Leaf-swallowing by chimpanzees: A behavioral adaptation for the control of strongyle nematode infections

Huffman, Michael A.; Page, Jonathan E.; Sukhdeo, M. V. K.; Gotoh, Saki; Kalunde, Mohamedi Seifu; Chandrasiri, Thushara; Towers, G.H.N.

doi:10.1007/bf02735188

Cited by 106 publications

(147 citation statements)

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“…From non-invasive parasitological surveys of chimpanzees and seven other non-human primate species at Kibale National Park, Uganda, high prevalences of Oesophagostomum eggs were observed (8.3 -85 %) (Krief et al, 2005;Bezjian et al, 2008;Ghai et al, 2014). From similar surveys of chimpanzees in Gambo Stream and Mahale National Parks, Tanzania, fairly high prevalences of Oesophagotomus eggs were recorded (38 -91 %) (File et al, 1976;Huffman et al, 1996Huffman et al, , 1997. For Oesophagostomum samples collected from Mahale chimpanzees, the species identification as O. stephanostomum had been made based on morphology of expelled adult worms in the feces after natural medical plant use of the primate, as well as coprocultured larvae (Huffman et al, 1996, Huffman & Caton, 2001.…”

Section: Discussionmentioning

confidence: 99%

“…From similar surveys of chimpanzees in Gambo Stream and Mahale National Parks, Tanzania, fairly high prevalences of Oesophagotomus eggs were recorded (38 -91 %) (File et al, 1976;Huffman et al, 1996Huffman et al, , 1997. For Oesophagostomum samples collected from Mahale chimpanzees, the species identification as O. stephanostomum had been made based on morphology of expelled adult worms in the feces after natural medical plant use of the primate, as well as coprocultured larvae (Huffman et al, 1996, Huffman & Caton, 2001. Recent molecular genetic studies have demonstrated that the ITS2 nucleotide sequence of rDNA allows an unequivocal identification of a range of strongylid nematode species, irrespective of the developmental stage of parasites.…”

Section: Discussionmentioning

confidence: 99%

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Prevalence and genetic diversity of Oesophagostomum stephanostomum in wild lowland gorillas at Moukalaba-Doudou National Park, Gabon

et al. 2014

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Using a sedimentation method, the prevalence of the nodular worm Oesophagostomum stephanostomum (Nematoda: Strongylida) in western lowland gorillas at Moukalaba-Doudou National Park (MDNP), Gabon, was determined in fecal samples collected between January 2007 and October 2011, along with their coprocultures. Concurrently, possible zoonotic Oesophagostomum infections in villagers living near MDNP were assessed from their fecal samples collected during October and November of 2011. In the gorillas, strongylid (Oesophagostomum and/or hookworm) eggs were found in 47 of 235 fecal samples (20.0 %) and Oesophagostomum larvae were detected in 101 of 229 coprocultures (44.1 %). In the villagers, strongylid eggs were found in 9 of 71 fecal samples (12.7 %), but no Oesophagostomum larvae were detected in coprocultures. The internal transcribed spacer (ITS) region of ribosomal RNA gene (rDNA) and cytochrome c oxidase subunit-1 (cox-1) region of mitochondrial DNA (mtDNA) of coprocultured Oesophagostomum larvae were amplified using parasite DNA extracted from 7–25 larvae/sample, cloned into Escherichia coli, and sequenced. Sequenced rDNA contained 353/354-bp long ITS1, 151-bp long 5.8S rDNA, and 227-bp long ITS2. Parts of clones showed variations at 1–3 bases in the ITS1 region at a frequency of 24/68 (35.3 %) and at 1–2 bases in the ITS2 region at a frequency of 7/68 (10.3 %), whereas the 5.8S rDNA was essentially identical. Sequenced cox-1 gene of the parasites, 849 bp in length, showed a higher number of nucleotide variations, mainly at the third nucleotide position of the codon. The majority of clones (27/41 (65.9 %)) had an identical amino acid sequence. These results suggest that at MDNP, Gabon, only a single population of O. stephanostomum with a degree of genetic diversity is prevalent in western lowland gorillas, without zoonotic complication in local inhabitants. The possible genetic variations in the ITS region of rDNA and cox-1gene of mtDNA presented here may be valuable when only a limited amount of material is available for the molecular species diagnosis of O. stephanostomum.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Prevalence and genetic diversity of Oesophagostomum stephanostomum in wild lowland gorillas at Moukalaba-Doudou National Park, Gabon

et al. 2014

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“…If red colobus do consume barks for their medicinal benefits, investigations of the two species that lacked clear chemical activity (Celtis durandii and Olea welwitschii) may uncover new active compounds. In addition to the potential chemical effect of bark, its highly fibrous nature may increase gut motility, which could assist in purging intestinal nematodes [43].…”

Section: Discussionmentioning

confidence: 99%

Sickness behaviour associated with non-lethal infections in wild primates

et al. 2015

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Non-lethal parasite infections are common in wildlife, but there is little information on their clinical consequences. Here, we pair infection data from a ubiquitous soil-transmitted helminth, the whipworm (genus Trichuris), with activity data from a habituated group of wild red colobus monkeys (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We use mixed-effect models to examine the relationship between non-lethal parasitism and red colobus behaviour. Our results indicate that red colobus increased resting and decreased more energetically costly behaviours when shedding whipworm eggs in faeces. Temporal patterns of behaviour also changed, with individuals switching behaviour less frequently when whipworm-positive. Feeding frequency did not differ, but red colobus consumption of bark and two plant species from the genus Albizia, which are used locally in traditional medicines, significantly increased when animals were shedding whipworm eggs. These results suggest self-medicative plant use, although additional work is needed to verify this conclusion. Our results indicate sickness behaviours, which are considered an adaptive response by hosts during infection. Induction of sickness behaviour in turn suggests that these primates are clinically sensitive to non-lethal parasite infections.

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“…Musa was identified using clear diagnostic features of the ear, fingers and toes. The most likely cause of Musa's death is an obstruction of the urogenital tract caused by an invasive infection of parasite nodular worms (Oesophagostomum stephanostomum) that had caused bleed ingthrough, and blockage of, the urinary tract during the last few days of his life (Huffman et al, 1996;Huffman et al, 1997). Musa's general state of health had been declining for several months before his death.…”

Section: Pulin (Female Ca 23 Years Old)mentioning

confidence: 99%