Travel Medicine and Infectious Disease
Volume 8, Issue 3 , Pages 169-175 , May 2010

Unhealthy travelers present challenges to sustainable primate ecotourism

  • Michael P. Muehlenbein

      Affiliations

    • Department of Anthropology, Indiana University, 701 E. Kirkwood Ave., Student Building 130, Bloomington, IN 47405-7000, USA
    • Sabah Wildlife Department, 5th Floor, B Block, Wisma MUIS, Kota Kinabalu 88100, Sabah, Malaysia
    • Corresponding Author InformationCorresponding author. Department of Anthropology, Indiana University, 701 E. Kirkwood Ave., Student Building 130, Bloomington, IN 47405-7000, USA. Tel.: +1 812 855 1495; fax: +1 812 855 4358.
    • ,
  • Leigh Ann Martinez

      Affiliations

    • Department of Anthropology, Indiana University, 701 E. Kirkwood Ave., Student Building 130, Bloomington, IN 47405-7000, USA
    • ,
  • Andrea A. Lemke

      Affiliations

    • Department of Anthropology, University of Wisconsin, 3413 N. Downer Ave., Sabin Hall 290, Milwaukee, WI 53201, USA
    • ,
  • Laurentius Ambu

      Affiliations

    • Sabah Wildlife Department, 5th Floor, B Block, Wisma MUIS, Kota Kinabalu 88100, Sabah, Malaysia
    • ,
  • Senthilvel Nathan

      Affiliations

    • Sabah Wildlife Department, 5th Floor, B Block, Wisma MUIS, Kota Kinabalu 88100, Sabah, Malaysia
    • ,
  • Sylvia Alsisto

      Affiliations

    • Sabah Wildlife Department, 5th Floor, B Block, Wisma MUIS, Kota Kinabalu 88100, Sabah, Malaysia
    • ,
  • Rosman Sakong

      Affiliations

    • Red Ape Encounters, P.O. Box 3109, Sandakan 90734, Sabah, Malaysia

Received 19 October 2009 ,Revised 23 February 2010 ,Accepted 17 March 2010.

References 

  1. Filion FL, Foley JP, Jacqemot AJ. The economics of global ecotourism. In:  Munasinghe M,  McNealy J editor. Protected area economics and policy: linking conservation and sustainable development. Washington, DC: The World Bank; 1994;p. 235–252
  2. In:  Munasinghe M,  McNealy J editor. Protected area economics and policy: linking conservation and sustainable development. Washington, DC: The World Bank; 1994;
  3. Mowforth M, Munt I. Tourism and sustainability: development and new tourism in the third world. London: Routledge; 2003;
  4. Schoene CUR, Brend SA. Primate sanctuaries – a delicate conservation approach. South African Journal Wildlife Research. 2002;32:109–113
  5. Bruner AG, Gullison RE, Rice RE, da Fonseca GAB. Effectiveness of parks in protecting tropical biodiversity. Science. 2001;291:125–128
  6. Jaffe E. Good gone wild: sometimes, ecotourism hurts what it sets out to help. Science. 2006;170:218–220
  7. Berman CM, Jinhua L, Ogawa H, Ionica C, Yin H. Primate tourism, range restriction, and infant risk among Macaca thibetana at Mt. Huangshan, China. International Journal of Primatology. 2007;28:1123–1141
  8. Walker BG, Dee Boersma P, Wingfield JC. Habituation of adult magellanic penguins to human visitation as expressed through behavior and corticosterone secretion. Conservation Biology. 2006;20:146–154
  9. Romero LM, Wikelski M. Exposure to tourism reduces stress-induced corticosterone levels in Galápagos marine iguanas. Biological Conservation. 2002;108:371–374
  10. Romero LM. Physiological stress in ecology: lessons from biomedical research. Trends in Ecology and Evolution. 2004;19:249–255
  11. Sapolsky RM, Romero LM, Minck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews. 2000;21:55–89
  12. Muehlenbein MP. The application of endocrine measures in primate parasite ecology. In:  Huffman M,  Chapman C editor. Primate parasite ecology: the dynamics of host-parasite relationships. New York: Cambridge University Press; 2009;p. 63–81
  13. Muyambi F. The impact of tourism on the behaviour of mountain gorillas. Gorilla Journal. 2005;30:14–15
  14. Brack M. Agents transmissible from simians to man. Berlin: Springer-Verlag; 1987;
  15. Reinquist DM, Whitney RA. Zoonoses acquired from pet primates. Veterinary Clinics of North America-Small Animal Practice. 1987;17:219–240
  16. Woodford MH, Butynski TM, Karesh WB. Habituating the great apes: the disease risks. Oryx. 2002;36:153–160
  17. Köndgen S, Kühl H, N'Goran PK, Walsh PD, Schenk S, Ernst N, et al. Pandemic human viruses cause decline of endangered great apes. Current Biology. 2008;18:1–5
  18. Graczyk TK, Nizeyi JB, Ssebide B, Thompson RCA, Read C, Cranfield MR. Anthropozoonotic Giardia duodenalis genotype (assemblage) a infections in habitats of free-ranging human-habituated gorillas, Uganda. Journal of Parasitology. 2002;88:905–909
  19. Goldberg TL, Gillespie TR, Rwego IB, Wheeler E, Estoff EL, Chapman CA. Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biological Conservation. 2007;135:511–517
  20. Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL. Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conservation Biology. 2008;22:1600–1607
  21. Rolland RM, Hausfater G, Marshall B, Levy SB. Antibiotic-resistant bacteria in wild primates: increased prevalence in baboons feeding on human refuse. Applied Environmental Microbiology. 1985;49:791–794
  22. Ashford RW, Reid GDF, Butynski TM. The intestinal faunas of man and mountain gorillas in a shared habitat. Annals of Tropical Medicine and Parasitology. 1990;84:337–340
  23. Nizeyi JB, Mwebe R, Nanteza A, Cranfield MR, Kalema GRNN, Graczyk TK. Campylobacteriosis, salmonellosis, and shigellosis in free-ranging human-habituated mountain gorillas of Uganda. Journal of Wildlife Diseases. 2001;37:239–244
  24. Graczyk TK, Nizeyi JB, da Silva AJ, Moura INS, Pieniazek NJ, Cranfield MR, et al. A single genotype of Encephalitozoon intestinalis infects free-ranging gorillas and people sharing their habitats in Uganda. Parasitology Research. 2002;88:926–931
  25. Mountain Gorilla Veterinary Project 2002 Employee Health Group . Risk of disease transmission between conservation personnel and the mountain gorillas: results from an employee health program in Rwanda. EcoHealth. 2004;1:351–361
  26. Goodall J. The chimpanzees of Gombe: patterns of behavior. Cambridge, MA: Harvard University Press; 1986;
  27. Kortlandt A. An epidemic of limb paresis (polio?) among the chimpanzee population at Beni (Zaire) in 1964, possibly transmitted by humans. Pan Africa News. 1996;3:9–10
  28. Byers AC, Hastings B. Mountain gorilla mortality and climatic factors in the Parc National des Volcans, Ruhengeri Prefecture, Rwanda, 1988. Mountain Research and Development. 1991;2:145–151
  29. Hosaka K. Epidemics and wild chimpanzee study groups. Pan Africa News. 1995;2:1–4
  30. Wallis J, Lee DR. Primate conservation: the prevention of disease transmission. International Journal of Primatology. 1999;20:803–826
  31. Macfie L. Case report on scabies infection in Bwindi gorillas. Gorilla Journal. 1996;13:19–20
  32. Mueller-Graf CDM, Collins DA, Packer C, Woolhouse MEJ. Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology. 1997;115:621–627
  33. Van Herck K, Castelli F, Zuckerman J, Nothdurft H, Van Damme P, Dahlgren AL, et al. Knowledge, attitudes and practices in travel-related infectious diseases: the European airport survey. Journal of Travel Medicine. 2004;11:3–8
  34. Van Herck K, Zuckerman J, Castelli F, Van Damme P, Walker E, Steffen R. Traveler's knowledge, attitudes, and practices on prevention of infectious diseases: results from a pilot study. Journal of Travel Medicine. 2003;10:75–78
  35. Wilder-Smith A, Khairullah NS, Song JH, Chen CY, Torresi J. Travel health knowledge, attitudes and practices among Australasian travelers. Journal of Travel Medicine. 2004;11:9–15
  36. Steffen R, Tornieporth N, Costa Clemens SA, Chatterjee S, Cavalcanti AM, Collard F, et al. Epidemiology of travelers' diarrhea: details of a global survey. Journal of Travel Medicine. 2004;11:231–238
  37. Toovey S, Jamieson A, Holloway M. Travelers' knowledge, attitudes and practices on the prevention of infectious diseases: results from a study at Johannesburg International Airport. Journal of Travel Medicine. 2004;11:16–22
  38. Hilton E, Singer C, Kozarsky P, Smith M, Lardis MP, Borenstein MT. Status of immunity to tetanus, measles, mumps, rubella, and polio among US travelers. Annals of Internal Medicine. 1991;115:32–33
  39. Rack J, Wichmann O, Kamara B, Gunther M, Cramer J, Schonfeld C, et al. Risk and spectrum of diseases in travelers to popular tourist destinations. Journal of Travel Medicine. 2005;12:248–253
  40. Muehlenbein MP, Martinez LA, Lemke AA, Ambu L, Nathan S, Andau P, et al. Perceived vaccination status in ecotourists and risks of anthropozoonoses. EcoHealth. 2008;5:371–378
  41. Adams HR, Sleeman JM, Rwego I, New JC. Self-reported medical history survey of humans as a measure of health risk to the chimpanzees (Pan troglodytes schweinfurthii) of Kibale National Park, Uganda. Oryx. 2001;35:308–312
  42. Mawdsley JL, Bardgett RD, Merry RJ, Pain BF, Theodorou MK. Pathogens in livestock waste, their potential movement through soil and environmental pollution. Applied Soil Ecology. 1995;2:1–15
  43. Cleaveland S, Laurenson MK, Taylor LH. Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philosophical Transactions of the Royal Society of London Series B. 2001;356:991–999
  44. Wolfe ND, Kilbourn AM, Karesh WB, Rahman HA, Bosi EJ, Cropp BC, et al. Sylvatic transmission of arboviruses among Bornean orangutans. American Journal of Tropical Medicine and Hygiene. 2001;64:310–316
  45. Kilbourn AM, Karesh WB, Wolfe ND, Bosi EJ, Cook RA, Andau M. Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia. Journal of Wildlife Diseases. 2003;39:73–83
  46. Wolfe ND, Karesh WB, Kilbourn AM, Cox-Singh J, Bosi EJ, Rahman HA, et al. The impact of ecological conditions on the prevalence of malaria among orangutans. Vector-Borne and Zoonotic Diseases. 2002;2:97–103
  47. Woolhouse M, Gaunt E. Ecological origins of novel human pathogens. Critical Reviews in Microbiology. 2007;33:1–12
  48. Mak JW, Cheong WH, Yen PK, Lim PK, Chan WC. Studies on the epidemiology of subperiodic Brugia malayi in Malaysia: problems in its control. Acta Tropica. 1982;39:237–245
  49. McIntosh BM. Antibody against Chikungunya virus in wild primates in Southern Africa. South African Journal of Medical Sciences. 1970;35:65–74
  50. Monath TP. Yellow fever: an update. Lancet Infectious Diseases. 2001;1:11–20
  51. Nizeyi JB, Sebunya D, Dasilva AJ, Cranfield MR, Pieniazek NJ, Graczyk TK. Cryptosporidiosis in people sharing habitats with free-ranging mountain gorillas (Gorilla gorilla beringei), Uganda. American Journal of Tropical Medicine and Hygiene. 2002;66:442–444
  52. Singh B, Kim Sing L, Matusop A, Radhakrishnan A, Shamsul SS, Cox-Singh J, et al. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet. 2004;363:1017–1024
  53. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 1999;397:436–441
  54. Wolfe ND, Henien W, Carr JK, Garcia AD, Shanmugam V, Tamoufe U, et al. Emergence of unique primate T-lymphotropic viruses among central African bushmeat hunters. Proceedings of the National Academy of Sciences USA. 2005;102:7994–7999
  55. Wolfe ND, Switzer WM, Carr JK, Bhullar VB, Shanmugam V, Tamoufe U, et al. Naturally acquired simian retrovirus infections in central African hunters. Lancet. 2004;363:932–937
  56. Jones-Engel L, Engel GA, Schillaci MA, Rompis A, Putra A, Suaryana KG, et al. Primate-to-human retroviral transmission in Asia. Emerging Infectious Diseases. 2005;11:1028–1035
  57. Engel GA, Jones-Engel L, Schillaci MA, Suaryana KG, Putra A, Fuentes A, et al. Human exposure to herpesvirus B-seropositive macaques, Bali, Indonesia. Emerging Infectious Diseases. 2002;8:789–795
  58. Ostrowski SR, Leslie MJ, Parrott T, Abelt S, Piercy PE. B-virus from pet macaque monkeys: an emerging threat in the United States?. Emerging Infectious Diseases. 1998;4:117–121
  59. Homsey J. Ape tourism and human diseases: how close should we get? Report for the International Gorilla Conservation Programme Regional Meeting. Rwanda; 1999.
  60. Jane Goodall Institute . Chimpanzee ecotourism health protocol manual. Entebbe: Uganda: Jane Goodall Institute; 2006;
  61. Leendertz FH. Pathogens as drivers of population declines: the importance of systematic monitoring in great apes and other threatened mammals. Biological Conservation. 2006;131:325–337
  62. Muehlenbein MP, Ancrenaz M. Minimizing pathogen transmission at primate ecotourism destinations: the need for input from travel medicine. Journal of Travel Medicine. 2009;16:229–232
  63. Ceballos-Lascurán H. Tourism, ecotourism, and protected areas: the state of nature-based tourism around the world and guidelines for its development. Gland, Switzerland: World Conservation Union; 1996;
  64. Eagles PFJ, McCool SF, Haynes CD. Sustainable tourism in protected areas: guidelines for planning and management. Gland, Switzerland: World Conservation Union; 2002;
  65. Ecotourism Society . Ecotourism guidelines for nature tour operators. North Bennington, Vermont: The Ecotourism Society; 1993;
  66. World Tourism Organization . World ecotourism summit – final report. Madrid, Spain: World Tourism Organization and the United Nations Economic Programme; 2002;
  67. Horvath LL, Murray CK, DuPont HL. Travel health information at commercial travel websites. Journal of Travel Medicine. 2003;10:272–279
  68. Sandbrook C, Semple S. The rules and reality of mountain gorilla Gorilla beringei beringei tracking: how close do tourists get?. Oryx. 2006;40:428–433

PII: S1477-8939(10)00037-2

doi: 10.1016/j.tmaid.2010.03.004

Travel Medicine and Infectious Disease
Volume 8, Issue 3 , Pages 169-175 , May 2010

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