Wildlife tourism and conservation: an interdisciplinary evaluation of gorilla ecotourism in Dzanga-Sangha, Central African Republic

Wildlife tourism is proliferating worldwide and has the potential to raise revenue for conservation as well as public awareness of conservation issues. However, concerns are growing about the potentially negative influence of such tourism on the wildlife involved. An absence of scientific information means that the potential costs of tourism are unidentified, tourism management strategies are not informed by scientific studies, and the ethics of habituating animals to humans remain relatively unexplored, though much discussed. This combination of ecological and anthropological research questions necessitates a bio-social approach. In this thesis I adopt an interdisciplinary approach to explore the factors that influence human-animal interactions and incorporate them into conservation biology. I use the Dzangha-Sangha Gorilla Habituation and Ecotourism Project in the Central African Republic as a case study. First, I explore the context of wildlife tourism and why people watch gorillas in the wild, their reactions to and behaviours during their gorilla encounters and the effect these encounters have on the visitors. People are drawn to gorillas because gorillas are human-like and tourists seek close encounters which are rare and authentic. Photography is a key motivation for tourists to visit gorillas but also a major cause of disturbance. Next, I detail a series of experiments I conducted to validate methods for measuring physiological stress in the western lowland gorilla. Using these methods, I then address the question of whether gorillas incur stress as a result of habituation and ecotourism activities, comparing faecal glucocorticoid metabolite levels (FGCMs) in four gorilla groups at different stages of habituation. Two (and possibly all three) of the human-contacted groups had significantly higher levels of FGCMs than unhabituated gorillas, and the group undergoing habituation had the highest FGCMs, suggesting that the process of habituation is perceived as a threat by gorillas, and that habituation reduces this response over time. FGCMs in habituated groups were significantly associated with increasing frequency of violation of the 7 m distance rule by observers and with a medical intervention but not with other measures of human pressure, suggesting that some elements of human-gorilla contact still elicit a GC response in habituated gorillas. I then demonstrate a positive association between FGCMs and parasite infection that may reflect hormonal suppression of the immune system in gorillas with higher FGCM levels, or, stimulation of the HPA axis as a result of increased parasite infection. Finally, I explore socio-cultural, epidemiological and management aspects of human interactions with gorillas in order to identify how and why visitors break regulations and the subsequent risk of human-gorilla disease transmission. Socio-cultural and emotive factors motivate people to get close to gorillas. Epidemiological factors interact with socio-cultural and emotive drivers to create a variable profile of disease risk presented by each person during their interactions with gorillas. The outcomes of this interdisciplinary risk assessment will inform policy makers as to how they may better protect gorillas, and other animals, from the potential negative effects of human disturbance resulting from habituation, tourism and research activities. The implications of this study will help to maximize the potential for such projects to be beneficial, low-impact and sustainable conservation solutions

Grooming in Barbary macaques: better to give than to receive?

It is well established that grooming underpins sociality in group-living primates, and a number of studies have documented the stress-reducing effects of being groomed. In this study, we quantified grooming behaviour and physiological stress (assessed by faecal glucocorticoid analysis) in free-ranging Barbary macaques, Macaca sylvanus. Our results indicate that it is the giving rather than the receiving of grooming that is associated with lower stress levels. These findings shed important new light on the benefits of this key behaviour in primate social life

Humans and Great Apes Cohabiting the Forest Ecosystem in Central African Republic Harbour the Same Hookworms

Background Hookworms are important pathogens of humans. To date, Necator americanus is the sole, known species of the genus Necator infecting humans. In contrast, several Necator species have been described in African great apes and other primates. It has not yet been determined whether primate-originating Necator species are also parasitic in humans. Methodology/Principal Findings The infective larvae of Necator spp. were developed using modified Harada-Mori filter-paper cultures from faeces of humans and great apes inhabiting Dzanga-Sangha Protected Areas, Central African Republic. The first and second internal transcribed spacers (ITS-1 and ITS-2) of nuclear ribosomal DNA and partial cytochrome c oxidase subunit 1 (cox1) gene of mtDNA obtained from the hookworm larvae were sequenced and compared. Three sequence types (I–III) were recognized in the ITS region, and 34 cox1 haplotypes represented three phylogenetic groups (A–C). The combinations determined were I-A, II-B, II-C, III-B and III-C. Combination I-A, corresponding to N. americanus, was demonstrated in humans and western lowland gorillas; II-B and II-C were observed in humans, western lowland gorillas and chimpanzees; III-B and III-C were found only in humans. Pairwise nucleotide difference in the cox1 haplotypes between the groups was more than 8%, while the difference within each group was less than 2.1%. Conclusions/Significance The distinctness of ITS sequence variants and high number of pairwise nucleotide differences among cox1 variants indicate the possible presence of several species of Necator in both humans and great apes. We conclude that Necator hookworms are shared by humans and great apes co-habiting the same tropical forest ecosystems

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

Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas?

Increased anthropogenic activity can result in parasite exchanges and/or general changes in parasite communities, imposing a health risk to great apes. We studied protist and helminth parasites of wild western lowland gorilla groups in different levels of habituation, alongside humans inhabiting Dzanga-Sangha Protected Areas in the Central African Republic. Faeces were collected yearly during November and December from 2007 to 2010 and monthly from November 2010 to October 2011. Protist and helminth infections were compared among gorilla groups habituated, under habituation and unhabituated, and the effect of host traits and seasonality was evaluated. Zoonotic potential of parasites found in humans was assessed. No significant differences in clinically important parasites among the groups in different stages of habituation were found, except for Entamoeba spp. However, humans were infected with four taxa which may overlap with taxa found in gorillas. Females were less infected with spirurids, and adults had higher intensities of infection of Mammomonogamus sp. We found seasonal differences in the prevalence of several parasite taxa, but most importantly, the intensity of infection of unidentified strongylids was higher in the dry season. This study highlights that habituation may not necessarily pose a greater risk of protist and helminth infections in gorilla groups

Comparison of ITS-1 sequences of hookworms from apes and humans from Dzanga Sangha Protected Areas.

<p>Host and accession number in DNA database are given in parentheses. Dots indicate homologous nucleotides with <i>N. americanus</i> (<i>N. a.</i>) from Guatemala (AF217891); dash indicates absence of nucleotide. Major indels are shaded.</p

Comparison of ITS-2 sequences of hookworms from apes and humans from Dzanga Sangha Protected Areas.

<p>Host and accession number in DNA database are given in parentheses. Dots indicate homologous nucleotides with <i>N. americanus</i> (<i>N. a.</i>) from Guatemala (AF217891); dash indicates absence of nucleotide. Major indels are shaded.</p

Restriction enzyme digestion of DNA sequences amplified with Civ18S1500F and Nem5.8R.

<p>By digestion with <i>Alu</i> I, two bands were formed for type I in area from 200 to 500 bp, while only one band was formed for types II and III. By digestion using <i>Hinc</i> II, two bands of about 300 and 500 bp were formed for type I, while only one band similar to original band was visible for types II and III.</p

Amplification of partial ITS-1 region using specific primers.

<p>Primers AmerF3 and AmerR2 only amplified specific band of about 250-1, while no clear band was formed for types II and III. CongF and Nem5.8R resulted in formation of specific band of about 650 bp for types II and III, while prominent bands were not formed for type I.</p