Sharing Space with Monkeys and Human Tolerance Are Critical Supplements to Primate Conservation, but Not Substitutes for Protected Nature Reserves: A Long-Term View from Sri Lanka, with a Reply to Rudran [2021].

Many investigators of human-monkey competition (HMC) in Sri Lanka have revealed some common threads. Except at temple and protected sites, all monkeys were considered as household or agricultural pests wherever they shared space with humans. This included the widely distributed toque macaque (Macaca sinica), the grey langur (Semnopithecus priam thersites) of the Dry Zone, and the purple-faced langur (S. vetulus) of the southwestern and central rain forests where human densities and habitat fragmentation were greatest. People sharing space with monkeys resorted to various non-lethal methods to chase monkeys away from their properties and most preferred to have monkeys removed to protected areas; such translocations have been politically popular, though contrary to ecological principles. The main cause of HMC near primate habitats has been environmental conversion to agriculture, whereas in many towns the refuse generated in the wake of widespread growing tourism lured omnivorous macaques towards human habitation and stimulated macaque population growth. While most Sri Lankans share space with monkeys reluctantly, only a minority, flouting cultural restraints, want monkeys destroyed. Nonetheless, a major threat to primate conservation has been habitat loss and the killing of monkeys, especially in the densely populated southwestern area of the island where recent surveys showed that most macaques have been wiped out. Two subspecies, S. v. nestor of the rain forest lowlands and M. s. opisthomelas of the montane forests, are Critically Endangered. Sharing space with monkeys rests on public tolerance, understanding, and empathy with monkeys. Religious concepts venerating monkeys provide fertile ground for this. Our science-based educational documentaries (n > 35), among other efforts, also have contributed to these human sentiments in Sri Lanka and globally. The trends in HMC suggest that protected nature reserves for all wildlife are more secure for primate survival than ethnoprimatology by itself would be. Rudran [Folia Primatologica 2021, DOI: 10.1159/000517176] criticized our recent publication on HMC in Sri Lanka [Dittus et al., Folia Primatologica 2019, 90: 89-108]. We consider his comments as misconstruing efforts in primate conservation through denying the importance of traditional protected areas, overlooking our achievements in educating the public and reducing HMC, as well as misunderstanding the limits of marketing monkeys to tourists as a source of income to support conservation.

Shields on Electric Posts Prevent Primate Deaths: A Case Study at Polonnaruwa, Sri Lanka.

When monkeys, such as the toque macaques (Macaca sinica) of Sri Lanka, seek food on the ground near human habitation, they may use electrical posts to escape aggression from conspecifics, dogs, or humans. Shields mounted on electrical posts prevented monkeys from reaching the electrical wires, thereby averting their electrocution: the frequency of electrocutions (n = 0) was significantly less (p < 0.001) in the 12 years after installation of the shields than in the 12 years before (n = 18). Electric shocks were either fatal (n = 14) or caused permanent injury (n = 4) (collectively referred to as electrocutions hereafter). The shields may find broader applications in other primate species and environments wherever monkeys are attracted by human food near electrical posts. Primates and other arboreal mammals also accessed live wires from trees; at known electrocution hotspots, short spans of exposed wires were insulated by encapsulating them in PVC water pipes. It was impossible, however, to prevent electrocutions from all electric supply infrastructures that put monkeys at risk. A wider use of insulated electric conductors in planning power distribution in habitats frequented by wild animals would be desirable in preventing electric shocks to wildlife.

Assessing Public Perceptions and Solutions to Human-Monkey Conflict from 50 Years in Sri Lanka.

Sri Lanka is a biodiversity hotspot with high human density that contributes to increasing human-monkey conflict (HMC). In 50 years of primate studies there, the development of HMC has been documented, and many workshops and interventions organized to ameliorate HMC. These activities prompted the present survey. In the extensive lowland dry zone of Sri Lanka, the affected nonhuman primates are the toque macaque, gray and purple-faced langurs and slender loris. We surveyed and evaluated the attitudes of rural residents towards these four species in an effort to contribute to an ethnoprimatological approach to conservation, i.e., promote a coexistence and sharing of habitat between humans and monkeys. We selected 13 villages near Polonnaruwa, located centrally in the dry zone. The four nonhuman primate species differ in their behavioral ecologies, and this influenced how frequently they were thought of as pests. Most HMC was with the macaque and gray langur, less with the purple-faced langur and least with the loris. The underlying sentiment among stakeholders towards monkeys was generally either neutral or positive. Nonetheless, the majority (80%) of people desired a translocation of the troublesome monkeys from their properties to protected areas, which is impractical. Few (< 1%) openly wanted monkeys destroyed. While a traditional reverence for monkeys provides a solid basis for science and media-based education, it also contributes to the feeding of monkeys and consequent unnatural population growth, and enhanced HMC. Public understanding of the underlying causes of HMC was poor, hindering effective solutions. A combination of a feeding ban, possibly contraceptive intervention at localized HMC trouble spots, and extensive education may be the only benign alternatives to the destruction of wild primates by a powerful minority. Coexistence through strengthening and expansion of exclusive suitable protected habitats for all wildlife is a priority.

Vitamin D status in wild toque macaques (Macaca sinica) in Sri Lanka.

The vitamin D receptor is found on most cells, including active immune cells, implying that vitamin D has important biological functions beyond calcium metabolism and bone health. Although captive primates should be given a dietary source of vitamin D, under free-living conditions vitamin D is not a required nutrient, but rather is produced in skin when exposed to UV-B light. The circulating level of 25 hydroxyvitamin D (25-OH-D) considered adequate for humans is a topic of current controversy. Levels of circulating 25-OH-D sufficient for good health for macaques and other Old World anthropoids are assumed to be the same as human values, but data from free-living animals are scant. This study reports values for 25-OH-D and the active vitamin D metabolite, 1,25-dihydroxyvitamin D (1,25[OH]2 D) for wild, forest-ranging toque macaques (Macaca sinica) in Sri Lanka. Plasma samples were obtained from eight adult males, seven juvenile males, six young nulliparous females, nine adult females not pregnant or lactating, eleven lactating adult females, and four pregnant females. Mean values for the complete sample were 61.3 ± 4.0 ng/ml for 25-OH-D and 155.6 ± 8.7 pg/ml for 1,25[OH]2 D. There were no significant differences for either metabolite among age and sex classes, nor between lactating and non-reproductive females. Values from the literature for circulating 25-OH-D in captive macaques are three times higher than those found in this wild population, however, 1,25[OH]2 D values in captive animals were similar to the wild values. The data from this study indicate that anthropoid primates exposed to extensive sunlight will have circulating values of 25-OH-D generally above 30 ng/ml, providing some support for the Endocrine Society recommendations for humans. Current dietary vitamin D supplementation of captive macaques likely exceeds requirement. This may affect metabolism and immune function, with possible consequences for macaque health and biomedical research results.

Validating skinfold thickness as a proxy to estimate total body fat in wild toque macaques (Macaca sinica) using the mass of dissected adipose tissue.

Skinfold thickness (SFT) has been used often in non-human primates and humans as a proxy to estimate fatness (% body fat). We intended to validate the relation between SFT (in recently deceased specimens) and the mass of adipose tissue as determined from dissection of fresh carcasses of wild toque macaques (Macaca sinica). In adult male and female toque macaques body composition is normally 2% adipose tissue. Calipers for measuring SFT were suitable for measuring only some subcutaneous deposits of adipose tissue but were not suitable for measuring large fat deposits within the body cavity or minor intermuscular ones. The anatomical distribution of 13 different adipose deposits, in different body regions (subcutaneous, intra-abdominal and intermuscular) and their proportional size differences, were consistent in this species (as in other primates), though varying in total mass among individuals. These consistent allometric relationships were fundamental for estimating fatness of different body regions based on SFT. The best fit statistically significant correlations and regressions with the known masses of dissectible adipose tissue were evident between the SFT means of the seven sites measured, as well as with a single point on the abdomen anterior to the umbilicus. SFT related to total fat mass and intra-abdominal fat mass in curvilinear regressions and to subcutaneous fat mass in a linear relationship. To adjust for differences in body size among individuals, and to circumvent intangible variations in total body mass allocated, for example to the gastro-intestinal contents, dissected fat mass was estimated per unit body size (length of crown-rump)(3). SFT had greater coefficients of correlation and regressions with this Fat Mass Index (g/dm(3)) than with Percent Body Fat.

Arboreal adaptations of body fat in wild toque macaques (Macaca sinica) and the evolution of adiposity in primates.

There is a paucity of information on body composition and fat patterning in wild nonhuman primates. Dissected adipose tissue from wild toque macaques (Macaca sinica) (WTM), feeding on a natural diet, accounted for 2.1% of body weight. This was far less than fatness reported for nonhuman primates raised in captivity or for contemporary humans. In WTM, fatness increased with age and diet richness, but did not differ by sex. In WTM (none of which were obese) intra-abdominal fat filled first, and "excess" fat was stored peripherally in a ratio of about 6:1. Intermuscular fat was minimal (0.1%). The superficial paunch held <15% of subcutaneous fat weight in contrast to its much larger proportions in obese humans and captive monkeys where most added fat accumulates subcutaneously. With increasing total adiposity, accumulating fat shifted in its distribution among eight different main internal and peripheral deposit areas-consistent with maintaining body balance and a low center of gravity. The available data suggest that, in arboreal primates, adaptations for agile locomotion and terminal branch feeding set constraints on the quantity and distribution of fat. The absence of a higher percentage of body fat in females and neonates (as are typical of humans) suggests that arboreal adaptations preclude the development of fat-dependent, large-brained infants and the adipose-rich mothers needed to sustain them. The lifestyle and body composition of wild primates represent a more appropriate model for early human foragers than well-fed captive monkeys do.

Transmission dynamics of Cryptosporidium infection in a natural population of non-human primates at Polonnaruwa, Sri Lanka.

Infections from Cryptosporidium parvum are of interest not only to public health, but also to wildlife conservation, particularly when humans and livestock encroach on nature and thereby increase the risk of cross-species transmissions. To clarify this risk, we used polymerase chain reaction to examine the hypervariable region of the C. parvum 18S rRNA gene in feces from three monkey species. Samples were isolated from regions where disease transmission between monkeys, livestock, and humans was likely (soiled habitat) or unlikely (clean habitat). Monkey individuals, their social groups, and different species shared multiple genotypes/isolates of C. parvum. Ecological and molecular analyses suggested that Cryptosporidium infection among Toque macaques in soiled habitats was mainly the bovine genotype C. parvum. Monkeys inhabiting clean habitat, particularly gray and purple-faced langurs, lacked Cryptosporidium species/types associated with bovines. Livestock apparently was a main source of infection for wild primates.

Prevalence of cryptosporidium and other enteric parasites among wild non-human primates in Polonnaruwa, Sri Lanka.

Cryptosporidiosis is a rapidly emerging disease in the tropics. This is the first report of Cryptosporidium and other protozoan infections (Entamoeba spp., Iodamoeba, Chilomastix, and Balantidium spp.) in wild primates that inhabit the natural forest of Sri Lanka. It is unclear if non-human primates serve as a reservoir for these parasites under certain conditions. A cross-sectional coprologic survey among 125 monkeys (89 toque macaques, 21 gray langurs, and 15 purple-faced langurs) indicated that Cryptosporidium was detected in all three primate species and was most common among monkeys using areas and water that had been heavily soiled by human feces and livestock. Most macaques (96%) shedding Cryptosporidium oocysts were co-infected with other protozoans and important anthropozoonotic gastrointestinal parasites (e.g., Enterobius and Strongyloides). The transmission of these parasites among primates in the wild may have important implications for public health as well as wildlife conservation management.

Hematology of a natural population of toque macaques (Macaca sinica) at polonnaruwa, Sri Lanka.

Hematological studies were conducted in three wild groups of toque macaques (Macaca sinica) inhabiting the Polonnaruwa Sanctuary in northeastern Sri Lanka. The macaques were temporarily trapped and anesthetized, and femoral blood was drawn from 35 males and 37 females (age range: 0.33-24.5 yr). Statistically significant (P<0.05) differences were observed by sex for total plasma proteins (PP), and by age for red blood cell (RBC) counts, hemoglobin (Hb), mean corpuscular volume (MCV), mean corpuscular Hb (MCH), mean corpuscular Hb concentration (MCHC), PP, erythrocyte sedimentation rate (ESR), differential and absolute neutrophil counts, differential lymphocyte counts, and absolute eosinophil counts. In general, the results were similar to those reported for other species of colony-bred and free-ranging macaques. However, there also were differences. First, in contrast to earlier studies of nonhuman primates, we examined the hematology of infants. Compared to other age classes, infants (<1 yr old) had lower RBC, Hb, MCHC, and ESR values, and a higher MCV. These findings were similar to those obtained in human infants. Second, we observed variations in hematology among social groups in relation to their ecology. Two groups (IH3 and M3) had ready access to water throughout the dry season (the period of sampling), whereas the third group (J) did not. The Hb, RBC, and PP values obtained in groups IH3 and M3 were similar to those reported in other macaque species. However, these parameters in group J were significantly (P<0.01) higher, which suggests that this group (representing about 26% of the sample) had been dehydrated during the dry season. Finally, two indices indicative of injury and infection--the ESR and leukocyte counts--were higher in the wild toque macaques than has been reported for other species of macaques held in captivity, and about 15% of the toque macaques sampled had extreme outlier values for these parameters; however, none were visibly ill or died. These results suggest that wild toque macaques are subject to a wide array of physical and biological insults that are unique to natural populations.

Primate population studies at Polonnaruwa. II. Heritability of body measurements in a natural population of toque macaques (Macaca sinica).

The heritability of quantitative traits, or the proportion of phenotypic variation due to additive genetic or heritable effects, plays an important role in determining the evolutionary response to natural selection. Most quantitative genetic studies are performed in the laboratory, due to difficulty in obtaining genealogical data in natural populations. Genealogies are known, however, from a unique 20-year study of toque macaques (Macaca sinica) at Polonnaruwa, Sri Lanka. Heritability in this natural population was, therefore, estimated. Twenty-seven body measurements representing the lengths and widths of the head, trunk, extremities, and tail were collected from 270 individuals. The sample included 172 offspring-mother pairs from 39 different matrilineal families. Heritabilities were estimated using traditional mother-offspring regression and maximum likelihood methods which utilize all genealogical relationships in the sample. On the common assumption that environmental (including social) factors affecting morphology were randomly distributed across families, all but two of the traits (25 of 27) were significantly heritable, with an average heritability of 0.51 for the mother-offspring analysis and 0.56 for the maximum likelihood analysis. Heritability estimates obtained from the two analyses were very similar. We conclude that the Polonnaruwa macaques exhibit a comparatively moderate to high level of heritability for body form. © 1992 Wiley-Liss, Inc.