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16 - Considering risks of pathogen transmission associated with primate-based tourism

from Part V - Broader issues

Published online by Cambridge University Press:  05 September 2014

Michael P. Muehlenbein
Affiliation:
Indiana University
Janette Wallis
Affiliation:
University of Oklahoma
Anne E. Russon
Affiliation:
Glendon College, York University
Janette Wallis
Affiliation:
University of Oklahoma
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Summary

Introduction

Sustainable, nature-based tourism should attempt to educate visitors about wildlife and the environment, while minimizing modification or degradation of the natural resources in the sites they visit. When possible, these activities should broadly benefit the social and natural environments by involving the participation of local communities (Ceballos-Lascuráin, 1996). And, if managed well, nature-based tourism should facilitate species conservation by raising the needed funds for wildlife and habitat conservation, while increasing public awareness of conservation issues. Unfortunately, rapid and unmonitored development of tourism projects in protected areas can produce deleterious effects on the very species we wish to conserve. Such risks may include habitat degradation caused by pollution and environmentally damaging development of infrastructure; animal crowding into restricted areas; and the introduction of invasive species.

These issues take on special importance when the species in question are (nonhuman) primates. Most wild populations of primates are relatively small and their reproductive cycles are protracted (with low reproductive rates relative to most mammals of similar size), so they are particularly vulnerable to population decreases, including those that result from human activities. Humans have contributed to significant population declines of wild primates through hunting and bushmeat consumption, habitat loss and fragmentation, and illegal capture of live primates for entertainment or other purposes. Tourism activities involving primates in their native habitat (including free-living rehabilitants as well as their wild counterparts) could benefit primate conservation but we must remain diligent about monitoring potential negative consequences, especially since primate tourism has been increasing in popularity over the past few decades. For example, the habituation to human presence essential to primate tourism may increase the likelihood that these animals will raid crops, invade garbage pits, and break into vehicles or lodgings for food. They may also become more vulnerable to poaching as a result of their loss of fear, their natural diet and ranging may become permanently altered, and their normal social behaviors may become altered (e.g. the appearance of a group of tourists may interrupt mating behaviors). Many of the chapters in this volume document these tourism impacts on the primates visited. Habituation could even lead to alterations in animal stress responses, possibly leading to immunosuppression with decreased reproductive success and increased susceptibility to infectious diseases (Muehlenbein, 2009; Muehlenbein et al., 2012).

Type
Chapter
Information
Primate Tourism
A Tool for Conservation?
, pp. 278 - 291
Publisher: Cambridge University Press
Print publication year: 2014

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References

Almeida, M. A. B., Santos, E. D., Cardoso, J. D. C. et al. (2012). Yellow fever outbreak affecting Alouatta populations in southern Brazil (Rio Grande do Sul State), 2008–2009. American Journal of Primatology, 74: 68–76.CrossRefGoogle Scholar
Ambu, L. (2007). Strategy of the Sabah Wildlife Department for wildlife conservation in Sabah. First International Conservation Conference in Sabah: The Quest for Gold Standards. Kota Kinabalu, Malaysia: Sabah Wildlife Department.Google Scholar
Ashford, R. W., Reid, G. D. F., and Butynski, T. M. (1990). The intestinal faunas of man and mountain gorillas in a shared habitat. Annals of Tropical Medicine and Parasitology, 84: 337–340.CrossRefGoogle Scholar
Brack, M. (1987). Agents Transmissible from Simians to Man. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Burgos-Rodriquez, A. G. (2011). Zoonotic diseases of primates. Veterinary Clinics of North America: Exotic Animal Practice, 14: 557–575.Google Scholar
Byers, A. C. and Hastings, B. (1991). Mountain gorilla mortality and climatic factors in the Parc National des Volcans, Ruhengeri Prefecture, Rwanda, 1988. Mountain Research and Development, 2: 145–151.CrossRefGoogle Scholar
Ceballos-Lascuráin, H. (1996). Tourism, Ecotourism, and Protected areas: The State of Nature-based Tourism Around the World and Guidelines for its Development. Gland, Switzerland: World Conservation Union.CrossRefGoogle Scholar
Chi, F., Leider, M., Leendertz, F. et al. (2007). New Streptococcus pneumoniae clones in deceased wild chimpanzees. Journal of Bacteriology, 189: 6085–6088.CrossRefGoogle ScholarPubMed
Costa, E. A., Luppi, M. M., Malta, M. C. C. et al. (2011). Outbreak of human Herpesvirus Type 1 infection in nonhuman primates (Callithrix penincillata). Journal of Wildlife Diseases, 47: 690–693.CrossRefGoogle Scholar
Cox-Singh, J. and Singh, B. (2008). Knowlesi malaria: Newly emergent and of public health importance?Trends in Parasitology, 24: 406–410.CrossRefGoogle ScholarPubMed
Crockett, M. and Keystone, J. (2005). “I hate needles” and other factors impacting on travel vaccine uptake. Journal of Travel Medicine, 12: S41–S46.CrossRefGoogle ScholarPubMed
Ferber, D. (2000). Primatology. Human diseases threaten great apes. Science, 289: 1277–1278.CrossRefGoogle ScholarPubMed
Fuentes, A. (2006). Human culture and monkey behavior: Assessing the contexts of potential pathogen transmission between macaques and humans. American Journal of Primatology, 68: 880–896.CrossRefGoogle ScholarPubMed
Gao, F., Bailes, E., Robertson, D. L. et al. (1999). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature, 397: 436–441.CrossRefGoogle ScholarPubMed
Goldberg, T. L., Gillespie, T. R., Rwego, I. B. et al. (2007). Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biological Conservation, 135: 511–517.CrossRefGoogle Scholar
Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior. Cambridge, MA: Harvard University Press.Google Scholar
Graczyk, T. K, Nizeyi, J. B., Ssebide, B. et al. (2002a). Anthropozoonotic Giardia duodenalis genotype (assemblage) A infections in habitats of free-ranging human habituated gorillas, Uganda. Journal of Parasitology, 88: 905–909.CrossRefGoogle ScholarPubMed
Graczyk, T. K., Nizeyi, J. B., da Silva, A. J. et al. (2002b). A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitology Research, 88: 926–931.CrossRefGoogle ScholarPubMed
Hamer, D. H. and Connor, B. A. (2004). Travel health knowledge, attitudes and practices among United States travellers. Journal of Travel Medicine, 11: 23–26.CrossRefGoogle Scholar
Hanamura, S., Kiyono, M., Lukasik-Braum, M. et al. (2008). Chimpanzee deaths at Mahale caused by a flu-like disease. Primates, 49: 77–80.CrossRefGoogle ScholarPubMed
Hilton, E., Singer, C., Kozarsky, P. et al. (1991). Status of immunity to tetanus, measles, mumps, rubella, and polio among US travellers. Annals of Internal Medicine, 115: 32–33.CrossRefGoogle Scholar
Homsy, J. (1999). Ape Tourism and Human Diseases: How Close Should we Get? Report for the International Gorilla Conservation Programme Regional Meeting, Rwanda.Google Scholar
Horvath, L. L., Murray, C. K., and DuPont, H. L. (2003). Travel health information at commercial travel websites. Journal of Travel Medicine, 10: 272–279.CrossRefGoogle ScholarPubMed
Hosaka, K. (1995a). Epidemics and wild chimpanzee study groups. Pan Africa News, 2: 1–2.Google Scholar
Hosaka, K. (1995b). Mahale: A single flu epidemic killed at least 11 chimps. Pan Africa News, 2: 3–4.Google Scholar
Huff, J. L. and Barry, P. A. (2003). B-virus (Cercopithecine herpesvirus 1) infection in humans and macaques: potential for zoonotic disease. Emerging Infectious Diseases, 9: 246–250.CrossRefGoogle ScholarPubMed
Huijbregts, B., De Wachter, P., Ndong, L. S., Akou, O., and Akou, M. E. (2003). Ebola and the decline of gorilla Gorilla gorilla and chimpanzee Pan troglodytes populations in Minkebe Forest, north-eastern Gabon. Oryx, 37: 437–443.CrossRefGoogle Scholar
Johnston, A. R., Gillespie, T. R., Rwego, I. B. et al. (2010). Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Neglected Tropical Diseases, 4: e683.CrossRefGoogle ScholarPubMed
Jones-Engel, L., May, C., C., Engel, G. A. et al. (2008). Diverse contexts of zoonotic transmission of simian foamy viruses in Asia. Emerging Infectious Diseases, 14: 1200–1208.CrossRefGoogle Scholar
Kalema-Zikusoka, G., Kock, R. A., and Macfie, E. J. (2002). Scabies in free-ranging mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Veterinary Research, 150: 12–15.Google ScholarPubMed
Kaur, T., Singh, J., Tong, S. et al. (2008). Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, western Tanzania. American Journal of Primatology, 70: 755–765.CrossRefGoogle ScholarPubMed
Klee, S. R., Ozel, M., Appel, B. et al. (2006). Characterization of Bacillus anthracis-like bacteria isolated from wild great apes from Côte d’Ivoire and Cameroon. Journal of Bacteriology, 188: 5333–5344.CrossRefGoogle ScholarPubMed
Köndgen, S., Kühl, H., N’Goran, P. K. et al. (2008). Pandemic human viruses cause decline of endangered great apes. Current Biology, 18: 1–5.CrossRefGoogle ScholarPubMed
Kortlandt, A. (1996). An epidemic of limb paresis (polio?) among the chimpanzee population at Beni (Zaire) in 1964, possibly transmitted by humans. Pan Africa News, 3: 9–10.CrossRefGoogle Scholar
Leendertz, F. H., Ellerbrok, H., Boesch, C. et al. (2006). Anthrax kills wild chimpanzees in a tropical rainforest. Nature, 430: 451–452.CrossRefGoogle Scholar
Leroy, E. M., Rouquet, P., Formenty, P. et al. (2004). Multiple Ebola virus transmission events and rapid decline of Central African wildlife. Science, 303: 387–390.CrossRefGoogle ScholarPubMed
Lopez-Velez, R. and Bayas, J. M. (2007). Spanish travellers to high-risk areas in the tropics: Airport survey of travel health knowledge, attitudes, and practices in vaccination and malaria prevention. Journal of Travel Medicine, 14: 297–305.CrossRefGoogle Scholar
Lukasik-Braum, M. and Spelman, L. (2008). Chimpanzee respiratory disease and visitation rules at Mahale and Gombe National Parks in Tanzania. American Journal of Primatology, 70: 734–737.CrossRefGoogle ScholarPubMed
Macfie, E. (1991). The Volcano Veterinary Centre update. Gorilla Conservation News, 5: 20.Google Scholar
Macfie, E. (1996). Case report on scabies infection in Bwindi gorillas. Gorilla Journal, 13: 19–20.Google Scholar
Macfie, E. J. and Williamson, E. A. (2010). Best Practice Guidelines for Wild Great Ape Tourism. Gland, Switzerland. IUCN/SSC Primate Specialist Group.Google Scholar
Muehlenbein, M. P. (2009). The application of endocrine measures in primate parasite ecology. Huffman, M. and Chapman, C. (eds.), Primate Parasite Ecology: The Dynamics of Host-Parasite Relationships. New York: Cambridge University Press, pp. 63–81.Google Scholar
Muehlenbein, M. P. and Ancrenaz, M. (2009). Minimizing pathogen transmission at primate ecotourism destinations: The need for input from travel medicine. Journal of Travel Medicine, 16: 229–232.CrossRefGoogle ScholarPubMed
Muehlenbein, M. P., Ancrenaz, M., Sakong, R. et al. (2012). Ape conservation physiology: Fecal glucocorticoid responses in wild Pongo pygmaeus morio following human visitation. PLoS ONE, 7 (3): e33357.CrossRefGoogle ScholarPubMed
Muehlenbein, M. P., Martinez, L. A., Lemke, A. A. et al. (2008). Perceived vaccination status in ecotourists and risks of anthropozoonoses. EcoHealth, 5: 371–378.CrossRefGoogle ScholarPubMed
Muehlenbein, M. P., Martinez, L. A., Lemke, A. A. et al. (2010). Unhealthy travellers present challenges to sustainable ecotourism. Travel Medicine and Infectious Disease, 8: 169–175.CrossRefGoogle Scholar
Mueller-Graf, C. D. M., Collins, D. A., Packer, C., and Woolhouse, M. E. J. (1997). Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology, 115: 621–627.CrossRefGoogle Scholar
Nishida, T., Corp, N., Hamai, M. et al. (2003). Demography, female life history, and reproductive profiles among the chimpanzees of Mahale. American Journal of Primatology, 59: 99–121.CrossRefGoogle ScholarPubMed
Nizeyi, J. B., Mwebe, R., Nanteza, A. et al. (2001). Campylobacteriosis, salmonellosis, and shigellosis in free-ranging human-habituated mountain gorillas of Uganda. Journal of Wildlife Diseases, 37: 239–244.CrossRefGoogle ScholarPubMed
Palacios, G., Lowenstine, L., Cranfield, M. et al. (2011). Human metapneumovirus infection in wild mountain gorillas, Rwanda. Emerging Infectious Diseases, 17: 711–713.CrossRefGoogle ScholarPubMed
Prazuck, T., Semaille, C., Defayolle, M. et al. (1998). Immunization status of French and European tropical travellers: Study of 9,156 subjects departing from Paris to 12 tropical destinations. Revue d’Epidemiologie et de Santé Publique, 46: 64–72.Google Scholar
Rack, J., Wichmann, O., Kamara, B. et al. (2005). Risk and spectrum of diseases in travellers to popular tourist destinations. Journal of Travel Medicine, 12: 248–253.CrossRefGoogle Scholar
Rolland, R. M., Hausfater, G., Marshall, B., and Levy, S. B. (1985). Antibiotic resistant bacteria in wild primates: Increased prevalence in baboons feeding on human refuse. Applied Environmental Microbiology, 49: 791–794.Google ScholarPubMed
Rwego, I. B., Isabirye-Basuta, G., Gillespie, T. R., and Goldberg, T. L. (2008). Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conservation Biology, 22: 1600–1607.CrossRefGoogle ScholarPubMed
Sakamaki, T., Mulavwa, M., and Furuichi, T. (2009). Flu-like epidemics in wild bonobos (Pan paniscus) at Wamba, the Luo Scientific Reserve, Democratic Republic of Congo. Pan Africa News, 16: 1–4.CrossRefGoogle Scholar
Salzer, J. S., Rwego, I. B., Golderg, T. L., Kuhlenschmidt, M. S., and Gillespie, T. K. (2007). Giardia sp. and Cryptosporidium sp. infections in primates in fragmented and undisturbed forest in Western Uganda. Journal of Parasitology, 93: 439–440.CrossRefGoogle ScholarPubMed
Sandbrook, C. and Semple, S. (2006). The rules and reality of mountain gorilla Gorilla beringei beringei tracking: How close do tourists get?Oryx, 40: 428–433.CrossRefGoogle Scholar
Santiago, M. L., Range, F., Keele, B. F. et al. (2005). Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atye atys) from the Tai Forest, Côte d’Ivoire: Implications for the origin of epidemic human immunodeficiency virus type 2. Journal of Virology, 79: 12515–12527.CrossRefGoogle Scholar
Schunk, M., Wachinger, W., and Nothdurft, H. D.. (2001). Vaccination status and prophylactic measures of travellers from Germany to subtropical and tropical areas: results of an airport survey. Journal of Travel Medicine, 8: 260–262.CrossRefGoogle Scholar
Sholley, C. (1989). Mountain gorilla update. Oryx, 23: 57–58.Google Scholar
Sholley, C. and Hastings, B. (1989). Outbreak of illness among Rwanda’s gorillas. Gorilla Conservation News, 3: 7.Google Scholar
Steffen, R., Tornieporth, N., Costa Clemens, S. A. et al. (2004). Epidemiology of travellers’ diarrhea: Details of a global survey. Journal of Travel Medicine, 11: 231–238.CrossRefGoogle Scholar
Toovey, S., Jamieson, A., and Holloway, M. (2004). Travellers’ knowledge, attitudes and practices on the prevention of infectious diseases: results from a study at Johannesburg International Airport. Journal of Travel Medicine, 11: 16–22.CrossRefGoogle Scholar
Van Herck, K., Castelli, F., Zuckerman, J. et al. (2004). Knowledge, attitudes and practices in travel-related infectious diseases: The European airport survey. Journal of Travel Medicine, 11: 3–8.CrossRefGoogle ScholarPubMed
Van Herck, K., Zuckerman, J., Castelli, F. et al. (2003). Travellers’ knowledge, attitudes, and practices on prevention of infectious diseases: Results from a pilot study. Journal of Travel Medicine, 10: 75–78.CrossRefGoogle Scholar
Van Heuverswyn, F., Li, Y., Neel, C. et al. (2006). SIV infection in wild gorillas. Nature, 444: 164.CrossRefGoogle ScholarPubMed
Wallis, J., and Lee, D. R. (1999). Primate conservation: The prevention of disease transmission. International Journal of Primatology, 20: 803–826.CrossRefGoogle Scholar
Wilder-Smith, A., Khairullah, N. S., Song, J. H., Chen, C. Y., and Torresi, J. (2004). Travel health knowledge, attitudes and practices among Australasian travellers. Journal of Travel Medicine, 11: 9–15.CrossRefGoogle Scholar
Williams, J. M., Londsdorf, E. V., Wilson, M. L. et al. (2008). Causes of death in the Kasekela chimpanzees of Gombe National Park, Tanzania. American Journal of Primatology, 70: 766–777.CrossRefGoogle ScholarPubMed
Woolhouse, M. and Gaunt, E. (2007). Ecological origins of novel human pathogens. Critical Reviews in Microbiology, 33: 1–12.CrossRefGoogle ScholarPubMed
Zuckerman, J. N. and Steffen, R. (2000). Risks of Hepatitis B in travellers as compared to immunization status. Journal of Travel Medicine, 7: 170–174.CrossRefGoogle Scholar

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