High Frequency of Leaf Swallowing and its Relationship to Intestinal Parasite Expulsion in “Village” Chimpanzees at Bulindi, Uganda

Abstract

Self-medication by great apes to control intestinal parasite infections has been documented at sites across Africa. Chimpanzees (Pan troglodytes) swallow the leaves of certain plant species whole, without chewing. Previous studies demonstrated a relationship between chimpanzee leaf swallowing and expulsion of nematode worms (Oesophagostomum sp.) and tapeworms (Bertiella sp.) in dung. We investigated the relationship between leaf swallowing and parasite expulsion in chimpanzees inhabiting a fragmented forest-farm mosaic at Bulindi, Uganda. During 13 months whole undigested leaves occurred in chimpanzee dung at a considerably higher frequency (10.4% of dungs) than at other sites (0.4-4.0%). Leaf swallowing occurred year-round and showed no pronounced seasonality. Chimpanzees egested adults of multiple species of Oesophagostomum (including O. stephanostomum) and proglottids of two tapeworms-Bertiella sp. and probably Raillietina sp. The latter may not be a true infection, but the byproduct of predation on domestic fowl. Compared to previous studies, the co-occurrence of whole leaves and parasites in chimpanzee dung was low. Whereas the presence of leaves in dung increased the probability of adult nematode expulsion, no association between leaf swallowing and the shedding of tapeworm proglottids was apparent. Anthropogenic habitat changes have been linked to alterations in host-parasite interactions. At Bulindi, deforestation for agriculture has increased contact between apes and people. Elevated levels of leaf swallowing could indicate these chimpanzees are especially vulnerable to parasite infections, possibly due to environmental changes and/or increased stress levels arising from a high frequency of contact with humans. Frequent self-medication by chimpanzees in a high-risk environment could be a generalized adaptation to multiple parasite infections that respond differently to the behavior. Future parasitological surveys of apes and humans at Bulindi are needed for chimpanzee health monitoring and management, and to investigate the potential for disease transmission among apes, people, and domestic animals.

Leaf swallowing and parasitic infection of the Chinese lesser civet Viverricula indica in northeastern Taiwan

“…It is clear that the civets obtained very little, if any, nutritional or energetic benefit from this type of ingestive behavior. Ingesting grass leaves by the Chinese lesser civet may function to remove Toxocara worms, which live in the intestinal lumen and share several life history traits in common with Oesophagostomum, another nematode species (Anderson 2000;Holland and Smith 2006) closely associated with leaf swallowing in chimpanzee and bonobo populations across Africa (Huffman 1997(Huffman , 2010Dupain et al 2002;Fowler et al 2007;McLennan and Huffman 2012). At the very least, these data suggest that infections by this parasite stimulate the swallowing of grass by the civet and point toward a relationship between leaf swallowing and the expulsion of parasites, as noted for other wild carnivore species (Murie 1944;Huffman 1997).…”

“…The leaves go through the digestive tract and appear in the feces folded and undigested along with either Oesophagostomum stephanostomum (Nematoda) adult worms or Bertiella sturderi (Cestoda) proglottids (Wrangham 1995;Huffman et al 1996Huffman et al , 2009Huffman and Caton 2001). The co-occurrence of folded, undigested leaves and these parasites was statistically significant at sites where the behavior has been studied in detail (e.g., Oesophagostomum: Huffman et al (1996), McLennan and Huffman (2012) and Bertiella: Wrangham (1995)). Furthermore, ingesting leaves was positively correlated with the seasonal increase in the intensity of infection by these parasites in chimpanzees at these sites (Huffman et al 1997).…”

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

“…Swallowing rough or bristly leaves increases gut motility causing expulsion of adult worms, which disrupts the nematode’s life cycle and likely reduces worm burdens [53]. Thus, whole undigested leaves occurred in association with adult Oesophagsotomum in chimpanzee faeces at Mahale [52] and also at Bulindi, Uganda [54]. A similar relationship between leaf swallowing and tapeworm ( Bertiella sp.)…”

Research with Chemistry and Pharmacology of Natural Products in Brazil: A Comparison with 70 Selected Countries from 5 Continents

“…Chemical substances with pharmacological properties have been isolated from marine organisms (algae, phytoplankton, sponges, cnidarians, bryozoans, mollusks, echinoderms, shrimps, sea cucumbers and fishes), 34- [182][183][184][185][186][187][188][189][190][191] Scientists are now interested not only in the isolation and identification of these natural products, but also in deciphering how living organisms detect them, how (or why) they perceive them to act as they do and the synergy and mechanisms of action of the active principles responsible for their biological (and sometimes therapeutic) activities.…”