Scientific activism to protect the world's primates and their environments from extinction: Introduction to the special issue.

Nonhuman primates and their habitats are facing an impending extinction crisis. Approximately 69% of primate species are listed by the International Union for Conservation of Nature as threatened and 93% have declining populations. Human population growth (expected to reach 10.9 billion by the year 2100), the unsustainable demands of a small number of consumer nations for forest-risk commodities, deforestation and habitat conversion, the expansion of roads and rail networks, cattle ranching, the hunting and trapping of wild primate populations, and the potential spread of infectious diseases are among the primary drivers of primate population decline. Climate change will only exacerbate the current situation. The time to act to protect primate populations is now! In this special issue of the American Journal of Primatology, we present a series of commentaries, formulated as "Action Letters." These are designed to educate and inform primatologists, conservation biologists, wildlife ecologists, political leaders, and global citizens about the conservation challenges faced by particular primate taxa and particular world regions, and present examples of specific actions that one can take, individually and collectively, to promote the persistence of wild primate populations and environmental justice for local human populations and impacted ecological communities. As scientists, researchers, and educators, primatologists are in a unique position to lead local, national, and international efforts to protect biodiversity. In this special issue, we focus on primates of the Brazilian Amazon, lemurs of northeast Madagascar, Temminck's red colobus monkey (Piliocolobus badius temminckii), night monkeys (Aotus spp.), long-tailed macaques (Macaca fascicularis), the primate pet trade, and professional capacity building to foster conservation awareness and action. We encourage primatologists, regardless of their research focus, to engage in both advocacy and activism to protect wild primate populations worldwide.

Population densities of Hylobates agilis in forests with different disturbance histories in Ulu Muda Forest Reserve, Malaysia.

Small ape habitat throughout Malaysia is rapidly being lost, degraded, and fragmented, and the effects of these changes on the abundance on this taxon are currently unknown. This study assessed the group density of Hylobates agilis in virgin forest, previously logged forest (1960s-1990s), and recently logged forest (2015-2017) of the Ulu Muda Forest Reserve (UMFR), Kedah, Malaysia. We conducted fixed-point active acoustic triangulation at nine survey areas to estimate group density. We used vegetation "speed plots" and satellite imagery to quantify habitat characteristics and used model selection to identify ecological predictors of group density variation. The estimated group density of H. agilis in UMFR was 4.03 ± 0.14 groups km-2 , with an estimated total of 2927 ± 102 groups in areas below 450 m a.s.l. in UMFR. Group density did not differ significantly among habitat types. The best ecological predictors for group density were canopy cover and proportion of deforested area. Areas with recent deforestation were associated with relatively high group densities, suggesting compression of the populations persisting in these habitat types. The consistently high group densities detected in all forest types emphasizes the importance of degraded forest as habitat for H. agilis. Because of the threats to small apes in Malaysia, and the uncertain status of most populations, we recommend a nationwide population census and regular monitoring to inform conservation planning and implementation. Most urgently, we call for immediate and permanent protection of UMFR and other forests in the Greater Ulu Muda landscape to protect the globally significant populations of H. agilis, as well as other charismatic and threatened megafauna, birds, and flora in the area.

The human-primate interface in the New Normal: Challenges and opportunities for primatologists in the COVID-19 era and beyond.

The emergence of SARS-CoV-2 in late 2019 and human responses to the resulting COVID-19 pandemic in early 2020 have rapidly changed many aspects of human behavior, including our interactions with wildlife. In this commentary, we identify challenges and opportunities at human-primate interfaces in light of COVID-19, focusing on examples from Asia, and make recommendations for researchers working with wild primates to reduce zoonosis risk and leverage research opportunities. First, we briefly review the evidence for zoonotic origins of SARS-CoV-2 and discuss risks of zoonosis at the human-primate interface. We then identify challenges that the pandemic has caused for primates, including reduced nutrition, increased intraspecific competition, and increased poaching risk, as well as challenges facing primatologists, including lost research opportunities. Subsequently, we highlight opportunities arising from pandemic-related lockdowns and public health messaging, including opportunities to reduce the intensity of problematic human-primate interfaces, opportunities to reduce the risk of zoonosis between humans and primates, opportunities to reduce legal and illegal trade in primates, new opportunities for research on human-primate interfaces, and opportunities for community education. Finally, we recommend specific actions that primatologists should take to reduce contact and aggression between humans and primates, to reduce demand for primates as pets, to reduce risks of zoonosis in the context of field research, and to improve understanding of human-primate interfaces. Reducing the risk of zoonosis and promoting the well-being of humans and primates at our interfaces will require substantial changes from "business as usual." We encourage primatologists to help lead the way.

Are social media reports useful for assessing small ape occurrence? A pilot study from Peninsular Malaysia.

Citizen science-based research has been used effectively to estimate animal abundance and breeding patterns, to monitor animal movement, and for biodiversity conservation and education. Here, we evaluate the feasibility of using social media observations to assess the distribution of small apes in Peninsular Malaysia. We searched for reports of small ape observations in Peninsular Malaysia on social media (e.g., blogs, Facebook, Instagram, Twitter, YouTube, iNaturalist, etc.), and also used online, radio, print messaging, and word of mouth to invite citizen scientists such as birders, amateur naturalists, hikers, and other members of the public to provide information about small ape observations made during their activities. These reports provided new information about the occurrence of all three species of small apes (Hylobates agilis, Hylobates lar, and Symphalangus syndactylus) in Peninsular Malaysia. Social media users reported observations of small apes in almost every state. Despite the fact that small apes are believed to occur primarily in the interior of large forested areas, most observations were from fairly small (<100 km2 ) forests near areas of high traffic and high human population (roads and urban areas). This suggests that most outdoor enthusiasts primarily visit well-traveled and easily accessible areas, which results in biased sampling if only incidental observations reported on social media are used. A more targeted approach specifically soliciting reports from citizen scientists visiting large, less-accessible forests may result in better sampling in these habitats. Social media reports indicated the presence of small apes in at least six habitats where they had not been previously reported. We verified the reported data based on whether reports included a date, location, and uploaded photographs, videos and/or audio recordings. Well-publicized citizen science programs may also build awareness and enthusiasm about the conservation of vulnerable wildlife species.

Abrupt Decline in a Protected Population of Siamangs (Symphalangus syndactylus) in Southern Sumatra.

Between 2011 and 2016, approximately 50% of siamangs in the Way Canguk Research Area disappeared, including members of 7 of 12 habituated groups. Demographic data from 1998 to 2015 confirm that the population decline in the habituated groups reflects a larger trend in the local population. There was no evidence of hunting of primates in the area, and ecological data do not suggest substantial changes in food availability or predation pressure during this period. From 2011 to 2014, we monitored the habituated groups only intermittently, and most deaths or disappearances were not observed. However, in 2014-2016, we monitored some groups more intensively, and observed 2 individuals with symptoms including whitened skin on the face, hands, and abdomen, hair loss, swelling of the face, frequent scratching, and lethargy. One affected individual disappeared days after this observation, while the other survived. The spatiotemporal pattern of disappearances in the habituated groups was consistent with that expected if the deaths resulted from disease transmission among neighbouring groups. Thus, the available evidence, while preliminary, suggests that a local disease epizootic may have been a factor driving the population decline. We recommend that researchers establish monitoring protocols to better understand primate disease epidemiology and to guide conservation management.

Changes in fecal estrogen levels and sexual behavior in captive sichuan snub-nosed monkeys (Rhinopithecus roxellana) following a male replacement.

Rhinopithecus roxellana are generally seasonal breeders, although copulation can occur throughout the year. Previous studies suggest that estradiol modulates female sexual behavior during the mating season. However, the effects of social context on estrogen levels and behavior have not been fully explored. We studied the relationship between sexual behaviors and fecal estrogens in a group of captive R. roxellana during a period of social instability. We collected behavioral data for six months and collected fecal samples at 2-3-day intervals for four months spanning the mating and nonmating seasons, and analyzed fecal estrogen levels via RIA. Females showed clear cyclic solicitation and copulation peaks in the mating season, which corresponded with sharp peaks in fecal estrogens. During the nonmating season, solicitation rates, copulation rates, and fecal estrogens were generally low. However, one nonpregnant female displayed a sharp peak in solicitations, copulations, and estrogens during the nonmating season 10-14 days after a male replacement. Our results provide preliminary evidence that social and behavioral changes affect estrogen levels in R. roxellana.

Responses of Javan Gibbon (Hylobates moloch) groups in submontane forest to monthly variation in food availability: evidence for variation on a fine spatial scale.

Primates tend to prefer specific plant foods, and primate home ranges may contain only a subset of food species present in an area. Thus, primate feeding strategies should be sensitive to the phenology of specific species encountered within the home range in addition to responding to larger scale phenomena such as seasonal changes in rainfall or temperature. We studied three groups of Javan gibbons (Hylobates moloch) in the Gunung Halimun-Salak National Park, Indonesia from April 2008 to March 2009 and used general linear mixed models (GLMM) and a model selection procedure to investigate the effects of variation in fruit and flower availability on gibbon behavior. Preferred foods were defined as foods that are overselected relative to their abundance, while important food species were those that comprised >5% of feeding time. All important species were also preferred. Season and measurements of flower and fruit availability affected fruit-feeding time, daily path lengths (DPL), and dietary breadth. Models that included the availability of preferred foods as independent variables generally showed better explanatory power than models that used overall fruit or flower availability. For one group, fruit and preferred fruit abundance had the strongest effects on diets and DPL in the models selected, while another group was more responsive to changes in flower availability. Temporal variation in plant part consumption was not correlated in neighboring groups. Our results suggest that fine-scale local factors are important determinants of gibbon foraging strategies.

Diet and ranging behavior of the endangered Javan gibbon (Hylobates moloch) in a submontane tropical rainforest.

Altitude influences forest structure and food abundance and distribution, which in turn affect primate feeding and ranging patterns. Javan gibbons (Hylobates moloch) are endemic to forests spanning a broad range of altitudes on Java, Indonesia. Most information about Javan gibbon behavior comes from studies in lowland forests, while the vast majority of wild gibbons remaining inhabit hill and lower montane forests. We studied the diets, activity patterns, and ranging behavior of three gibbon groups in hill/lower montane (950-1,100 m asl) forest in the Gunung Halimun-Salak National Park (GHSNP) from April 2008 to March 2009. The mean home range size was 37 ha and the mean daily path length was 1,180 m. The study groups spent 36% of time feeding, 41% resting, 15% traveling, 6% engaging in social behavior, and 2% in aggressive interactions. Fruit was the most important food (63% of feeding time) followed by leaves (24%), and flowers (12%). Our results suggest that Javan gibbons in higher elevation habitats have substantially larger home ranges than lowland populations, despite broad similarity in their activity budgets and diets. Conservation managers should consider the effects of altitude and habitat quality on gibbon ranging behavior when developing habitat corridors, selecting sites for translocation or reintroduction projects, and designating and managing protected areas.

Flowers are an important food for small apes in southern Sumatra.

Flowers are included in the diets of many primates, but are not generally regarded as making an important contribution to primate energy budgets. However, observations of a number of lemur, platyrrhine, and cercopithecine populations suggest that some flower species may function as key primate fallback foods in periods of low abundance of preferred foods (generally ripe fruits), and that flowers may be preferred foods in some cases. I report heavy reliance on flowers during some study months for a siamang (Symphalangus syndactylus) population in southern Sumatra. Siamangs at Way Canguk spent 12% of feeding time eating flowers from October 2000 to August 2002, and in 1 month flower-feeding time exceeded 40% of total feeding time. The overall availabilities of fig and nonfig fruits, flowers, and new leaves in the study area were not significant predictors of the proportion of time that siamangs spent consuming any plant part. However, flower-feeding time was highest in months when nonfig fruit-feeding time was lowest, and a switch from heavy reliance on fruit to substantial flower consumption was associated with a shift in activity patterns toward reduced energy expenditure, which is consistent with the interpretation that flowers may function as a fallback food for Way Canguk siamangs. Hydnocarpus gracilis, a plant from which siamangs only consume flowers, was the third-most-commonly consumed plant at Way Canguk (after Ficus spp. and Dracontomelon dao), and flowers from this plant were available in most months. It is possible that relatively high local availability of these important siamang plant foods is one factor promoting high siamang density in the study area.

The effects of lactation and infant care on adult energy budgets in wild siamangs (Symphalangus syndactylus).

In mammals with biparental care of offspring, males and females may bear substantial energetic costs of reproduction. Adult strategies to reduce energetic stress include changes in activity patterns, reduced basal metabolic rates, and storage of energy prior to a reproductive attempt. I quantified patterns of behavior in five groups of wild siamangs (Symphalangus syndactylus) to detect periods of high energetic investment by adults and to examine the relationships between infant care and adult activity patterns. For females, the estimated costs of lactation peaked at around infant age 4-6 months and were low by infant age 1 year, whereas the estimated costs of infant-carrying peaked between ages 7 and 12 months, and approached zero by age 16 months. There was a transition from primarily female to male care in the second year of life in some groups. Females spent significantly less time feeding during lactation than during the later stages of infant care, suggesting that female siamangs do not use increased food intake to offset the costs of lactation. Female feeding time was highest between infant ages 16 and 21 months, a period of relatively low female investment in the current offspring that coincided with the period of highest male investment in infant care. This suggests that male care may reduce the costs of infant care for females in the later stages of a reproductive attempt. The female energy gain resulting from male care was likely invested in somatic maintenance and future reproduction, rather than the current offspring.

Patterns of dispersal in Sumatran siamangs (Symphalangus syndactylus): preliminary mtDNA evidence suggests more frequent male than female dispersal to adjacent groups.

Gibbons of both sexes have been observed emigrating from their natal groups, but the consequences of dispersal in gibbons are poorly understood, and it is unclear whether these are the same for both sexes. I sequenced a 350-bp fragment of mitochondrial DNA from 18 adults in seven siamang (Symphalangus syndactylus) groups at the Way Canguk Research Station in southern Sumatra to assess patterns of matrilineal relatedness among and within siamang groups, and to assess their fit with different patterns of sex-specific dispersal. A total of 11 haplotypes were identified in the seven study groups; 50% of adult males in five contiguous groups shared a haplotype with a member of an immediately adjacent group, whereas only 16.7% of females shared a haplotype with a neighbor. The apparent difference persisted if only same-sex individuals were considered (37.5% of males vs. 0% of females). Four of the seven study groups contained two adult males and a single adult female. In three multimale groups, the three adults all had different haplotypes, suggesting that neither male was the retained adult offspring of the female, whereas in the fourth group, the haplotype of one male was identical with that of the adult female. The high diversity of haplotypes and the absence of clustering among female haplotypes in the study neighborhood suggest that female dispersal to territories adjacent to the natal group may be relatively rare. The presence of some clustering of male haplotypes suggests that shorter dispersal distances may be more common in males.