The Occurrence and Ape‐to‐Ape Transmission of the Entodiniomorphid Ciliate Troglodytella abrassarti in Captive Gorillas

Abstract

ABSTRACT. Entodiniomorphid ciliates are often present in the colons of wild apes. In captive apes the infection tends to gradually disappear, with the exception of Troglodytella abrassarti. We used fecal examinations to screen the gorillas (Gorilla gorilla gorilla) in European (Czech Republic, UK) and Australian Zoos to explore the ape-to-ape transmission pattern of T. abrassarti. Gorillas from two out of three European Zoos were positive for T. abrassarti, while gorillas from the Australian Zoo were negative. We documented a horizontal transmission of T. abrassarti to a non-infected adult gorilla introduced into a Troglodytella-positive group in the Prague Zoo and traced the origin of the ciliate infection to the Paignton Zoo (UK) using serial fecal examinations. During this study, two infant gorillas born in the Prague Zoo (CZ) first became positive for T. abrassarti at the age of 9 mo. Ciliate morphology and the sequencing of the small subunit rRNA gene and the internal transcribed spacer rDNA spacer region revealed that T. abrassarti affects both captive gorillas and chimpanzees. We conclude that zoo transport plays a major role in the distribution of T. abrassarti among captive gorillas.Key Words. Chimpanzee, Gorilla gorilla, molecular phylogeny, Pan troglodytes, zoo. DESPITE the fact that Troglodytella abrassarti was described almost one hundred years ago (Brumpt and Joyeux 1912), the entodiniomorphid ciliates still represent a neglected group of symbiotic organisms in the colonic ecosystem of gorillas and chimpanzees. The role of entodiniomorphid ciliates in ape digestion is not known. Nevertheless, entodiniomorphid ciliates are thought to participate in colonic fermentation of fiber similar to that in the horse colon or the rumen of cattle (Collet et al. 1984;Reichenow 1920). However, diarrhea and deaths in captive apes have also been attributed to entodiniomorphid ciliates (Ruch 1959).Field studies usually report only the prevalence of ciliates without attempts at species determination. Moreover, the evaluation of field material is complicated by the rapid degradation of trophozoites in the feces, potentially leading to an underestimation of their diversity (Bonhomme, Grain, and Collet 1989;Goussard et al. 1983;Imai et al. 1991;Profousová et al. 2007). As a result, we still have limited data about the diversity, host specificity, and transmission of entodiniomorphids in gorillas and chimpanzees.Most records of T. abrassarti are from the common chimpanzees, Pan troglodytes (Ashford, Reid, and Wrangham 2000;File, Mcgrew, and Tutin 1976;Krief et al. 2005). Only a single report of T. abrassarti exists in wild gorillas (Gorilla gorilla gorilla) from Gabon (Goussard et al. 1983). It is widely believed that entodiniomorphid ciliates tend to gradually disappear in captive apes due to unsuitable diet and probably also because of anti-parasitic treatment and antibiotic treatments (McClure and Guilloud 1971;Ruch 1959). Transmission between host adults and/or between adults and infants has not been studied. However...

Pathogenic Eukaryotes in Gut Microbiota of Western Lowland Gorillas as Revealed by Molecular Survey

“…The most prevalent protozoal species that were found in this study were ciliates; approximately 6 species were detected in the fecal sample, which is in agreement with results from previous studies that identified entodiniomorph ciliates in the majority of fecal samples that had been collected from wild western lowland gorillas at Bai Hokou, Dzanga-Ndoki National Park (Central African Republic) and the Lopé Reserve (Gabon)111213. However, our results conflict with those from the study by Modry et al 38, in which T. abrassarti was the sole entodiniomorph ciliate that was detected in captive western lowland gorillas at the Prague Zoo in the Czech Republic. T. abrassarti has also been morphologically observed in fecal specimens from wild lowland gorillas39, where it appears to play an important role in digestion because of its ability to ferment polysaccharides in the hindguts of primates40.…”

Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park, Tanzania

“…Ashford et al, 2000;Dupain et al, 2009;Huffman et al, 1997Huffman et al, , 2009Krief et al, 2005;Landsoud-Soukate et al, 1995;McGrew et al, 1989;Modrý et al, 2009;Nejsum et al, 2006]. To date, however, few studies describing the parasites of chimpanzees introduced into non-native habitat have been reported [Hasegawa et al, 2005;Petrzelkova et al, 2006].…”

Novel Insights into the Genetic Diversity of Balantidium and Balantidium-like Cyst-forming Ciliates

“…The ciliates Isotricha protostoma and Troglodytella abrassarti , distantly related to N. coli , exhibit rather low ITS polymorphism and high host specificity [50], [51]. Transmission of these ciliates is limited, due to the fragile nature of their trophozoites, to close contact between hosts [52], [53]. Higher genetic polymorphism of ITS genes of N. coli can result from transmissions facilitated by the resilient cysts of Neobalantidium .…”