The primate gastrointestinal tract is home to trillions of bacteria, whose composition is associated with numerous metabolic, autoimmune, and infectious human diseases. Although there is increasing evidence that modern and Westernized societies are associated with dramatic loss of natural human gut microbiome diversity, the causes and consequences of such loss are challenging to study. Here we use nonhuman primates (NHPs) as a model system for studying the effects of emigration and lifestyle disruption on the human gut microbiome. Using 16S rRNA gene sequencing in two model NHP species, we show that although different primate species have distinctive signature microbiota in the wild, in captivity they lose their native microbes and become colonized with Prevotella and Bacteroides, the dominant genera in the modern human gut microbiome. We confirm that captive individuals from eight other NHP species in a different zoo show the same pattern of convergence, and that semicaptive primates housed in a sanctuary represent an intermediate microbiome state between wild and captive. Using deep shotgun sequencing, chemical dietary analysis, and chloroplast relative abundance, we show that decreasing dietary fiber and plant content are associated with the captive primate microbiome. Finally, in a meta-analysis including published human data, we show that captivity has a parallel effect on the NHP gut microbiome to that of Westernization in humans. These results demonstrate that captivity and lifestyle disruption cause primates to lose native microbiota and converge along an axis toward the modern human microbiome.human microbiome | primate microbiome | dietary fiber | dysbiosis | microbial ecology

The mammalian gastrointestinal (GI) tract is home to trillions of bacteria that play a substantial role in host metabolism and immunity. While progress has been made in understanding the role that microbial communities play in human health and disease, much less attention has been given to host-associated microbiomes in nonhuman primates (NHPs). Here we review past and current research exploring the gut microbiome of NHPs. First, we summarize methods for characterization of the NHP gut microbiome. Then we discuss variation in gut microbiome composition and function across different NHP taxa. Finally, we highlight how studying the gut microbiome offers new insights into primate nutrition, physiology, and immune system function, as well as enhances our understanding of primate ecology and evolution. Microbiome approaches are useful tools for studying relevant issues in primate ecology. Further study of the gut microbiome of NHPs will offer new insight into primate ecology and evolution as well as human health.

Red-shanked doucs (Pygathrix nemaeus) are endangered, foregut-fermenting colobine primates which are difficult to maintain in captivity. There are critical gaps in our understanding of their natural lifestyle, including dietary habits such as consumption of leaves, unripe fruit, flowers, seeds, and other plant parts. There is also a lack of understanding of enteric adaptations, including their unique microflora. To address these knowledge gaps, we used the douc as a model to study relationships between gastrointestinal microbial community structure and lifestyle. We analyzed published fecal samples as well as detailed dietary history from doucs with four distinct lifestyles (wild, semi-wild, semi-captive, and captive) and determined gastrointestinal bacterial microbiome composition using 16S rRNA sequencing. A clear gradient of microbiome composition was revealed along an axis of natural lifestyle disruption, including significant associations with diet, biodiversity, and microbial function. We also identified potential microbial biomarkers of douc dysbiosis, including Bacteroides and Prevotella, which may be related to health. Our results suggest a gradient-like shift in captivity causes an attendant shift to severe gut dysbiosis, thereby resulting in gastrointestinal issues.

Marmoset wasting syndrome (MWS) describes a series of symptoms in callitrichids that lead to general weakness and a failure to thrive in captive conditions such as zoological institutions. Though the cause of MWS has not been identified, the majority of hypotheses are linked to deficiencies of specific nutrients and increased stress levels. Questionnaires were sent to zoos requesting information on diets and housing of currently living and dead callitrichids before their deaths, as well as their postmortem reports. Risk factors for development and occurrence of MWS include close proximity of predator enclosures and high levels of dietary magnesium and zinc. Variables with effects which may protect against the development of MWS included provision of a nest box, natural trees within enclosure, reduced visibility to visitors, as well as dietary factors such as higher concentrations of potassium and fiber fractions. The protective effects of limited concentrate feeds and increased total dietary fiber may help reduce the risks of developing MWS. The minerals may not have biological implications in MWS per se, however, they may be reflective of diets too high in concentrates and too low in plant matter. Habitat designs that are less naturalistic and those which provide insufficient privacy or hide areas may increase chronic stress for callitrichid species, possibly because of visitor-related stress. Other causes of chronic stress in captive zoo populations should be the topic of further research to reduce occurrence of MWS.

Asian slow lorises are found in zoos and rescue centres worldwide with Nycticebus pygmaeus, the pygmy slow loris, boasting the largest population in captivity. Diet are reportedly high in fruit and concentrates and low in insects and exudates. Wild feeding studies place insects, nectar, and gums as the most important diet components. Captive populations also show high incidences of health afflictions, many of which may be caused by nutrition. Our study, aims at identifying a causative agent within the diets of N. pygmaeus in regards to diseases prominent within captive populations. We sent out 55 diet and health questionnaires to institutions worldwide. Returned diets were nutritionally analyzed. Nutrient values and proportions of each ingredient were used in a principle components analysis. Resulting factors were used as variables in a binary logistic regression (BLR), with dental disease as the dependent variable. 39 questionnaires were returned with a total of 47 diets. 20 (51.7%) institutions reported the presence of diseases with dental issues being prominent. Factors that were significant in the principle components analysis included gum, nectar, protein, acid detergent fibre, calcium, ash, phosphorus, potassium, Ca:P, magnesium, vitamin D, and energy. Gum was the only significant predictor in the BLR. Lastly, a chi square test for association was performed with the presence of dental disease as the dependent variable and the amount of fruit in the diet. The combination of high fruits and little to no gum promotes the occurrence of dental diseases. Current captive diets do not reflect the evolutionary adaptations of Nycticebus primates. Zoo Biol. 34:547–553, 2015. © 2015 Wiley Periodicals, Inc.

The strategy used by the Javan slow lorises during periods of lower food availability were similar to folivorous primates and included increased dependence on lower quality foods. The reproductive costs of gestation and lactation may place a burden on females that requires them to alter their foraging strategy during the dry season to ensure enough protein and overall energy is ingested. The overall strategy used by these exudativorous primates is one of nutrient maximization as no nutrient was clearly preferred over another.

In captivity, the pygmy slow loris Nycticebus pygmaeus population worldwide suffers from poor reproduction, dental diseases, facial abscesses and various other health problems which, cumulatively, mean that the population is far from self-sustaining. The diet recommendations are anecdotal at best, and improvements are urgently needed for this vulnerable species. New evidence suggests that wild N. pygmaeus are primarily exudativores, and consume nectar and gum daily from a variety of tropical plant species, along with a large variety of insects. The typical diet in captivity contains fruit, a concentrated pellet, some insects and occasionally gum as enrichment. Our aims were to compare the behavioural activity budget of 1 male N. pygmaeus at Paignton Zoo on his original diet, on the same diet with added nectar and on an evidence-based naturalistic diet of mainly gum and nectar. We also investigated the nutrient intake of 2 males when given these diets. Behavioural observations were made overnight using night-vision cameras for 15, 10 and 11 d for each diet, respectively. Abnormal (generalised linear mixed model, GLMM χ 2 (1, 2) = 8.673, p = 0.013), travelling (GLMM χ 2 (1, 2) = 6.107, p = 0.047) and feeding (GLMM χ 2 (1, 2) = 79.679, p = 0.0001) behaviours all varied significantly between diets. In the behavioural study, the addition of gum, nectar and insects and the removal of fruit expanded and diversified the loris' activity budget and reduced the extent to which abnormal behaviour patterns were displayed. The intake study showed that both lorises consumed more when fed the naturalistic diet, suggesting they found it more palatable. Evidence of diet change suggests that a naturalistic approach to feeding N. pygmaeus enhances its welfare.KEY WORDS: Loris · Diets · Evidence-based husbandry · Gum · Nectar · Exudativore Resale or republication not permitted without written consent of the publisher Contribution to the Theme Section 'Conservation and ecology of slow lorises'FREE REE ACCESS CCESS

In a world increasingly dominated by human demand for agricultural products, we need to understand wildlife's ability to survive in agricultural environments. We studied the interaction between humans and Javan slow lorises (Nycticebus javanicus) in Cipaganti, Java, Indonesia. After its introduction in 2013, chayote (Sechium edule), a gourd grown on bamboo lattice frames, became an important cash crop. To evaluate people's use of this crop and to measure the effect of this increase on slow loris behaviour, home ranges, and sleep sites, we conducted interviews with local farmers and analysed the above variables in relation to chayote expansion between 2011-2015. Interviews with farmers in 2011, 2013 and 2015 confirm the importance of chayote and of bamboo and slow lorises in their agricultural practises. In 2015 chayote frames covered 12% of land in Cipaganti, occupying 4% of slow loris home ranges, which marginally yet insignificantly increased in size with the increase in chayote. Slow lorises are arboreal and the bamboo frames increased connectivity within their ranges. Of the sleep sites we monitored from 2013-2016, 24 had disappeared, and 201 continued to be used by the slow lorises and processed by local people. The fast growth rate of bamboo, and the recognition of the value of bamboo by farmers, allow persistence of slow loris sleep sites. Overall introduction of chayote did not result in conflict between farmers and slow lorises, and once constructed the chayote bamboo frames proved to be beneficial for slow lorises.