The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican black howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of howlers occupying suboptimal habitats, which may impact host health.

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Habitat degradation impacts black howler monkey ( Alouatta pigra ) gastrointestinal microbiomes

The sudden appearance of diseases like SARS (severe acute respiratory syndrome1), the devastating impacts of diseases like Ebola on both human and wildlife communities,2, 3 and the immense social and economic costs created by viruses like HIV4 underscore our need to understand the ecology of infectious diseases. Given that monkeys and apes often share parasites with humans, understanding the ecology of infectious diseases in nonhuman primates is of paramount importance. This is well illustrated by the HIV viruses, the causative agents of human AIDS, which evolved recently from related viruses of chimpanzees (Pan troglodytes) and sooty mangabeys (Cercocebus atys5), as well as by the outbreaks of Ebola virus, which trace their origins to zoonotic transmissions from local apes.6 A consideration of how environmental change may promote contact between humans and nonhuman primates and thus increase the possibility of sharing infectious diseases detrimental to humans or nonhuman primates is now paramount in conservation and human health planning.

http://www.envs.emory.edu/faculty/GILLESPIE/publications/Chapmanetal2005.pdf

Primates and the Ecology of their Infectious Diseases: How will Anthropogenic Change Affect Host-Parasite Interactions?

We address the strategies to prevent disease transmission from human to non-human primates in natural settings. Some field research methods, such as gaining close proximity for observation, provisioning for habituation, or reintroducing for repopulation, may place primate subjects at risk for acquiring human-carried diseases. Additional risks arise through inadequate waste disposal or nonhygienic conditions of humans residing at the study site. We describe several disease outbreaks at primate field sites, emphasizing the need for proper protocols to diagnose, to treat, and to prevent recurrence. Finding solutions to the disease transmission problem requires effecting change in the behavior and policies of many individuals, including field researchers, veterinarians, human health care providers, park personnel, government officials, local villagers, and tourists. The prevention of exposure to infectious disease is an important, fundamental aspect of primate conservation; the assurance of good health and longevity in wild primate populations is paramount to the more traditional conservation issues of poaching control and forest protection.

Primate Conservation: The Prevention of Disease Transmission

We examined the literature on the effects of habitat fragmentation and disturbance on howler monkeys (genus Alouatta) to (1) identify different threats that may affect howlers in fragmented landscapes; (2) review specific predictions developed in fragmentation theory and (3) identify the empirical evidence supporting these predictions. Although howlers are known for their ability to persist in both conserved and disturbed conditions, we found evidence that they are negatively affected by high levels of habitat loss, fragmentation and degradation. Patch size appears to be the main factor constraining populations in fragmented habitats, probably because patch size is positively related to food availability, and negatively related to anthropogenic pressures, physiological stress and parasite loads. Patch isolation is not a strong predictor of either patch occupancy or population size in howlers, a result that may be related to the ability of howlers to move among forest patches. Thus, we propose that it is probable that habitat loss has larger consistent negative effects on howler populations than habitat fragmentation per se. In general, food availability decreases with patch size, not only due to habitat loss, but also because the density of big trees, plant species richness and howlers' home range size are lower in smaller patches, where howlers' population densities are commonly higher. However, it is unclear which vegetation attributes have the biggest influence on howler populations. Similarly, our knowledge is still limited concerning the effects of postfragmentation threats (e.g. hunting and logging) on howlers living in forest patches, and how several endogenous threats (e.g. genetic diversity, physiological stress, and parasitism) affect the distribution, population structure and persistence of howlers. More long-term studies with comparable methods are necessary to quantify some of the patterns discussed in this review, and determine through meta-analyses whether there are significant inter-specific differences in species' responses to habitat loss and fragmentation.

Effects of habitat fragmentation and disturbance on howler monkeys: a review

In recent years much new information has been obtained about the epidemiology, population biology and public health significance of infections of Ascaris lumbricoides in humans. Results from experimental infections of A. suum in pigs have helped to elucidate the observations made in the community on human ascariasis. The main purpose of the review is to see how new information may contribute to further acceptance of ascariasis as a serious contributor to ill-health and so to the design and implementation of sustainable control programmes intended to reduce the morbidity due to infection with A. lumbricoides. Eradication is neither a realistic nor prudent aim given the current shortage of appropriate sanitation in many countries where ascariasis is endemic. A substantial body of evidence shows that for the four common species of soil-transmitted nematode, including A. lumbricoides, regular administration of broad-spectrum anthelminthic drugs to children attending primary schools is a cost-effective means of controlling the infections. Anthelminthic drugs must be of proven quality and efficacy and health professionals should be prepared to detect and manage drug resistance should that emerge. Despite a deeper understanding of the immune response of a variety of hosts to infections with either A. lumbricoides or A. suum there is at present little prospect of an effective vaccine against ascariasis. The relationship between A. lumbricoides and A. suum is addressed, particularly since both species, if they are indeed separate species, occur in people and their pigs in many communities.

Ascaris and ascariasis.

A literature review of howler parasites provides the basis for an overview of the ecological significance of parasite surveys in primates. Within this framework, we have added insights into the interactions between primate hosts and their parasites from a long-term study in Costa Rica. We collected fecal samples from mantled howlers (Alouatta palliata) over a 9-year period (1986–1994 inclusive) and analyzed them for parasite eggs, larvae, cysts, and oocysts. We found many misperceptions inherent in the typical methodology of primate parasite surveys and in the reporting of the findings. Our work in Costa Rica suggests that a snapshot effect occurs with most surveys. A static view does not reflect the dynamic and changing ecological interaction between host and parasite. We describe some problems with parasite data analyses that emphasize the need for long-term longitudinal surveys in wild primate groups.

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Parasites of Wild Howlers (Alouatta spp.)

Examinations of primate parasitic infections can inform both primatologists and parasitologists about evolutionary and ecological relationships. Interspecific, intraspecific, and interindividual variation in parasitic infections may correlate with environmental, demographic, behavioral, and human variables. Understanding these relationships is particularly important for conservation management issues for endangered species. We describe techniques for the noninvasive collection and preservation of fecal samples from wild primates and the salvaging of parasitological information from primate hosts in the field.

Primates and parasites: A case for a multidisciplinary approach

Fecal samples from 155 mantled howling monkeys (Alouatta palliata palliata) examined at Centro Ecologico La Pacifica, Guanacaste Province, Costa Rica, revealed 75 (48%) had parasitic infections. A sampling of nine howling monkeys from Santa Rosa National Park, Costa Rica indicated only one infected animal (11%). Only three of 19 (16%) spider monkeys (Ateles geoffroyi) also from Santa Rosa were infected. Controrchis biliophilus, Trypanoxyuris minutus, unidentified strongylid eggs and Isospora sp. oocysts were found. Three monkeys from La Pacifica died and were examined for adult helminths. They were infected with Ascaris lumbricoides, C. biliophilus and T. minutus.

/pdf/a-coprological-survey-of-parasites-of-wild-mantled-howling-yo9t7ku9gs.pdf

A Coprological Survey of Parasites of Wild Mantled Howling Monkeys, Alouatta palliata palliata

Fecal samples were collected from black howler monkeys (Alouatta pigra) in north central Belize and analyzed for evidence of endoparasite life stages. At least six types of endoparasites were found in Alouatta pigra fecal samples collected in the Lamanai Archaeological Reserve and the Community Baboon Sanctuary in 1999. These include a digenean trematode, an oxyurid nematode, a strongyle-type nematode, an ascarid presumed to be Ascaris sp., Entamoeba coli and Iodamoeba butschlii. Higher trematode prevalence was found in adult Alouatta pigra compared to juveniles and higher prevalence of nematode larvae in all animals was found in the wet season compared to the dry season.

Coprological Surveys of Alouatta pigra at Two Sites in Belize

One hundred twenty-eight fecal exami- nations from 57 muriquis or woolly spider monkeys, Brachyteles arachnoides, and 62 fecal samples from 9 brown howling monkeys, Alouatta fusca, that coexist in the Atlantic forest in southeastern Brazil were ex- amined for evidence of parasite infections. Hosts from 4 sites, 2 in Minas Gerais (EBC and FE) and 2 in Sao Paulo (FBR and PECB), showed differences in parasite prevalence and diversity. Neither muriquis nor brown howling monkeys from site 1 (EBC) revealed parasites. Monkeys from site 2 (FE) had only eggs presumed to be Strongyloides cebus and those from site 3 (FBR) had only Trypanoxyuris brachytelesi. Eggs and larvae pre- sumed to be Strongyloides cebus, Trypanoxyuris brach- ytelesi, Graphidiodes berlai, and an unidentified dige- nean were found at site 4 (PECB). The 4 study sites differ substantially in size (40-37,000 ha), degree of human disturbance, climate, plant species composi- tion, and muriqui densities. Contrary to expectations, muriquis from the largest and least-disturbed forest (with the lowest population density) had the highest prevalence and diversity of parasitic infection. A va- riety of factors, including vegetation and climatic dif- ferences, could explain this paradoxical pattern. How- ever, the fact that PECB is the site least affected by human disturbance also suggests that the complex eco- logical web involved in parasitic transmission has been disrupted at the other sites. Our findings reaffirm the importance of using parasites as ecological indicator species in studies of wild primates and suggest that management plans which involve translocations must be sensitive to the potential effects of parasites on naive hosts.

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Michael D. Stuart

Papers

Parasites of Wild Howlers (Alouatta spp.)

Primates and parasites: A case for a multidisciplinary approach

A Coprological Survey of Parasites of Wild Mantled Howling Monkeys, Alouatta palliata palliata

Coprological Surveys of Alouatta pigra at Two Sites in Belize

A Coprological Survey of Parasites of Wild Muriquis, Brachyteles arachnoides, and Brown Howling Monkeys, Alouatta fusca