Ecotourism activities should attempt to educate visitors while minimizing modification or degradation of natural resources and broadly benefit the social and natural environments by involving the participation of local communities. Ecotourism can facilitate species conservation by raising needed funds for habitat conservation and increasing public awareness of conservation issues. However, rapid, unmonitored development of ecotourism projects in protected areas can produce deleterious effects on the very species we wish to conserve. Such risks may include habitat degradation due to pollution and inappropriate development of infrastructure, animal crowding into restricted areas, and introduction of invasive species, among others. Habituation of animals to human presence can increase the likelihood that animals will raid crops and invade garbage pits. Habituation may make wildlife more vulnerable to poaching because of loss of fear of humans. It may also lead to alterations in animal stress responses, possibly leading to immunosuppression with decreased reproductive success and increased susceptibility to infectious diseases.


Zoonotic (nonhuman animal to human) and anthropozoonotic (human to nonhuman animal) pathogen transmission are of vital consideration given the increasing demand from tourists to experience direct encounters with wildlife. This is particularly the case for primates, for which ecotourism activities have been flourishing over the past few decades. Nonhuman primates are genetically closely related to humans and are therefore particularly susceptible to many human pathogens. Their remaining wild populations are relatively small, their reproductive cycles protracted (with low reproductive rates) and their immune systems usually naïve to human pathogens. Disease, combined with continued problems of hunting and bushmeat consumption, habitat loss and fragmentation, and the illegal pet trade, can produce catastrophic population declines of wild primates.


The relative contribution of tourists to the spread of pathogens to wildlife is unknown, but the number of tourists visiting wildlife sanctuaries worldwide is increasing substantially. A major shortcoming of international travelers in general is their poor knowledge, attitudes and practices about travel health. Many travelers do not utilize pre-travel preventive health strategies, including physician advice and chemoprophylaxes. Traveler compliance to physician advice is surprisingly low, even in regards to avoiding certain dangerous food items such as salads, shellfish and tap water. Many travelers do not understand basic risks of infection, including their sources/causes.


A significant proportion of travelers to tropical regions (where most primate-based tourism takes place) are not protected against vaccine-preventable illnesses. A majority of these travelers demonstrate poor recall of actual vaccination status, as verified by reference to vaccination certificates or serological testing. Tourists are also stressed due to sleep dysregulation, unfamiliar diets and climate, and exposure to novel pathogens. Consequently, illness during travel is very common, particularly gastrointestinal and respiratory infections.


Like most other travelers, the majority of tourists that visit wildlife sanctuaries (which may include both wild and rehabilitated/released animals; not zoos) arguably underestimate their own risk of infection, as well as their potential contribution to the spread of diseases themselves. That is, despite their recognized travel itinerary to view endangered animals, ecotourists concerned about environmental protection may be largely unaware of the impact they may directly have on animal health. Risk of pathogen transmission at different primate-based tourism destinations arguably varies by a number of factors, including frequency and degree of contact, species involved, and tourist behaviors and infection status, among other things. Much as contact between humans and nonhuman primates varies by location, risk of pathogen transmission must also vary among locations.


We have recently completed an additional survey of tourists at the

Takasakiyama Monkey Park in Kyushu, Japan, home to over 1000 wild Japanese macaques (Macaca fuscata). Almost 93% of the 686 survey participants were Japanese. Only 1.5% were carrying their immunization record, many did not know what they were currently vaccinated for, and less than 30% reported ever being vaccinated for measles. 16.5% reported at least one symptom of current infection, with 12.8% reporting at least one current symptom of respiratory tract infection. Surprisingly, only 53.2% believed that humans can give diseases to wild primates. Lack of knowledge about zoonoses and anthropozoonoses may contribute to why 61.2% of participants still expressed desire to feed monkeys at the park, and 22.8% would own one as a pet. The primary reasons for desired or realized animal contact reported by both the park staff and the tourists, are that these animals are ‘cute,’ the thrill of adventure, because their behaviors are often similar to humans, and because they saw others (including professional primatologists) touching primates in various media sources. We hope to expand this work to include one more field season at Takasakiyama in addition to surveys and sample collections at the following locations within the next two years:


Jigokudani Monkey Park near Nagano, Japan.

Ubud Monkey Park, Bali, Indonesia.

Uluwatu Temple, Bali, Indonesia.

Cape of Good Hope Nature Reserve, South Africa.

Upper Rock Nature Reserve, Gibraltar.

Cruise port at Basseterre, St. Kitts.

Punta Laguna, Playa Del Carmen, Mexico.

Community Baboon Sanctuary, Belmopan City, Belize.

Manuel Antonio Park, Costa Rica.

Monkey Island, Gamboa, Panama.


The Sepilok Orangutan Rehabilitation Centre (SORC) is located on the northern edge of the Kabili-Sepilok Virgin Jungle Forest Reserve, outside of the city of Sandakan in the Malaysian state of Sabah in northern Borneo. Operated by the Sabah Wildlife Department, SORC was established in 1964 as a center for the rehabilitation of orphaned, injured, and/or confiscated orangutans and other endangered species. Following a six-month quarantine period, orangutans are taught how to transverse the forest and forage for food. Following extensive health inspections, these animals are eventually relocated or released into the surrounding forest. To facilitate public education and generate operational funds, the public is allowed to view two daily feedings of the free-ranging orangutans (approximately 40 Pongo pygmaeus morio) and long-tailed and pig-tailed macaques (approximately 160 total). A multilingual information sign indicates that smoking, eating and spitting are not allowed, that visitors should keep their distance from the animals, should not bring medications, bags or insect repellant, and other miscellaneous information. Park rangers are present during animal feedings, and the visitor viewing area is separated from the actual feeding platforms by approximately 10 meters. Although the visitations are relatively short (approximately 30 minutes), the number of tourists at any given feeding is not restricted. Approximately 100,000 visitors attend these feedings annually. The orangutans and macaques that surround Sepilok certainly exhibit less arboreality and greater proximity to humans compared to their wild counterparts, and direct contact between tourist and ape/monkey populations does happen occasionally.


To understand better the risks of anthropozoonotic pathogen transmission among tourists, orangutans and macaques, a team led by Michael Muehlenbein in collaboration with Dr. Laurentius Ambu, Dr. Sen Nathan and Sylvia Alsisto of the Sabah Wildlife Department (http://www.wildlife.sabah.gov.my/), and Dr. Marc Ancrenaz of Hutan (http://www.hutan.org.my/) began surveying tourists at SORC in 2007. Of the 633 tourists who completed the survey in 2007, a little more than half reported being currently vaccinated against tuberculosis, hepatitis A, hepatitis B, polio, and measles. Despite the fact that the majority of visitors to SORC are from temperate regions where influenza is relatively more prevalent, 67.1% of those surveyed with medical-related occupations (and so some formal training in infection risks) reported not being currently vaccinated for influenza (Muehlenbein et al. 2008).  These results are consistent with the low vaccination rates found among other international travelers. Such results lend support for the recommendation of required, standardized vaccination certificates at wildlife tourism locations, particularly those involving nonhuman primates. However, routine, required, and recommended vaccines vary between countries and by age and health status of the recipient. And because vaccination certifications are not usually standardized between countries, it is difficult to accurately ascertain current immune status for most travelers. Despite these facts, travelers could be urged to examine their actual vaccination status prior to leaving for holiday.


In 2007, 15% of tourists surveyed at SORC self-reported at least one of the following current symptoms: cough, sore throat, congestion, fever, diarrhea and vomiting (Muehlenbein et al. 2010). Those participants with recent animal contact (e.g., livestock, wildlife at other sanctuaries, unfamiliar domestic pets) were more likely to report current respiratory symptoms compared to individuals with no such animal contact. Such results highlight the fact that currently ill and potentially infectious tourists still visit wildlife sanctuaries, creating potential risk of pathogen transmission to the non-human primates they come to visit, in addition to the local inhabitants and animal caregivers. Some tourists may ignore such risks, whereas most (we suspect) are unaware or uninformed about such risks prior to travel. They not only underestimate their potential contribution to the spread of disease, but also underestimate their own risk of acquiring infection.


An additional 650 tourist surveys were obtained in 2009 at SORC. Of the respondents, 48% had visited other countries to specifically view monkeys or apes. Only 11% of these were made aware of health regulations at these destinations, and only 5.7% thought that such health regulations were enforced (unpublished data). Despite the fact that 96% of respondents believed humans can give diseases to wild animals, 35% of these respondents would still try to touch a wild monkey or ape if they had the opportunity. Clearly this problem deserves more attention.


In 2009, throat swab, saliva and gargle samples were also obtained from 600 adult visitors at Sepilok. Nucleic acids were successfully extracted from 529 preserved samples and were processed using a multiplex system for simultaneous differential diagnosis of influenza (A, B, H1N1 Mexico 2009), parainfluenza (1-4), respiratory syncytial virus (A, B), metapneumovirus (A, B), coxsackievirus, rhinovirus, adenovirus (B, E), bocavirus and coronavirus (NL63, HKUI, 229E, OC43). Viral prevalence was 6.24% (33 people infected with 9 unique viruses). Tourists who reported symptoms within the previous 24 hours were more than three times more likely to test positive for a respiratory virus. Although our results do not account for early or late infections, or bacterial respiratory infection, we do have the largest survey of ecotourist behavior and viral prevalence to date. Despite their interests in environmental protection and known travel to view endangered animals, tourists very likely create unnecessary risk of infection transmission to wildlife. Requiring tourists to present updated vaccination certificates, and providing masks to those who report symptoms may be future considerations for preventing infections.


Primate Tourism Alliance

Macaques in Bali

Getting too close at Trentham, UK

Feeding at Arashiyama, Japan

Case study: Tourists at the Sepilok Orangutan Rehabilitation Centre

Macaque at Jigokudani, Japan

Getting too close at Jigokudani, Japan

Getting too close at Sanghe, Bali

Getting too close at Uluwatu, Bali

All images copyright Michael Muehlenbein

Background

Future Work