Primates and parasites: A case for a multidisciplinary approach

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.     

The association of intestinal parasitosis and H. pylori infection in children and adults from a Mexican community with high prevalence of parasitosis

Background. ABSTExperimental evidences have suggested that a Th1 response is unable to eliminate H. pylori colonization; whereas a Th2 response, like the one induced by vaccination, reduces H. pylori infection in animal models. Some parasitic infections induce a polarized Th2 response, which theoretically would favor a reduced H. pylori prevalence. The aim of this work was to study the possible association between parasitic infections and H. pylori prevalence. Materials and Methods. The study population included 120 children and 188 adults from a low socioeconomic level village. H. pylori prevalence was determined in serum by ELISA; parasitic infections were identified in feces by microscopic examination; and total serum IgE levels, as an indirect indicator of some parasitic infections, were determined by ELISA. Results. In children, H. pylori prevalence was no different between those with and without intestinal parasitic infection. By contrast, adults with intestinal parasitic infection had a significantly lower H. pylori prevalence than adults without parasites (62.6% compared with 80.4%; p = 0.006, OR 2.45). Also in adults, but not in children, total IgE levels were significantly higher in those without H. pylori infection than in those with H. pylori infection (p < 0.001). Conclusions. Intestinal parasitic infections and serum IgE levels showed an age‐dependent association with H. pylori prevalence. In adults, but not in children, intestinal parasitic infections and increased IgE levels where associated with a reduced H. pylori prevalence.     

Gastrointestinal Parasites in Crop Raiding and Wild Foraging Papio anubis in Nigeria

We compared parasitic infection in a crop-raiding and a wild-foraging troop of olive baboons, Papio anubis, in Gashaka Gumti National Park, Nigeria, to quantify how crop raiding may have influenced primate-parasite interactions. We recovered gastrointestinal parasites from fecal samples from all adult individuals in both troops and processed them via formal-ether sedimentation. We compared parasitic species richness, prevalence, output, and load across troops. We recovered 9 parasite taxa. The wild-foraging troop had a significantly higher mean output than the crop-raiding troop for Physaloptera sp., Trichuris sp., and also a significantly higher total helminth load. The crop-raiding troop had a significantly higher mean output for the protozoan Balantidium coli and also showed a higher parasitic species richness, with 9 species recovered compared to the 7 recorded for the wild-foraging individuals. The changes in nutritional intake, behavior, and human proximity caused by crop raiding may have important epidemiological impacts on wild primate populations, and the nature of such impacts may vary across different taxa of parasites.     

Risk factors for helminth infections in a rural and a peri-urban setting of the Dongting Lake area, People's Republic of China

Schistosomiasis japonica and soil-transmitted helminthiasis are endemic parasitic diseases in the People’s Republic of China (PR China). As very few studies have reported on the distribution and interaction of multiple species helminth infections, we carried out a comparative study of households in a rural village and a peri-urban setting in the Dongting Lake area of Hunan province in November and December 2006 to determine the extent of single and multiple species infections, the underlying risk factors for infection, and the relationships with clinical manifestations and self-reported morbidity. In each household, stool samples were collected and subjected to the Kato-Katz method for identifying Schistosoma japonicum, Ascaris lumbricoides, hookworm and Trichuris trichiura infections. Clinical examinations were performed and questionnaire surveys conducted at both household and individual subject levels. Complete parasitological, clinical and questionnaire data were obtained for 1,298 inhabitants of the two settings. The overall prevalences of single infections of S. japonicum, A. lumbricoides, hookworm and T. trichiura were 6.5%, 5.5%, 3.0% and 0.8%, respectively; the majority of the infections were of light intensity. We found significant negative associations between wealth and infections with S. japonicum and A. lumbricoides. Clinical manifestations of splenomegaly, hepatomegaly and anaemia were prevalent (9.0%, 3.7% and 10.9%, respectively), the latter two being significantly (P < 0.05) associated with schistosomiasis. Self-reported symptoms were more common among females but there was considerable under-reporting in both sexes when relying only on spontaneous recall. Our findings may guide the design and targeting of a more equitable, comprehensive and integrated parasitic disease control programme in Hunan province and in other areas of PR China.     

Intestinal parasitism—protozoa and helminths—in primates at the Barcelona Zoo

Abstract: The faunistic results regarding intestinal parasitism by protozoa and helminths in 21 primate species (three Cebidae, thirteen Cercopithecidae, one Hylobatidae, one Lemuridae, three Pongidae) are reported. The primate species were housed in four separate galleries. Six faecal samples of each host species were subjected to coprological analysis. Fifteen parasite species were detected: 11 protozoa (Entamoeba coli, E. chattoni, E. hartmanni, Iodamoeba bütschlii, Endolimax nana, Giardia intestinalis, Chilomastix mesnilii, Enteromonas hominis, Trichomonas intestinalis, Balantidium coli, and Blastocystis hominis) and 4 helminths (Ancylostoma sp., Strongyloides fuelleborni, Strongyloides sp., and Trichuris trichiura). The results reveal certain parasitic similarities between host species housed in the same gallery; however, these primate species do not always carry identical parasite species.     

Seroprevalence of Trypanosoma cruzi and Leishmania mexicana in Free‐Ranging Howler Monkeys in Southeastern Mexico

Natural infection of wild mammals by protozoa parasites is quite common in nature. For Neotropical Primates different infections of parasites that are etiological agent of disease in human have been identified. In particular, infections by Trypanosoma cruzi and Leishmania sp., have been reported for some New World primate species, but there are no reports of infection with these parasites in any primate species in Mexico. A serological study was conducted on two howler monkey species (Alouatta pigra and A. palliata) from the Mexican states of Campeche and Tabasco. A total of 55 serum samples (20 samples from A. pigra, 20 samples from A. palliata, and 15 samples from semifree ranging A. palliata of Los Tuxtlas, Veracruz as negative controls) were analyzed for the detection of immunoglobulin G antibodies against T. cruzi and Leishmania mexicana through enzyme linked immunosorbent assay test, indirect immunofluorescence assay and Western blot. The overall prevalence of antibodies in howler monkeys was 17.5% for T. cruzi and 30% for L. mexicana. Our results also indicate that A. pigra is more susceptible to develop leishmaniasis than A. palliata. Finally, the finding of positive serology in these primates should be given serious consideration for public health, given the potential role of these primate species as wild reservoirs for these diseases and the increasing contact of monkeys with human populations due to habitat loss and fragmentation. Am. J. Primatol. 75:161‐169, 2013. © 2012 Wiley Periodicals, Inc.     

Diversity and temporal dynamics of primate milk microbiomes

Milk is inhabited by a community of bacteria and is one of the first postnatal sources of microbial exposure for mammalian young. Bacteria in breast milk may enhance immune development, improve intestinal health, and stimulate the gut‐brain axis for infants. Variation in milk microbiome structure (e.g., operational taxonomic unit [OTU] diversity, community composition) may lead to different infant developmental outcomes. Milk microbiome structure may depend on evolutionary processes acting at the host species level and ecological processes occurring over lactation time, among others. We quantified milk microbiomes using 16S rRNA high‐throughput sequencing for nine primate species and for six primate mothers sampled over lactation. Our data set included humans (Homo sapiens, Philippines and USA) and eight nonhuman primate species living in captivity (bonobo [Pan paniscus], chimpanzee [Pan troglodytes], western lowland gorilla [Gorilla gorilla gorilla], Bornean orangutan [Pongo pygmaeus], Sumatran orangutan [Pongo abelii], rhesus macaque [Macaca mulatta], owl monkey [Aotus nancymaae]) and in the wild (mantled howler monkey [Alouatta palliata]). For a subset of the data, we paired microbiome data with nutrient and hormone assay results to quantify the effect of milk chemistry on milk microbiomes. We detected a core primate milk microbiome of seven bacterial OTUs indicating a robust relationship between these bacteria and primate species. Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes. Gross energy in milk from protein and fat explained some of the variations in microbiome composition among species. Microbiome composition changed in a predictable manner for three primate mothers over lactation time, suggesting that different bacterial communities may be selected for as the infant ages. Our results contribute to understanding ecological and evolutionary relationships between bacteria and primate hosts, which can have applied benefits for humans and endangered primates in our care.     

Evolutionary relationships among the primate Mhc-DQA1 and DQA2 alleles

The variation of the Mhc-DQA1 and DQA2 loci of ten different primate species (hominoids and Old World monkeys) was studied in order to obtain an insight in the processes that generate polymorphism of major histocompatibility complex (Mhc) class II genes and to establish the evolutionary relationships of their alleles. To that end nucleotide sequences of 36 Mhc class II DQA1 and seven DQA2 second exons were determined and phylogenetic trees that illustrate their evolutionary relationships were constructed. We demonstrate the existence of four primate Mhc-DQA1 allele lineages, two of which probably existed before the separation of the ancestors of the hominoids and Old World monkeys (approximately 22–28 million years ago). Mhc-DQA2 sequences were found only in the hominoid species and showed little diversity. We found no evidence for a major contribution of recombinational events to the generation of allelic diversity of the primate Mhc-DQA1 locus. Instead, our data suggest that the primate Mhc-DQA1 and DQA2 loci are relatively stable entities that mutated primarily as a result of point mutations.The nucleotide sequence data reported in this paper have been submitted to the GenBank nucleotide sequence database and have been assigned the accession numbers M76186-M76229.     

Assessing the longitudinal structure of the early hominid foot: A two-dimensional architecture analysis

Early hominid feet are often very fragmentary preserved and their architectural approaches stayed limited and subject to controversy. This study proposes an architectural analysis of the primate foot realised on dislocated skeleton. It is based on the angular analysis of geometrical relationships between the joint areas. We investigate the longitudinal structure of the primate foot and we present the results concerning someAustralopithecus afarensis specimens from Hadar (Ethiopia) and theHomo habilis Olduvai Hominid 8 foot (Tanzania). The architectural analysis argues for the lack of a longitudinal medial arch inA. afarensis, their joints being in neutral position. On the contrary, the more recent OH8 specimen is arched both medially and laterally.     

Duration of the parasitic phase determines subsequent performance in juvenile freshwater pearl mussels (Margaritifera margaritifera)

Host–parasite systems have been useful in understanding coevolutionary patterns in sympatric species. Based on the exceptional interaction of the long‐lived and highly host‐specific freshwater pearl mussel (FPM; Margaritifera margaritifera) with its much shorter‐lived host fish (Salmo trutta or Salmo salar), we tested the hypotheses that a longer duration of the parasitic phase increases fitness‐related performance of mussels in their subsequent post parasitic phase, and that temperature is the main factor governing the duration of the parasitic phase. We collected juvenile mussels from naturally and artificially infested fish from eight rivers in Norway. Excysted juvenile mussels were maintained separately for each collection day, under similar temperature and food regimes, for up to 56 days. We recorded size at excystment, post excystment growth, and survival as indicators of juvenile fitness in relation to the duration of the parasitic phase. We also recorded the daily average temperatures for the entire excystment period. We observed strong positive relationships between the length of the parasitic phase and the post parasitic growth rate, size at excystment and post parasitic survival. Temperature was identified as an important factor governing excystment, with higher temperatures decreasing the duration of the parasitic phase. Our results indicate that juvenile mussels with the longest parasitic phase have better resources (larger size and better growth rate) to start their benthic developmental phase and therefore to survive their first winter. Consequently, the parasitic phase is crucial in determining subsequent survival. The temperature dependence of this interaction suggests that climate change may affect the sensitive relationship between endangered FPMs and their fish hosts.     

Prevalence of gastrointestinal parasites in captive non‐human primates of twenty‐four zoological gardens in China

Captive primates are susceptible to gastrointestinal (GIT) parasitic infections, which are often zoonotic and can contribute to morbidity and mortality. Fecal samples were examined by the means of direct smear, fecal flotation, fecal sedimentation, and fecal cultures. Of 26.51% (317/1196) of the captive primates were diagnosed gastrointestinal parasitic infections. Trichuris spp. were the most predominant in the primates, while Entamoeba spp. were the most prevalent in Old World monkeys (P < 0.05). These preliminary data will improve the management of captive primates and the safety of animal keepers and visitors.     

Evolutionary relationships among parvoviruses: virus-host coevolution among autonomous primate parvoviruses and links between adeno-associated and avian parvoviruses

The current classification of parvoviruses is based on virus host range and helper virus dependence, while little data on evolutionary relationships among viruses are available. We identified and analyzed 472 sequences of parvoviruses, among which there were (virtually) full-length genomes of all 41 viruses currently recognized as individual species within the family Parvoviridae. Our phylogenetic analysis of full-length genomes as well as open reading frames distinguished three evolutionary groups of parvoviruses from vertebrates: (i) the human helper-dependent adeno-associated virus (AAV) serotypes 1 to 6 and the autonomous avian parvoviruses; (ii) the bovine, chipmunk, and autonomous primate parvoviruses, including human viruses B19 and V9; and (iii) the parvoviruses from rodents (except for chipmunks), carnivores, and pigs. Each of these three evolutionary groups could be further subdivided, reflecting both virus-host coevolution and multiple cross-species transmissions in the evolutionary history of parvoviruses. No parvoviruses from invertebrates clustered with vertebrate parvoviruses. Our analysis provided evidence for negative selection among parvoviruses, the independent evolution of their genes, and recombination among parvoviruses from rodents. The topology of the phylogenetic tree of autonomous human and simian parvoviruses matched exactly the topology of the primate family tree, as based on the analysis of primate mitochondrial DNA. Viruses belonging to the AAV group were not evolutionarily linked to other primate parvoviruses but were linked to the parvoviruses of birds. The two lineages of human parvoviruses may have resulted from independent ancient zoonotic infections. Our results provide an argument for reclassification of Parvovirinae based on evolutionary relationships among viruses.     

Moving forward with the primate microbiome: Introduction to a special issue of the American Journal of Primatology

Primate microbiome research is a quickly growing field with exciting potential for informing our understanding of primate biology, ecology, and evolution as well as host‐microbe interactions more broadly. This introductory essay to a special section of the American Journal of Primatology provides a cross‐sectional snapshot of current activity in these areas by briefly summarizing the diversity of contributed papers and their relationships to key themes in host‐associated microbiome research. It then uses this survey as a foundation for consolidating a set of key research questions to broadly guide future research. It also argues for the importance of methods standardization to facilitate comparative analyses and the identification of generalizable patterns and relationships. While primatology will benefit greatly from the integration of microbial datasets, it is uniquely positioned to address important questions regarding microbiology and macro‐ecology and evolution more generally. We are eager to see where the primate microbiome leads us.     

Impact of the invasive parasitic copepod Mytilicola orientalis on native blue mussels Mytilus edulis in the western European Wadden Sea

Invasive species can indirectly affect native species by modifying parasite–host dynamics and disease occurrence. This scenario applies to European coastal waters where the invasive Pacific oyster (Magallana gigas) co-introduced the parasitic copepod Mytilicola orientalis that spills over to native blue mussels (Mytilus edulis) and other native bivalves. In this study, we investigated the impact of M. orientalis infections on blue mussels by conducting laboratory experiments using controlled infections with larval stages of the parasitic copepod. As the impact of infections is likely to depend on the mussels’ food availability, we also tested whether potential adverse effects of infection on mussels intensify under low food conditions. Blue mussels that were experimentally infected with juvenile M. orientalis had a significantly lower body condition (11–13%) compared with uninfected mussels after nine weeks of infection. However, naturally infected mussels from a mixed mussel and oyster bed did not significantly differ in body condition compared with uninfected mussels. Contrary to effects on mussel condition, we did not find an effect of experimental infections on clearance rates, shell growth or survival of blue mussels and no clear sign of exacerbating effects of food limitation. Our study illustrates that invasive species can indirectly affect native species via parasite co-introductions and parasite spillover. The results of this study call for the integration of such parasite-mediated indirect effects of invasions in impact assessments of invasive species.     

Some observations on the testicular changes in an acanthocephalan,Centrorhynchus corvi,in natural infections of the crow,Corvus splendens

Seasonal changes in the testes of an acanthocephalan, Centrorhynchus corvi, from natural infections of the crow, Corvus splendens, have been studied throughout the year. Histologically, three states of testicular activity, i.e. active, intermediate and inactive, have been distinguished. Worms with inactive testes are more frequent during winter and early spring, and those with active testes, during summer. The results are discussed in relation to season-mediated changes in host physiology and the possible mode of parasitic infections.     

Noninvasive Assessment of Gastrointestinal Parasite Infections in Free-Ranging Primates

Recent evidence of emerging human diseases with origins or likely transmission to humans, or both, that involve primates and a greater recognition of the risk of human pathogen transmission to free-ranging primates have raised awareness of the potential impact of zoonotic pathogen transmission on primate conservation and nonhuman primate and human health. As human population density continues to increase exponentially, speeding the reduction and fragmentation of primate habitats, greater human-primate contact is inevitable and even higher rates of pathogen transmission are likely. Thus interest has grown in collecting baseline data on patterns of parasitic infections in wild primate populations to provide an index of population health and to begin to assess and, to manage disease risks. Primatologists traditionally have been involved with such surveys through noninvasive assessment of gastrointestinal parasites. Unfortunately, previous studies have tended toward divergent methodologies, compromising the potential for longitudinal and comparative work. Here, I provide practical guidelines and standardized methodologies for the noninvasive assessment of gastrointestinal parasites of primates.

Few parasites,and no evidence for Wolbachia infections,in a freshwater ostracod inhabiting temporary ponds

Biological systems with asexual reproduction have often attracted research on parasites and host immune defence, because parasites are expected to be better able to exploit genetically less diverse populations. In addition, maternally inherited parasitic microorganisms such as Wolbachia can directly alter the reproductive systems of their hosts and induce parthenogenesis. In the freshwater ostracod Eucypris virens, both sexual and asexual reproduction is known, and we speculated that parasite pressures might help to explain their co‐existence. This species complex inhabits shallow, often eutrophic temporary water bodies, conditions that should provide ample opportunities for parasite infections. We surveyed natural populations of E. virens throughout its Europe‐wide range for natural parasites, and particularly tested for the presence of intracellular Wolbachia bacteria. Surprisingly, the results indicate that very few E. virens populations support parasite infections. We also found no evidence for the presence of Wolbachia in the populations screened. The results therefore show that parasitic infections do not play a role in the maintenance of sex in this system. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 207–216.     

Glycan microarray profiling of parasite infection sera identifies the LDNF glycan as a potential antigen for serodiagnosis of trichinellosis

Diagnostic methods for parasite infections still highly depend on the identification of the parasites by direct methods such as microscopic examination of blood, stool and tissue biopsies. Serodiagnosis is often carried out to complement the direct methods; however, few synthetic antigens with sufficient sensitivity and specificity are available. Here we evaluated a glycan microarray approach to select for synthetic glycan antigens that could be used for serodiagnosis of parasitic infections. Using a glycan array containing over 250 different glycan antigens, we identified GalNAcβ1–4(Fucα1–3)GlcNAc-R (LDNF) as a glycan antigen that is recognized by antibodies from Trichinella-infected individuals. We synthesized a neoglycoconjugate, consisting of five LDNF molecules covalently coupled to bovine serum albumin (BSA), and used this neoglycoconjugate as an antigen to develop a highly sensitive total-Ig ELISA for serological screening of trichinellosis. The results indicate that glycan microarrays constitute a promising technology for fast and specific identification of parasite glycan antigens to improve serodiagnosis of different parasitic infections, either using an ELISA format, or parasite-specific glycan arrays.     

Relationships between anaemia and parasitic infections in Kenyan schoolchildren: a Bayesian hierarchical modelling approach

Anaemia is multi-factorial in origin and disentangling its aetiology remains problematic, with surprisingly few studies investigating the relative contribution of different parasitic infections to anaemia amongst schoolchildren. We report cross-sectional data on haemoglobin, malaria parasitaemia, helminth infection and undernutrition among 1523 schoolchildren enrolled in classes 5 and 6 (aged 10–21 years) in 30 primary schools in western Kenya. Bayesian hierarchical modelling was used to investigate putative relationships. Children infected with Plasmodium falciparum or with a heavy Schistosoma mansoni infection, stunted children and girls were found to have lower haemoglobin concentrations. Children heavily infected with S. mansoni were also more likely to be anaemic compared with uninfected children. This study further highlights the importance of malaria and intestinal schistosomiasis as contributors to reduced haemoglobin levels among schoolchildren and helps guide the implementation of integrated school health programmes in areas of differing parasite transmission.