ensure the lasers remain parallel.

Sociality predicts orangutan vocal phenotype.

In humans, individuals' social setting determines which and how language is acquired. Social seclusion experiments show that sociality also guides vocal development in songbirds and marmoset monkeys, but absence of similar great ape data has been interpreted as support to saltational notions for language origin, even if such laboratorial protocols are unethical with great apes. Here we characterize the repertoire entropy of orangutan individuals and show that in the wild, different degrees of sociality across populations are associated with different 'vocal personalities' in the form of distinct regimes of alarm call variants. In high-density populations, individuals are vocally more original and acoustically unpredictable but new call variants are short lived, whereas individuals in low-density populations are more conformative and acoustically consistent but also exhibit more complex call repertoires. Findings provide non-invasive evidence that sociality predicts vocal phenotype in a wild great ape. They prove false hypotheses that discredit great apes as having hardwired vocal development programmes and non-plastic vocal behaviour. Social settings mould vocal output in hominids besides humans.

Effectiveness of 20 years of conservation investments in protecting orangutans.

Conservation strategies are rarely systematically evaluated, which reduces transparency, hinders the cost-effective deployment of resources, and hides what works best in different contexts. Using data on the iconic and critically endangered orangutan (Pongo spp.), we developed a novel spatiotemporal framework for evaluating conservation investments. We show that around USD 1 billion was invested between 2000 and 2019 into orangutan conservation by governments, nongovernmental organizations, companies, and communities. Broken down by allocation to different conservation strategies, we find that habitat protection, patrolling, and public outreach had the greatest return on investment for maintaining orangutan populations. Given the variability in threats, land-use opportunity costs, and baseline remunerations in different regions, there were differential benefits per dollar invested across conservation activities and regions. We show that although challenging from a data and analysis perspective, it is possible to fully understand the relationships between conservation investments and outcomes and the external factors that influence these outcomes. Such analyses can provide improved guidance toward a more effective biodiversity conservation. Insights into the spatiotemporal interplays between the costs and benefits driving effectiveness can inform decisions about the most suitable orangutan conservation strategies for halting population declines. Although our study focuses on the three extant orangutan species of Sumatra and Borneo, our findings have broad application for evidence-based conservation science and practice worldwide.

Wild Bornean orangutan (Pongo pygmaeus wurmbii) feeding rates and the Marginal Value Theorem.

The Marginal Value Theorem (MVT) is an integral supplement to Optimal Foraging Theory (OFT) as it seeks to explain an animal's decision of when to leave a patch when food is still available. MVT predicts that a forager capable of depleting a patch, in a habitat where food is patchily distributed, will leave the patch when the intake rate within it decreases to the average intake rate for the habitat. MVT relies on the critical assumption that the feeding rate in the patch will decrease over time. We tested this assumption using feeding data from a population of wild Bornean orangutans (Pongo pygmaeus wurmbii) from Gunung Palung National Park. We hypothesized that the feeding rate within orangutan food patches would decrease over time. Data included feeding bouts from continuous focal follows between 2014 and 2016. We recorded the average feeding rate over each tertile of the bout, as well as the first, midpoint, and last feeding rates collected. We did not find evidence of a decrease between first and last feeding rates (Linear Mixed Effects Model, n = 63), between a mid-point and last rate (Linear Mixed Effects Model, n = 63), between the tertiles (Linear Mixed Effects Model, n = 63), nor a decrease in feeding rate overall (Linear Mixed Effects Model, n = 146). These findings, thus, do not support the MVT assumption of decreased patch feeding rates over time in this large generalist frugivore.

Sociosexual behavioral patterns involving nulliparous female orangutans (Pongo sp.) reflect unique challenges during the adolescent period.

The primate adolescent period is characterized by a series of changes in physiology, behavior, and social relationships. Orangutans have the slowest life history and the longest period of dependency of all primates. As members of a semisolitary species with high levels of sexual coercion, adolescent female orangutans face a unique combination of challenges when achieving independence from their mother. This study examined the mating behavior of adolescent female orangutans and compared it with that of adult females to assess whether mating behavior reflects distinct strategies at these different points in the life cycle. Data were collected in Gunung Palung National Park on the island of Borneo over 20 years. Mating events from adolescent (n = 19) and adult females (n = 26) were scored and compared. Adolescent female mating events had significantly higher mating scores (indicating more proceptivity) than those of adult females (ß = 1.948, p = .001). Adolescent females also engaged in elaborate sociosexual interactions with different flanged males, behaviors that were never observed during mating events of adult females. These interactions involved characteristic behavior on the part of both the adolescent females and the flanged males. Given these findings and the documentation of similar accounts of adolescent female-flanged male mating from the island of Sumatra, we propose that adolescent female orangutans display distinctive behavioral repertoires throughout the genus Pongo which serves to overcome male ambivalence toward nulliparous females, establish familiarity, and evaluate coercive tendencies in flanged males. We suggest that these behavioral patterns are an integral part of female social development in a female philopatric, but highly dispersed species where consistent social support is absent after ranging independence is achieved.

Reducing the primate pet trade: Actions for primatologists.

This commentary emerged from a panel presentation at the International Primatological Society Congress in Nairobi, Kenya, 2018. The goal was to provide regional updates on the status of primate removal from habitat countries, especially for the pet trade, and develop guidelines that could help primatologists address this critical problem. The trade in live primates includes those used as pets, in entertainment, and as subjects of biomedical experimentation, but here we focus on those primates destined for the pet trade. Such transactions are a hugely lucrative business, impacting hundreds of thousands of individuals annually and affecting the survival of wild populations. Being intimately familiar with primate social behavior, life history and biology, primatologists, whether they work with captive or wild primates, are in a unique position to understand the nature of the trade and attempt to counter its effects. In addition to updating the status of the primate pet trade, we provide recommendations that may help primatologists formulate a plan to deal, locally and regionally, with illegal trafficking in live primates. General guidelines include increasing awareness of local customs, policies and laws; developing collaborative research opportunities for local people; engaging in training/informational opportunities; and instructing on how to take action when encountering illegally-trafficked primates.

Possible Male Infanticide in Wild Orangutans and a Re-evaluation of Infanticide Risk.

Infanticide as a male reproductive tactic is widespread across mammals, and is particularly prevalent in catarrhine primates. While it has never been observed in wild orangutans, infanticide by non-sire males has been predicted to occur due to their extremely long inter-birth intervals, semi-solitary social structure, and the presence of female counter-tactics to infanticide. Here, we report on the disappearance of a healthy four-month-old infant, along with a serious foot injury suffered by the primiparous mother. No other cases of infant mortality have been observed at this site in 30 years of study. Using photographic measurements of the injury, and information on the behavior and bite size of potential predators, we evaluate the possible causes of this injury. The context, including the behavior of the female and the presence of a new male at the time of the injury, lead us to conclude that the most likely cause of the infant loss and maternal injury was male infanticide. We suggest that in orangutans, and other species where nulliparous females are not preferred mates, these females may be less successful at using paternity confusion as an infanticide avoidance tactic, thus increasing the likelihood of infanticide of their first-born infants.

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

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

Population-specific use of the same tool-assisted alarm call between two wild orangutan populations (Pongo pygmaeus wurmbii) indicates functional arbitrariness [corrected].

Arbitrariness is an elementary feature of human language, yet seldom an object of comparative inquiry. While arbitrary signals for the same function are relatively frequent between animal populations across taxa, the same signal with arbitrary functions is rare and it remains unknown whether, in parallel with human speech, it may involve call production in animals. To investigate this question, we examined a particular orangutan alarm call - the kiss-squeak - and two variants - hand and leaf kiss-squeaks. In Tuanan (Central Kalimantan, Indonesia), the acoustic frequency of unaided kiss-squeaks is negatively related to body size. The modified variants are correlated with perceived threat and are hypothesized to increase the perceived body size of the sender, as the use of a hand or leaves lowers the kiss-squeak's acoustic frequency. We examined the use of these variants in the same context in another orangutan population of the same sub-species and with partially similar habitat at Cabang Panti (West Kalimantan, Indonesia). Identical analyses of data from this site provided similar results for unaided kiss-squeaks but dissimilar results for hand and leaf kiss-squeaks. Unaided kiss-squeaks at Cabang Panti were emitted as commonly and showed the same relationship to body size as in Tuanan. However, at Cabang Panti, hand kiss-squeaks were extremely rare, while leaf-use neither conveyed larger body size nor was related to perceived threat. These findings indicate functional discontinuity between the two sites and therefore imply functional arbitrariness of leaf kiss-squeaks. These results show for the first time the existence of animal signals involving call production with arbitrary function. Our findings are consistent with previous studies arguing that these orangutan call variants are socially learned and reconcile the role of gestures and calls within evolutionary theories based on common ancestry for speech and music.

Low testosterone correlates with delayed development in male orangutans.

Male orangutans (Pongo spp.) display an unusual characteristic for mammals in that some adult males advance quickly to full secondary sexual development while others can remain in an adolescent-like form for a decade or more past the age of sexual maturity. Remarkably little is understood about how and why differences in developmental timing occur. While fully-developed males are known to produce higher androgen levels than arrested males, the longer-term role of steroid hormones in male life history variation has not been examined. We examined variation in testosterone and cortisol production among 18 fully-developed ("flanged") male orangutans in U.S. captive facilities. Our study revealed that while testosterone levels did not vary significantly according to current age, housing condition, and species origin, males that had undergone precocious development had higher testosterone levels than males that had experienced developmental arrest. While androgen variation had previously been viewed as a state-dependent characteristic of male developmental status, our study reveals that differences in the physiology of early and late developing males are detectable long past the developmental transition and may instead be trait-level characteristics associated with a male's life history strategy. Further studies are needed to determine how early in life differences in testosterone levels emerge and what consequences this variation may have for male behavioral strategies.

Bornean orangutans on the brink of protein bankruptcy.

Protein is a limiting resource that is essential to the growth, maintenance and reproduction of tropical frugivores, yet few studies have examined how wild animals maintain protein balance. During chronic periods of fruit scarcity, Bornean orangutans (Pongo pygmaeus) often catabolize their own fat reserves despite unusually low metabolic requirements. Such energy deficits suggest a marginal existence, and raise the possibility that orangutans also endure periods of negative protein balance. To test this hypothesis, we conducted the first study of protein cycling in a wild primate. Our five year analysis of urinary metabolites revealed evidence of protein recycling when fruit was scarce. During these periods, orangutans consumed more leaves and bark, proteinaceous but tough foods that yielded a mean daily intake of 1.4 g protein kg(-1) metabolic mass. Such an amount is inadequate for humans and one-tenth the intake of mountain gorillas, but sufficient to avert, perhaps narrowly, a severe protein deficit. Our findings highlight the functional and adaptive value of traits that maximize protein assimilation during periods of ecological exigency.

Infant sex predicts breast milk energy content.

During human evolutionary history, and for many around the world, breast milk is the primary source of nutritional energy for infants. Variation in breast milk quality might logically have important effects on infant health, growth, and development, yet the sources of this variation remain largely unelucidated. We quantified nutrient and energy content of breast milk from 25 healthy, well-nourished Massachusetts mothers with infants aged 2-5 months. We examined several potential sources of variation in milk quality, particularly feeding patterns, infant sex, and maternal breast growth during pregnancy. After controlling for time since last feeding, a known correlate of milk composition, we found that mothers of male infants produced milk that had 25% greater energy content than mothers of female infants (P < 0.001). Change in maternal bra cup size during pregnancy was associated with 16.17 kcal/100 ml greater energy content of milk (P = 0.009), but was not significant after taking infant sex into account. Greater nutritional investment in sons may account for the greater observed growth rates in male compared to female infants.

Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans.

Assessment of energetic condition is a critical tool for behavioral and reproductive ecologists. However, accurate quantification of energy intake and expenditure is labor-intensive, and it can be problematic for field scientists to obtain regular data on individual animals. C-peptide, a polypeptide segment of the proinsulin molecule that is secreted along with insulin in an equimolar relationship, can be measured in urine, and thus offers a potential means for the non-invasive assessment of energy balance in wild animals. Here, we validate C-peptide for the quantification of energetic condition, with specific application to wild orangutans (Pongo pygmaeus). We determined that application of urine to filter paper results in significantly lower C-peptide recoveries versus fresh samples. However, concentrations in filter paper samples were significantly correlated with fresh urine and were stable over various storage conditions and durations. We compared the C-peptide concentrations from wild orangutan urine samples with three independent measures of energetic condition: ketone bodies (urinalysis), caloric intake (nutritional biochemistry), and food availability (phenology). As expected, C-peptide concentrations were significantly lower in samples that tested positive for ketones in the field. Monthly average C-peptide concentrations of both male and female orangutans were significantly correlated with monthly determinations of energy intake and food availability. Therefore, we conclude that the collection and preservation of urine samples for C-peptide analysis are feasible under most field conditions and, in this species, presents a useful tool for assessing changes in energy balance.

Fertility and mortality patterns of captive Bornean and Sumatran orangutans: is there a species difference in life history?

Across broad taxonomic groups, life history models predict that increased ecological predictability will lead to conservative investment in reproductive effort. Within species, however, organisms are predicted to have increased reproductive rates under improved environmental conditions. It is not clear how these models apply to closely-related species. In this paper, we examine predictions from these models as applied to variability in reproductive rates between the two species of orangutans, Pongo pygmaeus (Bornean) and Pongo abelii (Sumatran). Orangutans exhibit characteristics of a "slow" life history strategy with large bodies, late age at maturity, low reproductive rates, and long lifespan. Recently, researchers proposed that Sumatran orangutans may have an even slower life history than Bornean orangutans as a result of ecological and genetic differences (Wich et al., 2004). We examined this hypothesis by studying important aspects of life history of both species under conditions of relative ecological stability, in captivity. In this large dataset, there were no significant species differences in age of first or last reproduction, completed fertility, perinatal and postnatal mortality, or female longevity. Bornean orangutans in captivity did have significantly longer interbirth intervals, and male Bornean orangutans had higher survival past maturity. Our results do not support the hypothesis that selection has led to decreased reproductive effort under conditions of increased habitat quality in Sumatra (Wich et al., 2004), and instead suggest that phenotypic flexibility may be particularly important in explaining differences between closely related species.

Radioimmunoassay of estrone conjugates from urine dried on filter paper.

Hormonal analysis of urine from free-ranging primates has been limited due to the difficulty of preserving samples under field conditions. Drying urine on filter paper is an alternative for field preservation. This study describes a new laboratory method for eluting steroids from filter paper with methanol, along with a series of experiments used to develop and validate this method. The overall elution recovery of estrone sulfate (ES) from filter paper was 86.4%. Estrone conjugate (E1C) levels in humans and captive orangutans were analyzed by radioimmunoassay (RIA). Values from samples dried on filter paper were significantly correlated with values from matched frozen samples, with elution efficiencies ranging between 97.1% and 102.4%. Creatinine (Cr) measurements from frozen urine compared to urine dried on filter paper were also significantly correlated (r=0.96) with an elution efficiency of 101.7%. After the samples were stored for 2 years, the absolute values of E1C and Cr were significantly lower but were still significantly correlated with frozen urine values. These data demonstrate the effectiveness of filter paper as a medium for preserving urinary steroid samples, and the efficiency of methanol as a solvent for eluting E1C and Cr. This method thus provides a viable alternative to the traditional procedure of freezing urine for field studies, where freezers are not available.

Orangutan cultures and the evolution of material culture.

Geographic variation in some aspects of chimpanzee behavior has been interpreted as evidence for culture. Here we document similar geographic variation in orangutan behaviors. Moreover, as expected under a cultural interpretation, we find a correlation between geographic distance and cultural difference, a correlation between the abundance of opportunities for social learning and the size of the local cultural repertoire, and no effect of habitat on the content of culture. Hence, great-ape cultures exist, and may have done so for at least 14 million years.