Latitudinal gradients of parasite species richness in primates

Infectious disease risk is thought to increase in the tropics, but little is known about latitudinal gradients of parasite diversity. We used a comparative data set encompassing 330 parasite species reported from 119 primate hosts to examine latitudinal gradients in the diversity of micro and macroparasites per primate host species. Analyses conducted with and without controlling for host phylogeny showed that parasite species richness increased closer to the equator for protozoan parasites, but not for viruses or helminths. Relative to other major parasite groups, protozoa reported from wild primates were transmitted disproportionately by arthropod vectors. Within the protozoa, our results revealed that vector‐borne parasites showed a highly significant latitudinal gradient in species richness. This higher diversity of vector‐borne protozoa near the tropics could be influenced by a greater abundance or diversity of biting arthropods in the tropics, or by climatic effects on vector behaviour and parasite development. Many vector‐borne diseases, such as leishmaniasis, trypanosomiasis, and malaria pose risks to both humans and wildlife, and nearly one‐third of the protozoan parasites from free‐living primates in our data set have been reported to infect humans. Because the geographical distribution and prevalence of many vector‐borne parasites are expected to increase because of global warming, these results are important for predicting future parasite‐mediated threats to biodiversity and human health.     

Do threatened hosts have fewer parasites? A comparative study in primates

1. Parasites and infectious diseases have become a major concern in conservation biology, in part because they can trigger or accelerate species or population declines. Focusing on primates as a well-studied host clade, we tested whether the species richness and prevalence of parasites differed between threatened and non-threatened host species. 2. We collated data on 386 species of parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect wild populations of 36 threatened and 81 non-threatened primate species. Analyses controlled for uneven sampling effort and host phylogeny. 3. Results showed that total parasite species richness was lower among threatened primates, supporting the prediction that small, isolated host populations harbour fewer parasite species. This trend was consistent across three major parasite groups found in primates (helminths, protozoa and viruses). Counter to our predictions, patterns of parasite species richness were independent of parasite transmission mode and the degree of host specificity. 4. We also examined the prevalence of selected parasite genera among primate sister-taxa that differed in their ranked threat categories, but found no significant differences in prevalence between threatened and non-threatened hosts. 5. This study is the first to demonstrate differences in parasite richness relative to host threat status. Results indicate that human activities and host characteristics that increase the extinction risk of wild animal species may lead simultaneously to the loss of parasites. Lower average parasite richness in threatened host taxa also points to the need for a better understanding of the cascading effects of host biodiversity loss for affiliated parasite species.     

Metabarcoding of eukaryotic parasite communities describes diverse parasite assemblages spanning the primate phylogeny

Despite their ubiquity, in most cases little is known about the impact of eukaryotic parasites on their mammalian hosts. Comparative approaches provide a powerful method to investigate the impact of parasites on host ecology and evolution, though two issues are critical for such efforts: controlling for variation in methods of identifying parasites and incorporating heterogeneity in sampling effort across host species. To address these issues, there is a need for standardized methods to catalogue eukaryotic parasite diversity across broad phylogenetic host ranges. We demonstrate the feasibility of a metabarcoding approach for describing parasite communities by analysing faecal samples from 11 nonhuman primate species representing divergent lineages of the primate phylogeny and the full range of sampling effort (i.e. from no parasites reported in the literature to the best‐studied primates). We detected a number of parasite families and regardless of prior sampling effort, metabarcoding of only ten faecal samples identified parasite families previously undescribed in each host (x? = 8.5 new families per species). We found more overlap between parasite families detected with metabarcoding and published literature when more research effort—measured as the number of publications—had been conducted on the host species' parasites. More closely related primates and those from the same continent had more similar parasite communities, highlighting the biological relevance of sampling even a small number of hosts. Collectively, results demonstrate that metabarcoding methods are sensitive and powerful enough to standardize studies of eukaryotic parasite communities across host species, providing essential new tools for macroecological studies of parasitism.     

Molecular characterization of nodule worm in a community of Bornean primates

Strongyles are commonly reported parasites in studies of primate parasite biodiversity. Among them, nodule worm species are often overlooked as a serious concern despite having been observed to cause serious disease in nonhuman primates and humans. In this study, we investigated whether strongyles found in Bornean primates are the nodule worm Oesophagostomum spp., and to what extent these parasites are shared among members of the community. To test this, we propose two hypotheses that use the parasite genetic structure to infer transmission processes within the community. In the first scenario, the absence of parasite genetic substructuring would reflect high levels of parasite transmission among primate hosts, as primates’ home ranges overlap in the study area. In the second scenario, the presence of parasite substructuring would suggest cryptic diversity within the parasite genus and the existence of phylogenetic barriers to cross‐species transmission. By using molecular markers, we identify strongyles infecting this primate community as O. aculeatum, the only species of nodule worm currently known to infect Asian nonhuman primates. Furthermore, the little to no genetic substructuring supports a scenario with no phylogenetic barriers to transmission and where host movements across the landscape would enable gene flow between host populations. This work shows that the parasite's high adaptability could act as a buffer against local parasite extinctions. Surveys targeting human populations living in close proximity to nonhuman primates could help clarify whether this species of nodule worm presents the zoonotic potential found in the other two species infecting African nonhuman primates.     

Patterns of host specificity and transmission among parasites of wild primates

Multihost parasites have been implicated in the emergence of new diseases in humans and wildlife, yet little is known about factors that influence the host range of parasites in natural populations. We used a comprehensive data set of 415 micro- and macroparasites reported from 119 wild primate hosts to investigate broad patterns of host specificity. The majority (68%) of primate parasites were reported to infect multiple host species, including animals from multiple families or orders. This pattern corresponds to previous studies of parasites found in humans and domesticated animals. Within three parasite groups (viruses, protozoans and helminths), we examined parasite taxonomy and transmission strategy in relation to measures of host specificity. Relative to other parasite groups, helminths were associated with the greatest levels of host specificity, whereas most viruses were reported to infect hosts from multiple families or orders. Highly significant associations between the degree of host specificity and transmission strategy arose within each parasite group, but not always in the same direction, suggesting that unique constraints influence the host range of parasites within each taxonomic group. Finally characteristics of over 100 parasite species shared between wild primates and humans, including those recognised as emerging in humans, revealed that most of these shared parasites were reported from multiple host orders. Furthermore, nearly all viruses that were reported to infect both humans and non-human primates were classified as emerging in humans.     

Does habitat disturbance increase infectious disease risk for primates?

Many studies have suggested that ecosystem conservation protects human and wildlife populations against infectious disease. We tested this hypothesis using data on primates and their parasites. First, we tested for relationships between species' resilience to human disturbance and their parasite richness, prevalence and immune defences, but found no associations. We then conducted a meta‐analysis of the effects of disturbance on parasite prevalence, which revealed no overall effect, but a positive effect for one of four types of parasites (indirectly transmitted parasites). Finally, we conducted intraspecific analyses of malaria prevalence as a function of mammalian species richness in chimpanzees and gorillas, and an interspecific analysis of geographic overlap and parasite species richness, finding that higher levels of host richness favoured greater parasite risk. These results suggest that anthropogenic effects on disease transmission are complex, and highlight the need to define the conditions under which environmental change will increase or decrease disease transmission.     

A combined parasitological molecular approach for noninvasive characterization of parasitic nematode communities in wild hosts

Most hosts are concurrently or sequentially infected with multiple parasites; thus, fully understanding interactions between individual parasite species and their hosts depends on accurate characterization of the parasite community. For parasitic nematodes, noninvasive methods for obtaining quantitative, species‐specific infection data in wildlife are often unreliable. Consequently, characterization of gastrointestinal nematode communities of wild hosts has largely relied on lethal sampling to isolate and enumerate adult worms directly from the tissues of dead hosts. The necessity of lethal sampling severely restricts the host species that can be studied, the adequacy of sample sizes to assess diversity, the geographic scope of collections and the research questions that can be addressed. Focusing on gastrointestinal nematodes of wild African buffalo, we evaluated whether accurate characterization of nematode communities could be made using a noninvasive technique that combined conventional parasitological approaches with molecular barcoding. To establish the reliability of this new method, we compared estimates of gastrointestinal nematode abundance, prevalence, richness and community composition derived from lethal sampling with estimates derived from our noninvasive approach. Our noninvasive technique accurately estimated total and species‐specific worm abundances, as well as worm prevalence and community composition when compared to the lethal sampling method. Importantly, the rate of parasite species discovery was similar for both methods, and only a modest number of barcoded larvae (n = 10) were needed to capture key aspects of parasite community composition. Overall, this new noninvasive strategy offers numerous advantages over lethal sampling methods for studying nematode–host interactions in wildlife and can readily be applied to a range of study systems.     

Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density

Aim  Comparative studies have revealed strong links between ecological factors and the number of parasite species harboured by different hosts, but studies of different taxonomic host groups have produced inconsistent results. As a step towards understanding the general patterns of parasite species richness, we present results from a new comprehensive data base of over 7000 host–parasite combinations representing 146 species of carnivores (Mammalia: Carnivora) and 980 species of parasites.
Methods  We used both phylogenetic and non-phylogenetic comparative methods while controlling for unequal sampling effort within a multivariate framework to ascertain the main determinants of parasite species richness in carnivores.
Results  We found that body mass, population density, geographical range size and distance from the equator are correlated with overall parasite species richness in fissiped carnivores. When parasites are classified by transmission mode, body mass and home range area are the main determinants of the richness of parasites spread by close contact between hosts, and population density, geographical range size and distance from the equator account for the diversity of parasites that are not dependent on close contact. For generalist parasites, population density, geographical range size and latitude are the primary predictors of parasite species richness. We found no significant ecological correlates for the richness of specialist or vector-borne parasites.
Main conclusions  Although we found that parasite species richness increases instead of decreases with distance from the equator, other comparative patterns in carnivores support previous findings in primates, suggesting that similar ecological factors operate in both these independent evolutionary lineages.     

A multiyear survey of helminths from wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins

The establishment of baseline data on parasites from wild primates is essential to understand how changes in habitat or climatic disturbances will impact parasite–host relationships. In nature, multiparasitic infections of primates usually fluctuate temporally and seasonally, implying that the acquisition of reliable data must occur over time. Individual parasite infection data from two wild populations of New World primates, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, were collected over 3 years to establish baseline levels of helminth prevalence and parasite species richness (PSR). Secondarily, we explored variation in parasite prevalence across age and sex classes, test nonrandom associations of parasite co‐occurrence, and assess the relationship between group size and PSR. From 288 fecal samples across 105 individuals (71 saddleback and 34 emperor tamarins), 10 parasite taxa were identified by light microscopy following centrifugation and ethyl‐acetate sedimentation. Of these taxa, none were host‐specific, Dicrocoeliidae and Cestoda prevalences differed between host species, Prosthenorchis and Strongylida were the most prevalent. Host age was positively associated with Prosthenorchis ova and filariform larva, but negatively with cestode and the Rhabditoidea ova. We detected no differences between expected and observed levels of co‐infection, nor between group size and parasite species richness over 30 group‐years. Logistic models of individual infection status did not identify a sex bias; however, age and species predicted the presence of four and three parasite taxa, respectively, with saddleback tamarins exhibiting higher PSR. Now that we have reliable baseline data for future monitoring of these populations, next steps involve the molecular characterization of these parasites, and exploration of linkages with health parameters.     

Putting the Spotlight on Internally Displaced Animals (IDAs): A Survey of Primate Sanctuaries in Africa,Asia, and the Americas

As anthropogenic activity makes deeper incursions into forests, fragmenting habitat, wildlife is forced into closer proximity to humans leading to increased incidences of human–wildlife conflict and wildlife displacement. These same incursions facilitate poaching for the commercial trade in dead and live animals. As a direct result, the number of sanctuaries and internally displaced animals (IDAs) in need of sanctuary placement and rehabilitation are increasing. We focus on internally displaced primates given the prevalence of primate‐focused facilities and anthropomorphic considerations surrounding this taxonomic group. Surveys were distributed globally to map the extent and range of native primate sanctuaries and species. Over 70 facilities care for more than 6,000 native primates comprising 64 species, with almost half listed as endangered or critically endangered. As not all sanctuaries were identified at the time of the survey distribution, we estimate that the actual number of facilities is closer to double this number with a captive population in excess of 10,000 individual primates. Native primate sanctuaries hold significant numbers of primates in long‐term captive care, with less than half (37%) identified as candidates for release. The surveyed sanctuary population accounts for 35% of the world's captive primates, as compared to ISIS‐registered (where ISIS is International Species Information System) zoological facilities, although we estimate that the actual population is closer to 58%. For some species, the sanctuary population represents the only population in captivity. We discuss the prevalence of range‐state sanctuaries and their primate populations, and issues surrounding their future development and management. Am. J. Primatol. 75:116‐134, 2013. © 2012 Wiley Periodicals, Inc.     

Effects of resource availability and social aggregation on the species richness of raccoon endoparasite infracommunities

Within populations the contact rate of hosts and infectious parasites is mediated by the interactions of resource availability, host density, and host behavior. Fluctuations in host density can result in the loss or extinction of a parasite population as contact rates between parasites and susceptible individuals drop below thresholds of parasite population persistence. Less understood is how changes in resources and the behavioral ecology of host populations affect parasites. We used food provisioning to experimentally assess the effects of resource availability and of inducing host aggregation on the endoparasite community of free‐ranging raccoons. Twelve independent raccoon populations were subjected to differential resource provisioning for two years: a clumped food distribution to aggregate hosts (n = 5 populations), a dispersed food distribution to add food without aggregating hosts (n = 3), and a no food treatment (n = 4). Remote cameras indicated that aggregation sizes were three to four times greater in aggregated versus non‐aggregated populations. We considered endoparasites with direct and indirect life cycles separately and determined the best‐fit models of parasite species richness in relation to host aggregation, food supplements, and host age and sex. Social aggregation had a negligible impact on the species richness of directly or indirectly transmitted parasites. However, food additions decreased the number of indirectly transmitted parasite species by 35% in the oldest age classes. These results suggest that while resource availability can influence the transmission of indirectly transmitted parasites, an examination of additional factors will be necessary to understand the role of host contact and factors that shape the community structure of endoparasites in natural environments.     

Global spread of helminth parasites at the human–domestic animal–wildlife interface

Changes in species distributions open novel parasite transmission routes at the human–wildlife interface, yet the strength of biotic and biogeographical factors that prevent or facilitate parasite host shifting are not well understood. We investigated global patterns of helminth parasite (Nematoda, Cestoda, Trematoda) sharing between mammalian wildlife species and domestic mammal hosts (including humans) using >24,000 unique country‐level records of host–parasite associations. We used hierarchical modelling and species trait data to determine possible drivers of the level of parasite sharing between wildlife species and either humans or domestic animal hosts. We found the diet of wildlife species to be a strong predictor of levels of helminth parasite sharing with humans and domestic animals, followed by a moderate effect of zoogeographical region and minor effects of species’ habitat and climatic niches. Combining model predictions with the distribution and ecological profile data of wildlife species, we projected global risk maps that uncovered strikingly similar patterns of wildlife parasite sharing across geographical areas for the different domestic host species (including humans). These similarities are largely explained by the fact that widespread parasites are commonly recorded infecting several domestic species. If the dietary profile and position in the trophic chain of a wildlife species largely drives its level of helminth parasite sharing with humans/domestic animals, future range shifts of host species that result in novel trophic interactions may likely increase parasite host shifting and have important ramifications for human and animal health.     

Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals

Epidemiological theory predicts positive correlations between host population density or body mass and species richness among parasite communities. Here I test these predictions by a comparative study of communities of directly transmitted mammalian parasites, gastrointestinal strongylid nematodes. I use data from 45 species of mammals, representing examination of 17 200 individual hosts. The variable studied was the average number of gastrointestinal strongylid nematode species per host population, and three different methods were used to obtain estimates of parasite species richness that are unbiased by number of host individuals examined. Analyses were done using the phylogenetically independent contrast method. Host population density and parasite species richness were strongly positively correlated when the effects of host body weight had been controlled for. Controlling for other variables did not change this, and the relationship was found regardless of method used to correct for uneven sampling effort among host species. A positive relationship between parasite species richness and host body weight was also found, but the effect of host densities had to be controlled for to see this. These relationships between host traits and species richness of directly transmitted parasites are stronger than patterns found using data on indirectly transmitted mammalian parasites, and suggests that links between host traits and parasite species richness are stronger than previously suggested. The results are consistent with parasite species richness being positively linked to pathogen transmission rates and reductions in transmission rates possibly increasing extinction probabilities in parasite populations. The results also suggest that parasites may exert a cost of increases in rate of population energy usage, and thus show that pathogens may be important in generating independence between body mass and rate of population energy usage among host species.     

Gastrointestinal Parasites of Indigenous and Introduced Primate Species of Rubondo Island National Park,Tanzania

Translocation programs releasing animals into the wild need to assess the potential risks associated with the exchange of parasites and other pathogens between native and translocated species. We assessed the composition of the parasite communities in sympatric native and introduced primates. Over a 3-yr period we monitored the gastrointestinal parasites of 3 primate species living in the isolated ecosystem of Rubondo Island National Park, Tanzania: translocated chimpanzees (Pan troglodytes) and guerezas (Colobus guereza) and the indigenous vervets (Chlorocebus aethiops pygerythrus). We detected Troglodytella abrassarti and Enterobius cf. anthropopitheci only in chimpanzees and Chilomastix mesnili in chimpanzees and guerezas. In vervets, we recorded Anatrichosoma sp. and Subulura sp., previously reported in Rubondo chimpanzees. We found Blastocystis sp., Giardia sp., Iodamoeba buetschlii, Entamoeba coli, Entamoeba spp., Trichuris sp., Strongyloides spp., spirurids (cf. Protospirura muricola), and undetermined strongylids in all 3 primate species. Considering the absence of Protospirura muricola in other wild populations of chimpanzees and guerezas, it has probably been acquired from the native vervets, as have Anatrichosoma sp. and Subulura sp. Lower parasite load in Rubondo chimpanzees, in comparison with wild populations at other study sites of this species, might be due to their stay in captivity in Europe before being released on the island. Despite a lack of any apparent health problems from infections in introduced Rubondo primates, parasite monitoring during reintroduction/introduction projects is necessary to decrease potential risks resulting from the exchange of parasites between translocated and native species.     

Effectively vertical transmission of a Drosophila‐parasitic nematode: mechanism and consequences

1. Long‐term control of insects by parasites is possible only if the parasite populations persist. Because parasite transmission rate depends on host density, parasite populations may go extinct during periods of low host density. Vertical transmission of parasites, however, is independent of host density and may therefore provide a demographic bridge through times when their insect hosts are rare. 2. The nematode Howardula aoronymphium, which parasitises mycophagous species of Drosophila, can experience both horizontal and effectively vertical transmission, relative rates of which depend, in theory at least, on the density of hosts at breeding sites. 3. A nine‐generation experiment was carried out in which nematodes were transmitted either exclusively vertically or primarily horizontally. This experiment revealed that these parasites can persist and exhibit positive population growth even when there is only vertical transmission. 4. Assays at the end of the experiment revealed that the vertically transmitted nematodes had suffered no inbreeding depression and that they were similar to the horizontally transmitted nematodes in terms of virulence, infectivity, within‐host growth rate, and fecundity. Thus, vertical transmission of H. aoronymphium did not appear to compromise the ability of these parasites to control Drosophila populations.     

Parasite community structure in sympatric Bornean primates

Parasites are important components of ecosystems, influencing trophic networks, competitive interactions and biodiversity patterns. Nonetheless, we are not nearly close to disentangling their complex roles in natural systems. Southeast Asia falls within global areas targeted as most likely to source parasites with zoonotic potential, where high rates of land conversion and fragmentation have altered the circulation of wildlife species and their parasites, potentially resulting in altered host-parasite systems. Although the overall biodiversity in the region predicts equally high, or even higher, parasite diversity, we know surprisingly little about wild primate parasites, even though this constitutes the first step towards a more comprehensive understanding of parasite transmission processes. Here, we characterise the gastrointestinal helminth parasite assemblages of a community of Bornean primates living along the Kinabatangan floodplain in Sabah (Malaysian Borneo), including two species endemic to the island. Through parasitological analyses, and by using several measures of parasite infection as proxies for parasite diversity and distribution, we show that (i) most parasite taxonomic groups are not limited to a single host, suggesting a greater flexibility for habitat disturbance, (ii) parasite infracommunities of nocturnal primates differ from their diurnal counterparts, reflecting both phylogenetic and ecological constraints, and (iii) soil-transmitted helminths such as whipworm, threadworm and nodule worm are widespread across the primate community. This study also provides new parasite records for southern pig-tailed macaques (Macaca nemestrina), silvered langurs (Trachypithecus cristatus) and Western tarsiers (Cephalopachus bancanus) in the wild, while adding to the limited records for the other primate species in the community. Given the information gap regarding primate-parasite associations in the region, the information presented here should prove relevant for future studies of parasite biodiversity and infectious disease ecology in Asia and elsewhere.     

Diversity and host assemblage of avian haemosporidians in different terrestrial ecoregions of Peru

Characterizing the diversity and structure of host–parasite communities is crucial to understanding their eco-evolutionary dynamics. Malaria and related haemosporidian parasites are responsible for fitness loss and mortality in bird species worldwide. However, despite exhibiting the greatest ornithological biodiversity, avian haemosporidians from Neotropical regions are quite unexplored. Here, we analyze the genetic diversity of bird haemosporidian parasites (Plasmodium and Haemoproteus) in 1,336 individuals belonging to 206 bird species to explore for differences in diversity of parasite lineages and bird species across 5 well-differentiated Peruvian ecoregions. We detected 70 different haemosporidian lineages infecting 74 bird species. We showed that 25 out of the 70 haplotypes had not been previously recorded. Moreover, we also identified 81 new host–parasite interactions representing new host records for these haemosporidian parasites. Our outcomes revealed that the effective diversity (as well as the richness, abundance, and Shannon–Weaver index) for both birds and parasite lineages was higher in Amazon basin ecoregions. Furthermore, we also showed that ecoregions with greater diversity of bird species also had high parasite richness, hence suggesting that host community is crucial in explaining parasite richness. Generalist parasites were found in ecoregions with lower bird diversity, implying that the abundance and richness of hosts may shape the exploitation strategy followed by haemosporidian parasites. These outcomes reveal that Neotropical region is a major reservoir of unidentified haemosporidian lineages. Further studies analyzing host distribution and specificity of these parasites in the tropics will provide important knowledge about phylogenetic relationships, phylogeography, and patterns of evolution and distribution of haemosporidian parasites.     

How parasite interaction strategies alter virulence evolution in multi‐parasite communities

The majority of organisms host multiple parasite species, each of which can interact with hosts and competitors through a diverse range of direct and indirect mechanisms. These within‐host interactions can directly alter the mortality rate of coinfected hosts and alter the evolution of virulence (parasite‐induced host mortality). Yet we still know little about how within‐host interactions affect the evolution of parasite virulence in multi‐parasite communities. Here, we modeled the virulence evolution of two coinfecting parasites in a host population in which parasites interacted through cross immunity, immune suppression, immunopathology, or spite. We show (1) that these within‐host interactions have different effects on virulence evolution when all parasites interact with each other in the same way versus when coinfecting parasites have unique interaction strategies, (2) that these interactions cause the evolution of lower virulence in some hosts, and higher virulence in other hosts, depending on the hosts infection status, and (3) that for cross immunity and spite, whether parasites increase or decrease the evolutionarily stable virulence in coinfected hosts depended on interaction strength. These results improve our understanding of virulence evolution in complex parasite communities, and show that virulence evolution must be understood at the community scale.     

Ecology of malaria parasites infecting Southeast Asian macaques: evidence from cytochrome b sequences

Although malaria parasites infecting non‐human primates are important models for human malaria, little is known of the ecology of infection by these parasites in the wild. We extensively sequenced cytochrome b (cytb) of malaria parasites (Apicomplexa: Haemosporida) from free‐living southeast Asian monkeys Macaca nemestrina and Macaca fascicularis. The two most commonly observed taxa were Plasmodium inui and Hepatocystis sp., but certain other sequences did not cluster closely with any previously sequenced species. Most of the major clades of parasites were found in both Macaca species, and the two most commonly occurring parasite infected the two Macaca species at approximately equal levels. However, P. inui showed evidence of genetic differentiation between the populations infecting the two Macaca species, suggesting limited movement of this parasite among hosts. Moreover, coinfection with Plasmodium and Hepatocystis species occurred significantly less frequently than expected on the basis of the rates of infection with either taxon alone, suggesting the possibility of competitive exclusion. The results revealed unexpectedly complex communities of Plasmodium and Hepatocystis taxa infecting wild southeast Asian monkeys. Parasite taxa differed with respect to both the frequency of between‐host movement and their frequency of coinfection.     

Survey and comparison of major intestinal flora in captive and wild ring-tailed lemur (Lemur catta) populations

A survey to identify the major intestinal species of aerobic bacteria, protozoa and helminths was conducted on captive and wild populations of ring-tailed lemurs (Lemur catta). Samples were collected from 50 captive lemurs at 11 zoological institutions in the United States. In Madagascar, 98 aerobic bacteria samples and 99 parasite samples were collected from eight sites chosen to cover a variety of populations across the species range. Identical collection, preservation and lab techniques were used for captive and wild populations. The predominant types of aerobic bacteria flora were identified via five separate tests. The tests for parasites conducted included flotation, sedimentation and FA/GC. Twenty-seven bacteria unique to either the captive or wild populations were cultured with eight of these being statistically significantly different. Fourteen bacteria common to both populations were cultured, of which six differed significantly. Entamoeba coli was the only parasite common to both the captive and wild populations. Giardia spp., Isospora spp., strongyles-type ova, Entamoeba spp. and Entamoeba polecki were found only in captive samples. Cryptosporidium, Balantidium coli, pinworm-type ova, and two fluke-like ova were seen only in wild samples. In addition, samples were compared for both bacteria and parasites from three unique field sites in Madagascar. In this three-site comparison, six types of bacteria were statistically significantly different. No significant differences regarding parasites were seen. Significant differences were found between the captive and wild populations, whereas fewer differences were found between sites within Madagascar. Although we isolated Campylobacter and Giardia, all animals appeared clinically healthy.