Long-Term Monitoring of Microsporidia, Cryptosporidium and Giardia Infections in Western Lowland Gorillas (Gorilla gorilla gorilla) at Different Stages of Habituation in Dzanga Sangha Protected Areas, Central African Republic

Background Infectious diseases pose one of the greatest threats to endangered species, and a risk of gastrointestinal parasite transmission from humans to wildlife has always been considered as a major concern of tourism. Increased anthropogenic impact on primate populations may result in general changes in communities of their parasites, and also in a direct exchange of parasites between humans and primates. Aims To evaluate the impact of close contact with humans on the occurrence of potentially zoonotic protists in great apes, we conducted a long-term monitoring of microsporidia, Cryptosporidium and Giardia infections in western lowland gorillas at different stages of the habituation process, humans, and other wildlife in Dzanga-Sangha Protected Areas in the Central African Republic. Results We detected Encephalitozoon cuniculi genotypes I and II (7.5%), Enterocytozoon bieneusi genotype D and three novel genotypes (gorilla 1–3) (4.0%), Giardia intestinalis subgroup A II (2.0%) and Cryptosporidium bovis (0.5%) in gorillas, whereas in humans we found only G. intestinalis subgroup A II (2.1%). In other wild and domestic animals we recorded E. cuniculi genotypes I and II (2.1%), G. intestinalis assemblage E (0.5%) and C. muris TS03 (0.5%). Conclusion Due to the non-specificity of E. cuniculi genotypes we conclude that detection of the exact source of E. cuniculi infection is problematic. As Giardia intestinalis was recorded primarily in gorilla groups with closer human contact, we suggest that human-gorilla transmission has occurred. We call attention to a potentially negative impact of habituation on selected pathogens which might occur as a result of the more frequent presence of humans in the vicinity of both gorillas under habituation and habituated gorillas, rather than as a consequence of the close contact with humans, which might be a more traditional assumption. We encourage to observe the sections concerning hygiene from the IUCN best practice guidelines for all sites where increased human-gorilla contact occurs

Neighbour-joining tree based on nucleotide sequences of the whole ITS region of Enterocytozoon bieneusi isolates, including our new sequences (underlined).

<p>Genotypes previously found in apes and humans are shaded. The host is listed for each sample. Values on branches are percent bootstrapping using 1 000 replicates. The bootstrap proportions greater than 50% are shown on each branch. Nucleotide sequences generated from this study are underlined and are deposited in the GenBank under Accession Nos. JQ837793-JQ837800.</p

Enterocytozoon bieneusi, Encephalitozoon cuniculi, Cryptosporidium spp. and Giardia intestinalis infection in humans, wild and domestic animals.

<p><b>n</b>  =  number of samples; <b>EC I</b>  =  <i>E. cuniculi</i> genotype I; <b>EC II</b>  =  <i>E. cuniculi</i> genotype II; <b>E</b>  =  <i>Giardia intestinalis</i> assemblage E; <b>A</b>  =  <i>Giardia intestinalis</i> assemblage A.</p

<i>Enterocytozoon bieneusi</i>, <i>Encephalitozoon cuniculi</i>, <i>Cryptosporidium</i> spp. and <i>Giardia intestinalis</i> infection in wild western lowland gorillas (<i>Gorilla gorilla gorilla</i>) under different levels of human contact.

<p><b>D</b> =  <i>E. bieneusi</i> genotype D; <b>gorilla 1</b>  =  <i>E. bieneusi</i> genotype gorilla 1; <b>gorilla 2</b>  =  <i>E. bieneusi</i> genotype gorilla 2; <b>gorilla 3</b>  =  <i>E. bieneusi</i> genotype gorilla 3; <b>EC I</b>  =  <i>E. cuniculi</i> genotype I; <b>EC II</b>  =  <i>E. cuniculi</i> genotype II; <b>A</b>  =  <i>Giardia intestinalis</i> assemblage A; <b>n¹</b> number of samples; <b>n²</b> number of animals sampled.</p