Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees

Abstract

When physiological adaptation is insufficient, hosts have developed behavioral responses to avoid or limit contact with parasites. One such behavior, leaf-swallowing, occurs widely among the African great apes. This behavior involves the slow and deliberate swallowing without chewing of whole bristly leaves. Folded one at a time between tongue and palate, the leaves pass through the gastro-intestinal (GI) tract visibly unchanged. Independent studies in two populations of chimpanzees (Pan troglodytes schweinfurthii) showed significant correlations between the swallowing of whole leaves and the expulsion of the nodule worm Oesophagostomum stephanostomum and a species of tapeworm (Bertiella studeri). We integrate behavioral, parasitological and physiological observations pertaining to leaf-swallowing to elucidate the behavioral mechanism responsible for the expulsion and control of nodule worm infections by the ape host. Physical irritation produced by bristly leaves swallowed on an empty stomach, increases motility and secretion resulting in diarrhea which rapidly moves leaves through the GI tract. In the proximal hindgut, the site of third-stage larvae (L3) cyst formation and adult worm attachment, motility, secretion and the scouring effect of rough leaves is enhanced by haustral contractions and peristalsis-antiperistalsis. Frequently, at the peak of reinfection, a proportion of nonencysted L3 is also predictably vulnerable. These factors should result in the disruption of the life cycle of Oesophagostomum spp. Repeated flushing during peak periods of reinfection is probably responsible for long-run reduction of worm burdens at certain times of the year. Accordingly, leaf-swallowing can be viewed as a deliberate adaptive behavioral strategy with physiological consequences for the host. The expulsion of worms based on the activation of basic physiological responses in the host is a novel hitherto undescribed form of parasitic control.