Gastrointestinal parasite infections and self-medication in wild chimpanzees surviving in degraded forest fragments within an agricultural landscape mosaic in Uganda

<div><p>Monitoring health in wild great apes is integral to their conservation and is especially important where they share habitats with humans, given the potential for zoonotic pathogen exchange. We studied the intestinal parasites of wild chimpanzees (<i>Pan troglodytes schweinfurthii</i>) inhabiting degraded forest fragments amid farmland and villages in Bulindi, Uganda. We first identified protozoan and helminth parasites infecting this population. Sixteen taxa were demonstrated microscopically (9 protozoa, 5 nematodes, 1 cestode, and 1 trematode). DNA sequence analysis enabled more precise identification of larval nematodes (e.g. <i>Oesophagostomum stephanostomum</i>, <i>O</i>. <i>bifurcum</i>, <i>Strongyloides fuelleborni</i>, <i>Necator</i> sp. Type II) and tapeworm proglottids (genus <i>Bertiella</i>). To better understand the ecology of infections, we used multidimensional scaling analysis to reveal general patterns of association among parasites, climate, and whole leaf swallowing–a prevalent self-medicative behaviour at Bulindi linked to control of nodular worms (<i>Oesophagostomum</i> spp.). Prevalence of parasites varied with climate in diverse ways. For example, <i>Oesophagostomum</i> sp. was detected in faeces at higher frequencies with increasing rainfall but was most clearly associated with periods of low temperature. Certain parasites occurred together within chimpanzee hosts more or less frequently than expected by chance. For example, the commensal ciliate <i>Troglodytella abrassarti</i> was negatively associated with <i>Balantidium coli</i> and <i>Oesophagostomum</i> sp., possibly because the latter taxa make the large intestine less suitable for <i>T</i>. <i>abrassarti</i>. Whole leaves in faeces showed independent associations with the prevalence of <i>Oesophagostomum</i> sp., <i>Strongyloides</i> sp., and hookworm by microscopic examination, and with egestion of adult <i>O</i>. <i>stephanostomum</i> by macroscopic inspection. All parasites identified to species or genus have been reported in wild chimpanzees inhabiting less-disturbed environments than Bulindi. Nevertheless, several disease-causing taxa infecting these chimpanzees are potentially transmissible between apes and humans (e.g. rhabditoid and strongyle nematodes), underscoring the importance of identifying and reducing risks of pathogen exchange in shared landscapes.</p></div

Home range and habitat of chimpanzees in Bulindi, Hoima District, Uganda.

<p><b>(a)</b> Map adapted from Landsat imagery courtesy of USGS/NASA Landsat. The most commonly used portion of the home range is indicated by the yellow oval. Dark green areas are fragments of riverine forest, <i>Cyperus papyrus</i> swamp, regenerating bush and woodland; the surrounding matrix comprises smallholder farmland, homes and trading centres. The thin line at centre is a main road connecting Hoima and Masindi towns. <b>(b)</b> Typical view of narrow riverine forest dominated by tall <i>Phoenix reclinata</i> palms; a chimpanzee is visible in a small tree above the water. <b>(c)</b> Two adult males of the Bulindi community travelling across farmland while a local farmer (visible between the two chimpanzees) tends to his garden.</p

Multidimensional scaling (MDS) model of independent associations among whole leaf swallowing, rainfall, and six parasites with known or likely pathogenicity.

<p>The first-order dimension represents a stronger association than the second-order dimension. The closer two or more variables are, the more likely they covary independently of other points on the map. Colours differentiate groups of variables that show some degree of association in relation to other variables in the map.</p

Multidimensional scaling (MDS) model of independent associations among parasites.

<p>The first-order dimension represents a stronger association than the second-order dimension. The closer two or more variables are, the more likely they covary independently of other points on the map. Colours differentiate groups of variables that show some degree of association in relation to other variables in the map. Only parasites detected in >5% of faecal samples were included in the model.</p

Gastrointestinal parasites and symbionts found from coproscopic analysis of faeces of chimpanzees in Bulindi, Uganda.

<p><b>(a)</b> Protozoa: 1. <i>Troglodytella abrassarti</i>; 2. <i>Balantidium coli</i> (trophozoite); 3. <i>Balantidium coli</i> (cyst); 4. <i>Troglocorys cava</i>; 5. <i>Entamoeba coli</i>; 6. <i>Entamoeba</i> sp.; 7. <i>Iodamoeba buetschlii</i>; 8. <i>Giardia intestinalis</i>; 9. <i>Chilomastix mesnili</i>; 10. <i>Blastocystis</i> sp. <b>(b)</b> Helminths: 11. Dicrocoeliidae gen. sp.; 12. <i>Bertiella</i> sp.; 13. Spiruridae gen. sp.; 14. Hookworm; 15. <i>Oesophagostomum</i> sp.; 16. <i>Strongyloides</i> sp. (egg); 17. <i>Strongyloides</i> sp. (larva); 18. <i>Probstmayria gombensis</i> (adult).</p

Prevalence of microscopic and macroscopic gastrointestinal parasite taxa in faeces of chimpanzees in Bulindi, Uganda, during the two survey periods (1 = Sep–Nov 2012; 2 = Feb–Apr 2013).

<p>Prevalence of microscopic and macroscopic gastrointestinal parasite taxa in faeces of chimpanzees in Bulindi, Uganda, during the two survey periods (1 = Sep–Nov 2012; 2 = Feb–Apr 2013).</p

Temporal variation in leaf swallowing in relation to parasite infections and rainfall during the two survey periods.

<p><b>Top</b>: bars show the biweekly mean (± SD) number of infections by different parasites with pathogenic potential, determined by coproscopy (see text). <b>Bottom</b>: Lines show the % biweekly faeces containing wholly swallowed leaves and the biweekly prevalence in samples of potentially pathogenic nematodes (<i>Oesophagostomum</i> sp., <i>Strongyloides</i> sp. and hookworm); bars show biweekly rainfall. The patterning of rainfall bars indicate whether biweekly periods were in months classified as wet (solid), transient (hatched) or dry (vertical lines); see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0180431#sec002" target="_blank">Methods</a>. The number of faecal samples inspected per biweekly period (microscopically; macroscopically): <i>Period 1</i> –Sep.2 (33; 28), Oct.1 (46; 43), Oct.2 (30; 30), Nov.1 (32; 33), Nov.2 (31; 30); <i>Period 2</i> –Feb.2 (14; 21), Mar.1 (91; 81), Mar.2 (65; 61), Apr.1 (55; 46), Apr.2 (35; 33).</p

Within-host associations among parasites in chimpanzee faecal samples in Bulindi ^a.

<p>Within-host associations among parasites in chimpanzee faecal samples in Bulindi <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0180431#t004fn001" target="_blank">^a</a>.</p

Summary of DNA sequence analysis of larval nematodes from coprocultures (n = 38).

<p>Summary of DNA sequence analysis of larval nematodes from coprocultures (n = 38).</p

Parasite prevalence in wet months (>100 mm rainfall) and dry and transient months (≤100 mm rainfall) compared.

<p>Parasite prevalence in wet months (>100 mm rainfall) and dry and transient months (≤100 mm rainfall) compared.</p