A survey of gastrointestinal parasites of olive baboons (Papio anubis) in human settlement areas of Mole National Park, Ghana

Fecal samples from 55 free-ranging olive baboons (Papio anubis) in Mole National Park, Ghana, were collected 22 June-7 July 2008 and analyzed for gastrointestinal parasites. This is the first survey of baboon gastrointestinal parasites in Ghana and provides baseline data for this area. Ninety-three percent of samples were infected, leaving 7% with no parasites observed. Of those infected, there was a 76% prevalence of strongyles, 53% Strongyloides spp., 11% Abbreviata caucasica , 62% prevalence of Balantidium coli (trophozoites and cysts identified), 4% Entomeba hystolytica/dispar, and 47% unidentified protozoan parasites. Of the strongyle infections, 9% were identified as Oesophagostamum sp. One sample contained an unidentified spirurid nematode that resembled Gongylonema sp. Mole has a mixed forest-savanna habitat, and baboons frequently range into human areas, which makes them subject to parasites from each habitat and multiple sources of exposure. We found a high prevalence of nematode parasites, consistent with a wet or cooler forest environment, or high rates of fecal contamination. The presence of Strongyloides sp., E. hystolitica/dispar, and B. coli suggest potential public health risk from baboons, but molecular identification of these parasites, and documentation of their presence in local human populations, would be necessary to confirm zoonotic transmission.     

Gastrointestinal parasites of the colobus monkeys of Uganda

From August 1997 to July 2003, we collected 2,103 fecal samples from free-ranging individuals of the 3 colobus monkey species of Uganda-the endangered red colobus (Piliocolobus tephrosceles), the eastern black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus (C. angolensis)--to identify and determine the prevalence of gastrointestinal parasites. Helminth eggs, larvae, and protozoan cysts were isolated by sodium nitrate flotation and fecal sedimentation. Coprocultures facilitated identification of helminths. Seven nematodes (Strongyloides fulleborni, S. stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 3 protozoans (Entamoeba coli, E. histolytica, and Giardia lamblia) were detected. Seasonal patterns of infection were not apparent for any parasite species infecting colobus monkeys. Prevalence of S. fulleborni was higher in adult male compared to adult female red colobus, but prevalence did not differ for any other shared parasite species between age and sex classes.     

Gastrointestinal parasites of the guenons of western Uganda

From January 1998 to December 2002, we collected 293 fecal samples from free-ranging individuals of the 4 guenon species of western Uganda, i.e., redtail guenons (Cercopithecus ascanius), blue monkeys (Cercopithecus mitis), l'hoesti monkeys (Cercopithecus lhoesti), and vervet monkeys (Cercopithecus aethiops), to quantify the prevalence of gastrointestinal parasites. Helminth eggs, larvae, and protozoan cysts were isolated by sodium nitrate flotation and fecal sedimentation. Helminth parasites were identified, and infection prevalence was determined for all 4 guenon species. Coprocultures facilitated identification of strongylate nematodes. For the most common species, the redtail guenon, we documented prevalence of protozoan parasites and examined the effect of season and host sex on infection prevalence. Six nematodes (Strongyloidesfulleborni, Oesophagostomum sp., unidentified strongyle, Trichuris sp., Streptopharagus sp., and Enterobius sp.), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 5 protozoans (Entamoeba coli, Entamoeba histolytica, lodameoba butschlii, Giardia lamblia, and Chilomastix mesnili) were detected. Seasonal patterns of infection were not readily apparent for any parasite species infecting redtail guenons. Although prevalence never differed between male and female guenons, only adult females were infected with Oesophagostomum sp. and S. fulleborni.     

Biomorphology of gastrointestinal nematodes of small ruminants

Under the term gastrointestinal nematodes are included numerous parasites species of livestock belonging to the families Strongyloididae (Strongyloides), Strongylidae (Chabertia, Oesophagostomum) Trichostrongylidae (Trichostrongylus, Ostertagia, Teladorsagia, Cooperia, Marshallagia), Molineidae (Nematodirus), Ancylostomatidae (Bunostomum) and Trichuridae (Trichuris). This paper reviews the biomorphology aspects of these parasites as well as the controversy by the taxonomists in the classifications.     

Annual follow-up of the gastrointestinal parasitosis of the tepezcuintle,Agouti paca (Rodentia: Agoutidae) in captivity in the Mexican tropic

Previous reports showed that the tepezcuintle (Agouti paca) is commonly infested by gastrointestinal parasites (GIP), mainly Eucoccidiida and helminths. However, there is no available information on the frequency of those parasites and their faecal egg excretions at different moments during the year. These information would provide a valuable baseline for the establishment of control strategies against GIP in tepezcuintles under captivity. The objectives of the present study were to determine the prevalence of GIP orders and genera that infest tepezcuintles under captivity and, to describe the dynamics of faecal egg and oocyst excretion in a year. Ten tepezcuintles were sampled (faeces) twice every month for twelve months. The faecal samples were processed by the flotation and McMaster techniques. Two orders of parasites were determined: Strongylida and Eucoccidiida. Two genera of nematodes were also determined: Strongyloides and Trichuris. The prevalence of Strongylida eggs, Eucoccidiida oocysts and Trichuris sp. eggs reached 10-20% of animals in certain months. The most important genus was Strongyloides, found in 60 to 100% of the animals year round. The average excretion of eggs in the group was 45 to 372 eggs per gram. Tepezcuintles kept under captivity in Yucatan are parasited with Strongyloides sp throughout the year, but only occasionally had oocysts of Eucoccidiida and eggs of Strongylida and Trichuris sp.     

Gastrointestinal Parasites of Savanna Chimpanzees (Pan troglodytes schweinfurthii) in Ugalla,Tanzania

Understanding variability in patterns of parasite infections requires studies of multiple populations inhabiting a variety of habitats. Gastrointestinal parasites of chimpanzees (Pan troglodytes) have been studied extensively at several forested sites, but the parasite fauna of chimpanzees living in dry, open habitats is less well known. We studied the parasites of savanna chimpanzees (Pan troglodytes schweinfurthii) living in the Issa Valley, Ugalla (Tanzania). We examined 119 fresh fecal samples using standard coproscopical methods. We detected protozoans including Blastocystis sp., Entamoeba coli, E. histolytica/dispar, Iodamoeba buetschlii, Troglodytella abrassarti, and Troglocorys cava, but only two types of spirurid nematodes among the helminths. The parasites of the Ugalla chimpanzees differ from those of forest chimpanzees in the absence of Strongyloides sp. and strongylid nematodes and a high prevalence of spirurids. Strongylids and Strongyloides sp. have thin-shelled eggs and larvae, which develop in the external environment; thus they may not be able to survive for prolonged periods in the extreme environment of Ugalla. The Ugalla chimpanzees also live at a lower population density and exhibit a larger home range than forest chimpanzees, factors that may lead to lower exposure to infective nematode larvae. Spirurid eggs, however, have thick shells and a life cycle dependent on intermediary hosts, making their survival and transmission in such extreme conditions more feasible. These differences between parasite fauna of closed and open forest chimpanzees contribute to our understanding of the ecology of infectious disease, and have the potential to contribute to conservation policies and practices.     

Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups

Humans are responsible for massive changes to primate habitats, and one unanticipated consequence of these alterations may be changes in host-parasite interactions. Edges are a ubiquitous aspect of human disturbance to forest landscapes. Here we examine how changes associated with the creation of edges in Kibale National Park, Uganda, alter the parasite community that is supported by two species of African colobines: the endangered red colobus (Piliocolobus tephrosceles) and the black-and-white colobus (Colobus guereza). An analysis of 822 fecal samples from edge and forest interior groups revealed no difference in the richness of parasite communities (i.e., the number of parasite species recovered from the host's fecal sample). However, for both species the proportion of individuals with multiple infections was greater in edge than forest interior groups. The prevalence of specific parasites also varied between edge and forest interior groups. Oesophagostomum sp., a potentially deleterious parasite, was 7.4 times more prevalent in red colobus on the edge than in those in the forest interior, and Entamoeba coli was four times more prevalent in red colobus on the edge than in animals from the forest interior. Environmental contamination with parasites (measured as parasite eggs/gm feces) by red colobus from the edge and forest interior differed in a similar fashion to prevalence for red colobus, but it did not differ for black-and-white colobus. For example, egg counts of Oesophagostomum sp. were 10 times higher in red colobus from the edge than in those from the interior. The less severe infections in the black-and-white colobus relative to the red colobus may reflect the fact that black-and-white colobus raid agricultural crops while red colobus do not. This nutritional gain may facilitate a more effective immune response to parasites by the black-and-white colobus. The fact that animals on the edge are likely not nutritionally stressed raises an intriguing question as to what facilitates the elevated infections in edge animals. We speculate that interactions with humans may be linked to the observed patterns of infections, and hence that understanding the ecology of infectious diseases in nonhuman primates is of paramount importance for conservation and potentially for human-health planning.     

Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest

Forest fragmentation may alter host-parasite interactions in ways that contribute to host population declines. We tested this prediction by examining parasite infections and the abundance of infective helminths in 20 forest fragments and in unfragmented forest in Kibale National Park, Uganda. Over 4 years, the endangered red colobus (Procolobus rufomitratus) declined by 20% in fragments, whereas the black-and-white colobus (Colobus guereza) in fragments and populations of both colobines in unfragmented forest remained relatively stable. Seven nematodes (Strongyloides fulleborni, Strongyloides stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), one cestode (Bertiella sp.), and three protozoans (Entamoeba coli, Entamoeba histolytica/dispar, and Giardia sp.) were detected. Infection prevalence and the magnitude of multiple infections were greater for red colobus in fragmented than in unfragmented forest, but these parameters did not differ between forests for black-and-white colobus. Infective-stage colobus parasites occurred at higher densities in fragmented compared with unfragmented forest, demonstrating greater infection risk for fragmented populations. There was little evidence that the nature of the infection was related to the size of the fragment, the density of the host, or the nature of the infection in the other colobine, despite the fact that many of the parasites are considered generalists. This study suggests that forest fragmentation can alter host-parasite dynamics and demonstrates that such changes can correspond with changes in host population size in forest fragments.     

Occurrence of Gasterophilus intestinalis and some Parasitic Nematodes of Horses in Sweden

A survey was performed on the occurrence of some internal parasites in 461 horses (1–30 years old) slaughtered from October 1992 to September 1993 at the Linköping abattoir in central Sweden. Macroscopical examination was carried out specifically for parasites of the tear ducts and conjunctival sacs of the eyes, and of selected parts of the alimentary tract and car-dio-vascular system. The following parasites were found in selected parts of the large intestine: encapsulated cyathostome larvae (in 35.6% of the horses), and mature strongyle worms (17.4%); in the stomach: Gasterophilus intestinalis (12.3% during October-June) and Habronema muscae (1.1%); and in the conjunctival sac: Thelazia lacrymalis (3.1%). Significantly more encapsulated cyathostome larvae were found during January to June than during other times of the year, and horses aged 1–5 years harboured significantly more larvae than older horses. Severe damage to the cranial mesenteric artery and its main branches was noticed in 16 (6.1%) out of 263 horses specifically examined. However, the 4th stage larva of Strongylus vulgaris was only recovered in 6 (2.3%) of the horses. Quantitative and qualitative faecal egg counts were done on 412 and 384 of the horses, respectively. Eggs of strongyles, Parascaris equorum and Strongyloides westeri were found in 78.1%, 1.9% and 0.2% of the faecal samples, respectively. Highest prevalence of strongyle eggs was found during July to September. Third stage larvae of the following nematodes were recovered from faecal cultures: subfamily Cyathostomum sensu lato (78.1%) Triodontophorus spp. (6.5%), Strongylus vulgaris (3.6%), Trichostrongylus axei (1.3%), while Gyalocephalus sp., Oesophagodontus sp., Poteriostomum sp. and Strongylus edentatus each comprised less than 0.5%.     

Prevalence of metazoan parasite infections in five species of Asian macaques.

Necropsy examination was performed on a total of 697 wild-caught macaques of five species. Helminthic parasites were found to be prevalent among these macaques, with species of Strongyloides, Oesophagostomum, Anatrichosoma, Trichostrongylus, and Gongylonema being the most common patent infections. Some of the larval stages of nematodes (ascarids, spirurids), cestodes (hydatid, Sparganum), and pentastomids grew into adults in appropriate definitive hosts upon experimental feeding, enabling species identification.     

Gastro-intestinal helminths in a natural population ofMacaca sinica andPresbytis spp. at Polonnaruwa,Sri Lanka

Helminth parasites were identified in a natural population of primates at Polonnaruwa, Sri Lanka. Five fatally wounded or recently deceased toque macaques (Macaca sinica) and three langurs (Presbytis senex andP. entellus) were autopsied. The following nematodes were found:Oesophagostomum aculeatum (Chabertiidae),Streptopharagus pigmentata (Spirocercidae),Physaloptera sp. (Spiruridae),Enterobius vermicularis (Oxyuridae), andTrichuris trichiura (Trichuridae). One cestode,Hymenolepis was also recovered fromP. entellus. Among fresh faecal samples of 210M. sinica, worm eggs ofOesophagostomum andStrongyloides were most abundant, followed byTrichostrongylus. Trichuris andStreptopharagus eggs were found occasionally.     

Molecular identification of oesophagostomum and Trichuris eggs isolated from wild Japanese macaques

Natural habitat fragmentation and reducing habitat quality have resulted in an increased appearance of Japanese macaques, Macaca fuscata (Gray, 1870), in suburban areas in Japan. To investigate the risk of zoonotic infections, a coprological survey of helminth eggs passed by wild Japanese macaques was carried out in 2009 and 2010 in Shiga Prefecture, Japan. Microscopic examination found helminth eggs in high prevalence, and nucleotide sequencing of DNA extracted from the eggs identified Oesophagostomum cf. aculeatum and Trichuris trichiura. A fecal culture also detected infective larvae of Strongyloides fuelleborni. These zoonotic nematodes pose a potential health issue to local people in areas frequented by Japanese macaques.     

Risk factor analysis for the prevalence of gastrointestinal parasites found in large ruminants in Lower Dir Khyber Pakhtunkhwa Pakistan

The present study was designed to investigate the prevalence of gastrointestinal (GI) parasites in cattle and buffaloes of Lower Dir Khyber Pakhtunkhwa, Pakistan. The presence of the eggs, cysts, and oocysts of GI parasites in fecal samples were detected using direct smear methods and concentration techniques including floatation, centrifugation, and sedimentation. Identification of recovered fecal stages were determined by morphology using size and appearance of the recovered eggs, cysts, and oocysts. A total of 314 fecal samples were collected from the different Tehsils (Administrative Districts) and analyzed through microscopy. A higher prevalence was observed in the buffalo than the cow population. A total of 184 samples were positive for GI parasites of which 109/196 (55.61%) were from cattle, whereas 75/118 (63.55%) were from buffaloes. The minimum number of strongyle eggs detected in all the samples were 136.39 eggs/g (EPG). The mean EPG in cattle was 143.30 and 122.56 in buffaloes. The open-source water prevalence of GI parasites was higher than the other sources in cattle and the second highest after tap water in buffaloes. The seasonal prevalence of GI parasites ranged from 32.39% (23/71), in spring to 68.8% (86/125) in summer in cattle. In was For buffaloes the infection prevalence was 52.94% (27/51) and 71.64% (48/67) in spring and summer, respectively. Gastrointestinal parasites are a serious problem in cattle and buffaloes in the lower district of Dir Khyber Pakhtunkhwa Pakistan. In general, the burden of parasitic infection was low in most animals that received previous anti-parasitic treatment.     

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.     

Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda

Numerous intestinal parasites identified in populations of wild nonhuman primates can be pathogenic to humans. Furthermore, nonhuman primates are susceptible to a variety of human pathogens. Because of increasing human encroachment into previously nonimpacted forests, and the potential for disease transmission between human and nonhuman primate populations, further detailed investigations of primate ecological parasitology are warranted. For meaningful comparisons to be made, it is important for methods to be standardized across study sites. One aspect of methodological standardization is providing reliable estimates of parasite prevalence and knowing how many samples are needed to adequately estimate an individual's parasite prevalence. In this study the parasitic fauna of 37 adult, adolescent, and juvenile male chimpanzees from the Ngogo group, Kibale National Park, Uganda, were assessed from 121 fecal samples collected over a 3-month period. Twelve taxa of intestinal species (five helminth and seven protozoan) were recovered from the samples. The four most prevalent species were Troglodytella abrassarti (97.3%), Oesophagostomum sp. (81.1%), Strongyloides sp. (83.8%), and Entamoeba chattoni (70.3%). No one species was found in all samples from any one animal, and Troglodytella abrassarti, the most common intestinal organism, was found in all of the serial samples of only 69.4% of the chimpanzees. The cumulative species richness for individuals significantly increased for every sequential sample (up to three to four samples) taken per animal during this study. The results indicate that to accurately diagnose total intestinal infection and evaluate group prevalence, three to four sequential samples from each individual must be collected on nonconsecutive days. This conclusion applies only to short study periods in which possible seasonal effects are not taken into consideration. Validation of these results at different study sites in different regions with different climatic patterns is needed.     

Coprology of Panthera tigris altaica and Felis bengalensis euptilurus from the Russian Far East

Fecal samples from the Siberian tiger (Panthera tigris altaica) and the Amur cat (Felis bengalensis euptilurus) from Far Eastern Russia, were examined for parasites. A natural sedimentation methodology was used and a complete examination of all the sediment was performed. This fecal investigation allowed us to isolate and identify several developmental stages of gastrointestinal, hepatic, and respiratory parasites. Five parasites were found from P. t. altaica: 11 trematodes (Platynosomum fastosum) and 4 nematodes (Strongyloides sp., Ancylostomatidae, Toxascaris leonina, and Toxocara cati). Five parasites were found from F. b. euptilurus: 1 cestode (Diplopylidium sp.) and 4 nematodes (Trichuris sp., Ancylostomatidae, Toxascaris leonina, and Aelurostrongylus abstrusus). In addition, trophozoites of the amoeba Acanthamoeba sp. were detected in tiger feces.     

Gastrointestinal Parasites in Free-Ranging Kenyan Baboons (Papio cynocephalus and P. anubis)

We screened fecal samples from 3 groups of wild-living baboons (Papio cynocephalus and P. anubis), involved in longitudinal behavioral studies, for evidence of gastrointestinal parasites. The two objectives of the study were: 1) to compare parasites from two of the groups with different foraging behavior from the same area and 2) to obtain fecal parasitic data on 3 groups of baboons to provide baseline reference data. We sampled individual baboons opportunistically from Lodge and Hook's groups, Amboseli National Park and from Mpala Group, Mpala Wildlife Research Centre, Kenya. Lodge Group baboons supplemented foraging on wild foods by daily foraging in human-source refuse, whereas Hook's and Mpala groups did not. We collected fecal samples from 55, 30 and 42 individuals in Hook's, Lodge and Mpala groups, respectively, and processed them via ether sedimentation. We identified strongylids, Streptopharagus sp., Physaloptera sp., Trichuris sp., Enterobius sp., and Strongyloides sp., in the feces, but no parasite directly attributable to exposure to people. Garbage- and wild-feeding Amboseli baboons differed in the prevalence of Streptopharagus sp., Physaloptera sp. and Trichuris sp.     

Patterns of parasitic infections in faecal samples from stray cat populations in Qatar

The parasite fauna of stray cat populations, comprising mainly helminth parasites, is described for the first time from the arid environment of the Qatar peninsula. During the winter and summer months of 2005, 824 faecal samples were examined from six sites in Qatar. Up to seven species of parasites were identified, six of which were nematodes - Strongyloides stercoralis as the most prevalent (18.4%), followed by Aelurostrongylus abstrusus (7.5%), Toxocara cati (6.1%), Ancylostoma tubaeforme (5.9%) and Physaloptera sp. (4.8%) and Toxascaris leonina (0.7%) - and one sporozoan species, Isospora felis (0.5%). Unidentified cestode eggs were also recovered from 10.7% of samples examined. The parasite species were found to be highly overdispersed in faecal samples from all sites, whereas the prevalence and intensity of infections were influenced by site and season. Infection levels tended to be higher during the winter season, especially in the case of A. abstrusus and A. tubaeforme, when conditions of temperature and humidity were more favourable for the development of egg and/or larval stages of parasites compared with the extremely hot and dry summer months. The results are discussed in relation to the distribution of the cat population in the vicinity of Doha and its outskirts and the potential threat of parasite transmission to human communities in Qatar.     

Multiple anthelmintic resistance in gastrointestinal nematodes of small ruminants in Bangladesh

Anthelmintic resistance (AR) against gastrointestinal nematodes (GINs) of sheep and goats is a global concern. To address the problem, this study assessed the status of AR in different government and private sheep and goat farms in Bangladesh. We conducted fecal egg count reduction test (FECRT) and Egg hatch assay (EHA) experiments. For the detection of resistant larvae, pooled fecal samples from treated and non-treated groups were subjected to coproculture. Furthermore, 195 adult Haemonchus parasites were genotyped to ascertain benzimidazole (BZ) resistance allele from seven topographic zones of Bangladesh using allele specific PCR (AS-PCR). In FECRT, the percentage reduction along with 95% confidence intervals indicated that GINs were resistant to albendazole (ABZ), levamisole (LEV) and ivermectin (IVM). Coproculture revealed that Haemonchus spp., Oesophagostomum spp. and Trichostrongylus spp. were resistant to anthelmintics. ABZ resistance was also confirmed by in vitro EHA in all the farms except the private goat farm in Mymensingh. The genotype frequencies were 6% for homozygous resistant (rr), 59% for heterozygous (rS) and 35% for homozygous susceptible (SS) among different topographic zones. The allelic frequency of the mutation conferring resistance (r) ranged from 25% to 47% signifying resistance to BZ in nematodes of sheep/goats. The genotype frequencies (rr, rS and SS) and allelic frequencies (r and S) varied significantly (p˂0.05) in different zones in Bangladesh. Overall, the data suggest an alarming condition created by multiple AR in Bangladesh.     

Host age,sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques

Parasites are characteristically aggregated within hosts, but identifying the mechanisms underlying such aggregation can be difficult in wildlife populations. We examined the influence of host age and sex over an annual cycle on the eggs per gram of feces (EPG) of nematode parasites infecting wild Japanese macaques (Macaca fuscata yakui) on Yakushima Island. Five species of nematode were recorded from 434 fecal samples collected from an age-structured group of 50 individually recognizable macaques. All parasites exhibited aggregated EPG distributions. The age–infection profiles of all three directly transmitted species (Oesophagostomum aculeatum, Strongyloides fuelleborni, and Trichuris trichiura) exhibited convex curves, but concavity better characterized the age–infection curves of the two trophically transmitted species (Streptopharagus pigmentatus and Gongylonema pulchrum). There was a male bias in EPG and prevalence of infection with directly transmitted species, except in the prevalence of O. aculeatum, and no sex bias in the other parasites. Infection with O. aculeatum showed a female bias in prevalence among young adults, and additional interactions with sex and seasonality show higher EPG values in males during the mating season (fall) but in females during the birth season (spring). These patterns suggest that an immunosuppressive role by reproductive hormones may be regulating direct, but not indirect, life-cycle parasites. Exposure at an early age may trigger an immune response that affects all nematodes, but trophically transmitted species appear to accumulate thereafter. Although it is difficult to discern clear mechanistic explanations for parasite distributions in wildlife populations, it is critical to begin examining these patterns in host species that are increasingly endangered by anthropogenic threats.