Prevalence of Cryptosporidium spp., Enterocytozoon bieneusi,Encephalitozoon spp. and Giardia intestinalis in Wild,Semi-Wild and Captive Orangutans (Pongo abelii and Pongo pygmaeus) on Sumatra and Borneo,Indonesia

Background

Orangutans are critically endangered primarily due to loss and fragmentation of their natural habitat. This could bring them into closer contact with humans and increase the risk of zoonotic pathogen transmission.

Aims

To describe the prevalence and diversity of Cryptosporidium spp., microsporidia and Giardia intestinalis in orangutans at seven sites on Sumatra and Kalimantan, and to evaluate the impact of orangutans’ habituation and location on the occurrence of these zoonotic protists.

Result

The overall prevalence of parasites in 298 examined animals was 11.1%. The most prevalent microsporidia was Encephalitozoon cuniculi genotype II, found in 21 animals (7.0%). Enterocytozoon bieneusi genotype D (n = 5) and novel genotype Pongo 2 were detected only in six individuals (2.0%). To the best of our knowledge, this is the first report of these parasites in orangutans. Eight animals were positive for Cryptosporidium spp. (2.7%), including C. parvum (n = 2) and C. muris (n = 6). Giardia intestinalis assemblage B, subtype MB6, was identified in a single individual. While no significant differences between the different human contact level groups (p = 0.479–0.670) or between the different islands (p = 0.992) were reported in case of E. bieneusi or E. cuniculi, Cryptosporidium spp. was significantly less frequently detected in wild individuals (p < 2×10⁻¹⁶) and was significantly more prevalent in orangutans on Kalimantan than on Sumatra (p < 2×10⁻¹⁶).

Conclusion

Our results revealed that wild orangutans are significantly less frequently infected by Cryptosporidium spp. than captive and semi-wild animals. In addition, this parasite was more frequently detected at localities on Kalimantan. In contrast, we did not detect any significant difference in the prevalence of microsporidia between the studied groups of animals. The sources and transmission modes of infections were not determined, as this would require repeated sampling of individuals, examination of water sources, and sampling of humans and animals sharing the habitat with orangutans.     

Why Don't We Ask? A Complementary Method for Assessing the Status of Great Apes

Species conservation is difficult. Threats to species are typically high and immediate. Effective solutions for counteracting these threats, however, require synthesis of high quality evidence, appropriately targeted activities, typically costly implementation, and rapid re-evaluation and adaptation. Conservation management can be ineffective if there is insufficient understanding of the complex ecological, political, socio-cultural, and economic factors that underlie conservation threats. When information about these factors is incomplete, conservation managers may be unaware of the most urgent threats or unable to envision all consequences of potential management strategies. Conservation research aims to address the gap between what is known and what knowledge is needed for effective conservation. Such research, however, generally addresses a subset of the factors that underlie conservation threats, producing a limited, simplistic, and often biased view of complex, real world situations. A combination of approaches is required to provide the complete picture necessary to engage in effective conservation. Orangutan conservation (Pongo spp.) offers an example: standard conservation assessments employ survey methods that focus on ecological variables, but do not usually address the socio-cultural factors that underlie threats. Here, we evaluate a complementary survey method based on interviews of nearly 7,000 people in 687 villages in Kalimantan, Indonesia. We address areas of potential methodological weakness in such surveys, including sampling and questionnaire design, respondent biases, statistical analyses, and sensitivity of resultant inferences. We show that interview-based surveys can provide cost-effective and statistically robust methods to better understand poorly known populations of species that are relatively easily identified by local people. Such surveys provide reasonably reliable estimates of relative presence and relative encounter rates of such species, as well as quantifying the main factors that threaten them. We recommend more extensive use of carefully designed and implemented interview surveys, in conjunction with more traditional field methods.     

Abundance and Distribution of Sympatric Gibbons in a Threatened Sumatran Rain Forest

Agile gibbons (Hylobates agilis) and siamangs (Symphalangus syndactylus) are sympatric small apes inhabiting threatened forests of Sumatra, Indonesia. We censused both species in the 3,568-km² Bukit Barisan Selatan National Park, at the southern limit of their ranges, over a 7-mo period in 2001. First, we monitored daily calling rates from known populations to develop probabilities of calling during a specified number of days and used the probability of calling at 1 time during 3 days to convert calling rates to abundance. Next, we used 3-day calibrated call count censuses (n=31) stratified by distance from forest edge and across a range of elevations to estimate species-specific group densities. We used group size from the known populations as well as data collected ad libitum during the census to convert group density to individual density. Agile gibbon group density averaged 0.67 km^–2 (SE = 0.082) and group size averaged 2.6 (SE = 0.73) for a population estimate of 4,479 (SE = 1,331) individuals. Siamang group density averaged 2.23 km^–2 (SE = 0.245), and group size averaged 3.9 (SE = 1.09) for a population estimate of 22,390 (SE = 8,138). Agile gibbon and siamang densities are negatively correlated, with agile gibbons more abundant in mid-elevation forests and siamangs most abundant in lowland and submontane forests. The small group sizes of agile gibbons indicate potential survival problems in infant and juvenile size classes. Although neither species is presently threatened by direct human disturbance, continued deforestation will jeopardize the long-term viability of both species in Bukit Barsian Selatan National Park and on Sumatra.     

Synthesis and Structure−Activity Relationship of Omaezallene Derivatives

Omaezallene derivatives (nor‐bromoallene, nor‐bromodiene, and bromoenynes) were successfully synthesized. Their antifouling activity and toxicity to the cypris larvae of the barnacle Amphibalanus amphitrite and ecotoxicity to the marine crustacean Tigriopus japonicus were studied. It was revealed that the two side chains of omaezallene were essential to its antifouling activity because the activities of nor‐bromoallene and nor‐bromodiene were significantly diminished. The bromoenyne was found to exhibit potent antifouling activities comparable to omaezallene with low toxicity and ecotoxicity. Preparation of bromoenyne framework is much easier than that of bromodiene moiety in omaezallene. Based on the antifouling activities of the bromoenynes, the synthesis of fluorescent probes and evaluation of their biological activities were also carried out.     

Syntheses and Biological Activities of Danicalipin A Derivatives

Synthesis of three derivatives of danicalipin A, tetrachloride, trisulfate and a fluorescent probe was achieved through Wittig reaction strategy. Toxicity of the derivatives against brine shrimp (Artemia salina) as also investigated to provide useful information for the biological activity; i) less chloride derivative showed similar toxicity to danicalipin A, ii) the amphiphilic property, a characteristic feature of danicalipin A, was crucial because trisulfate considerably decreased the toxicity and iii) fluorescent derivative kept brine shrimp toxicity of danicalipin A.     

Quantifying killing of orangutans and human-orangutan conflict in Kalimantan, Indonesia

Human-orangutan conflict and hunting are thought to pose a serious threat to orangutan existence in Kalimantan, the Indonesian part of Borneo. No data existed prior to the present study to substantiate these threats. We investigated the rates, spatial distribution and causes of conflict and hunting through an interview-based survey in the orangutan's range in Kalimantan, Indonesia. Between April 2008 and September 2009, we interviewed 6983 respondents in 687 villages to obtain socio-economic information, assess knowledge of local wildlife in general and orangutan encounters specifically, and to query respondents about their knowledge on orangutan conflicts and killing, and relevant laws. This survey revealed estimated killing rates of between 750 and 1800 animals killed in the last year, and between 1950 and 3100 animals killed per year on average within the lifetime of the survey respondents. These killing rates are higher than previously thought and are high enough to pose a serious threat to the continued existence of orangutans in Kalimantan. Importantly, the study contributes to our understanding of the spatial variation in threats, and the underlying causes of those threats, which can be used to facilitate the development of targeted conservation management.     

Entamoeba histolytica infections in wild and semi-wild orangutans in Sumatra and Kalimantan

Key to the success of orangutan conservation management practices is the prevention of the introduction of infectious diseases to the remaining populations. Previous reports of Entamoeba spp. positive orangutans are of concern as Entamoeba spp. infection has been linked to morbidity and mortality in primates. It remains to be determined if the Entamoeba species infecting orangutans is the pathogenic Entamoeba histolytica. Orangutan fecal samples have been collected from orangutans from sites in Sumatra (Bukit Lawang, Ketambe, and Suaq, 241 samples from 64 individuals), and two sites in Kalimantan (Sebangau and Tuanan, 129 samples from 39 individuals). All samples were from wild orangutans except for a proportion from Sumatra which were from semi-wild (108 samples, 10 individuals). E. histolytica-specific nested PCR assays were carried out on the fecal samples. A total of 36 samples from 17 individuals tested positive for E. histolytica. When compared with published sequences using NCBI BLAST the E. histolytica positive samples showed a 98–99% concordance. The majority (76%, n = 36) of the positive isolates came from semi-wild orangutans in Bukit Lawang. This study supports the growing body of evidence that contact with humans is an important risk factor for infection of wild primates with E. histolytica.