The tourism sector is a fast-growing contributor to the global economy, and nature-based tourism (NBT), particularly in Asia and Africa, is booming. Through the creation of jobs and revenue NBT has the potential to combat deforestation in regions that are economically poor, but of high biodiversity value. Inspired by the success of gorilla tourism in Uganda and Rwanda, several gibbon tourism projects have been initiated in Southeast Asia and China. Despite the existence of these programmes, no research has been done to investigate the impact of tourism on the behaviour of gibbons. To address this, we collected observational data on a group of northern yellow-cheeked crested gibbons (Nomascus annamensis) at Veun Sai-Siem Pang National Park (VSSPNP), Cambodia, in the presence and absence of tourists. We found there was a significant increase in the amount of time individuals spent scanning their environment and travelling at the cost of rest when in the presence of tourists. We also found that individuals were significantly more likely to self-groom in the presence of tourists. These results highlight the importance of scientific research in implementing successful, low-impact NBT programmes that consider animal behavioural changes. We are continuing to collect data on gibbons at VSSPNP and at Mt. Gaoligong National Nature Reserve, China with the aim of extending the IUCN’s best-practice guidelines for great-ape tourism to include the small apes.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
Aldabal, L. & Bahammam, A.S. (2011) Metabolic, endocrine, and immune consequences of sleep deprivation. Open Respir. Med. J., 5, 31-43. DOI:10.2174/1874306401105010031.
Balmford, A., Beresford, J., Green, J., Naidoo, R., Walpole, M. & Manica, A. (2009) A global perspective on trends in nature-based tourism. PLoS Biol., 7, e1000144. DOI:10.1371/journal.pbio.1000144.
Bates, D., Mächler, M., Bolker, B. & Walker, S. (2015) Fitting linear mixed-effects models using lme4. J. Stat. Softw., 67(1), 1-48. DOI:10.18637/jss.v067.i01.
Behie, A.M., Pavelka, M.S.M. & Chapman, C.A. (2010) Sources of variation in fecal cortisol levels in howler monkeys in Belize. Am. J. Primatol., 72, 600-606. DOI:10.1002/ajp.20813.
Brand USA (2015) Market Profiles. Available at https://www.thebrandusa.com/system/files/programs/documents/FY15BP_MarketProfiles_01.pdf.
Brockelman, W.Y. & Ali, R. (1987) Methods of surveying and sampling forest primate populations. In: C. Marsh & R.A. Mittermeier (Eds) Primate Conservation in the Tropical Rain Forest, pp. 23-62. Alan R. Liss, Inc., New York, NY, USA.
Bryant, P.A., Trinder, J. & Curtis, N. (2004) Sick and tired: does sleep have a vital role in the immune system? Nat. Rev. Immunol., 4, 457-467. DOI:10.1038/nri1369.
Canty, A. & Ripley, B. (2019) boot: Bootstrap R (S-Plus) Functions. R package version 1.3-22. https://cran.r-project.org/web/packages/boot/boot.pdf.
CEPF (2011) Indo-Burma Ecosystem profile summary. CEPF, Arlington, VA, USA. Available at https://www.cepf.net/sites/default/files/indoburma_ecosystem_profile_summary_english.pdf.
Cheyne, S.M. (2011) Gibbon locomotion research in the field: problems, possibilities, and benefits for conservation. In: K. D’Août & E. Vereecke (Eds) Primate Locomotion. Developments in Primatology: Progress and Prospects, pp. 201-213. Springer, New York, NY, USA.
Chin, C.L.M., Moore, S.A., Wallington, T.J. & Dowling, R.K. (2000) Ecotourism in Bako National Park, Borneo: visitors’ perspectives on environmental impacts and their management. J. Sustain. Tour., 8, 20-35. DOI:10.1080/09669580008667347.
Choi, Y.E., Song, K., Kim, M. & Lee, J. (2017) Transformation planning for resilient wildlife habitats in ecotourism systems. Sustainability, 9, 487. DOI:10.3390/su9040487.
Crofoot, M.C., Lambert, T.D., Kays, R. & Wikelski, M.C. (2010) Does watching a monkey change its behaviour? Quantifying observer effects in habituated wild primates using automated radiotelemetry. Anim. Behav., 80, 475-480. DOI:10.1016/j.anbehav.2010.06.006.
de la Torre, S. (2014) Effects of tourism on Ecuadorian primates: is there a need for responsible primate tourism?. In: A.E. Russon & J. Wallis (Eds) Primate Tourism: a Tool for Conservation?, pp. 245-255. Cambridge University Press, Cambridge, UK.
de la Torre, S., Snowdon, C.T. & Bejarano, M. (2000) Effects of human activities on wild pygmy marmosets in Ecuadorian Amazonia. Biol. Conserv., 94, 153-163. DOI:10.1016/S0006-3207(99)00183-4.
Desmond, J.S. & Desmond, J.A.Z. (2014) Evaluating the effectiveness of chimpanzee tourism. In: A.E. Russon & J. Wallis (Eds) Primate Tourism: a Tool for Conservation?, pp. 199-212. Cambridge University Press, Cambridge, UK.
Dongwen, L., Ganesh, S. & Koolaard, J. (2018) predictmeans: calculate predicted means for linear models. Available at https://cran.r-project.org/package=predictmeans.
Fan, P., Ni, Q., Sun, G., Huang, B. & Jiang, X. (2009) Gibbons under seasonal stress: the diet of the black crested Gibbon (Nomascus concolor) on Mt. Wuliang, Central Yunnan, China. Primates, 50, 37. DOI:10.1007/s10329-008-0114-1.
Fan, P.F. & Bartlett, T.Q. (2017) Overlooked small apes need more attention! Am. J. Primatol., 79, e22658. DOI:10.1002/ajp.22658.
Fawcett, K., Hodgkinson, C. & Mehlman, P. (2004) An assessment of the impact of tourism on the Virunga Mountain gorillas: phase I – analyzing the behavioral data from gorilla groups designated for tourism. Technical report, Diane Fossey Gorilla Fund International, Atlanta, GA, USA.
Fisher, B. & Christopher, T. (2007) Poverty and biodiversity: measuring the overlap of human poverty and the biodiversity hotspots. Ecol. Econ., 62, 93-101. DOI:10.1016/j.ecolecon.2006.05.020.
Fuentes, A. (2000) Hylobatid communities: changing views on pair bonding and social organization in hominoids. Am. J. Phys. Anthropol., 113, 33-60.
Fuentes, A. (2010) Naturalcultural encounters in Bali: monkeys, temples, tourists, and ethnoprimatology. Cult. Anthropol., 25, 600-624. DOI:10.1111/j.1548-1360.2010.01071.x.
Geissmann, T. (2002) Duet-splitting and the evolution of Gibbon songs. Biol. Rev, 77, 57-76. DOI:10.1017/S1464793101005826.
Gillespie, T.R., Barelli, C. & Heistermann, M. (2013) Effects of social status and stress on patterns of gastrointestinal parasitism in wild white-handed gibbons (Hylobates lar). Am. J. Phys. Anthropol., 150, 602-608. DOI:10.1002/ajpa.22232.
Goldberg, T.L., Gillespie, T.R., Rwego, I.B., Wheeler, E., Estoff, E.L. & Chapman, C.A. (2007) Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biol. Conserv., 135, 511-517. DOI:10.1016/j.biocon.2006.10.048.
Goldsmith, M.L. (2014) Mountain gorilla tourism as a conservation tool: have we tipped the balance?. In: A.E. Russon & J. Wallis (Eds) Primate Tourism: a Tool for Conservation?, pp. 177-198. Cambridge University Press, Cambridge, UK.
Grossberg, R., Treves, A. & Naughton-Treves, L. (2003) The incidental ecotourist: measuring visitor impacts on endangered howler monkeys at a Belizean archaeological site. Environ. Conserv., 30, 40-51. DOI:10.1017/S0376892903000031.
Halekoh, U. & Højsgaard, S. (2014) A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models – the R Package pbkrtest. J. Stat. Softw., 59(9), 1-30. DOI:10.18637/jss.v059.i09.
Harrison, X.A., Donaldson, L., Correa-Cano, M.E., Evans, J., Fisher, D.N., Goodwin, C.E.D., Robinson, B.S., Hodgson, D.J. & Inger, R. (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ, 6, e4794. DOI:10.7717/peerj.4794.
Higham, J.P., Kraus, C., Stahl-Hennig, C., Engelhardt, A., Fuchs, D. & Heistermann, M. (2015) Evaluating noninvasive markers of nonhuman primate immune activation and inflammation. Am. J. Phys. Anthropol., 158, 673-684. DOI:10.1002/ajpa.22821.
Hodgkinson, C. & Cipolletta, C. (2009) Western lowland gorilla tourism: impact on gorilla behaviour. Gorilla J., 38, 29-32.
Hughes, A.C. (2017) Understanding the drivers of southeast Asian biodiversity loss. Ecosphere, 8, e01624. DOI:10.1002/ecs2.1624.
Iseborn, T. (2011) Preliminary field survey of pygmy slow loris (Nycticebus pygmaeus) and Bengal slow loris (Nycticebus bengalensis); assessment of hunting pressure and local attitudes towards the two species in Veun Sai Forests, Cambodia. MSc thesis, Oxford Brookes University, Oxford, UK.
IUCN(SSA) (2018) Gibbon distribution map [WWW Document]. Available at https://gibbons.asia/wp-content/uploads/2018/10/small-map-02.png.
Johns, A.D. & Skorupa, J.P. (1987) Responses of rain-forest primates to habitat disturbance: a review. Int. J. Primatol., 8, 157. DOI:10.1007/BF02735162.
Kibria, A.S.M.G., Behie, A., Costanza, R., Groves, C. & Farrell, T. (2017) The value of ecosystem services obtained from the protected forest of Cambodia: the case of Veun Sai-Siem Pang National Park. Ecosyst. Serv., 26, 27-36. DOI:10.1016/j.ecoser.2017.05.008.
King, A., Behie, A.M., Naven, H. & Rawson, B.M. (2016) Patterns of salt lick use by mammals and birds in northeastern Cambodia. Cambodian J. Nat. Hist., 2016, 40-50.
Kinnaird, M.F. & O’Brien, T.G. (1996) Ecotourism in the Tangkoko DuaSudara Nature Reserve: opening Pandora’ box? Oryx., 30, 65-73. DOI:10.1017/S0030605300021402.
Klailova, M., Hodgkinson, C. & Lee, P.C. (2010) Behavioral responses of one western lowland gorilla (Gorilla gorilla gorilla) group at Bai Hokou, Central African Republic, to tourists, researchers and trackers. Am. J. Primatol., 71, 897-906. DOI:10.1002/ajp.20829.
Köndgen, S., Kühl, H., N’Goran, P.K., Walsh, P.D., Schenk, S., Ernst, N., Biek, R., Formenty, P., Mätz-Rensing, K., Schweiger, B., Junglen, S., Ellerbrok, H., Nitsche, A., Briese, T., Lipkin, W.I., Pauli, G., Boesch, C. & Leendertz, F.H. (2008) Pandemic human viruses cause decline of endangered great apes. Curr. Biol., 18, 260-264. DOI:10.1016/j.cub.2008.01.012.
Krueger, C. & Tian, L. (2004) A comparison of the general linear mixed model and repeated measures ANOVA using a dataset with multiple missing data points. Biol. Res. Nurs., 6, 151-157. DOI:10.1177/1099800404267682.
Kuznetsova, A., Brockhoff, P.B. & Christensen, R.H.B. (2017) lmerTest package: tests in linear mixed effects models. J. Stat. Softw., 82(13), 1-26. DOI:10.18637/jss.v082.i13.
Macfie, E.J. & Williamson, E.A. (2010) Best Practice Guidelines for Great Ape Tourism. IUCN, Gland, Switzerland.
Marshall, A.J. & Leighton, M. (2006) How does food availability limit the population density of white-bearded gibbons?. In: G. Hohmann, M.M. Robbins & C. Boesch (Eds) Feeding Ecology in Apes Other Primates. Ecological, Physical, and Behavioral Aspects, pp. 313-335. Cambridge University Press, Cambridge, UK.
Marshall, A.J., Boyko, C.M., Feilen, K.L., Boyko, R.H. & Leighton, M. (2009) Defining fallback foods and assessing their importance in primate ecology and evolution. Am. J. Phys. Anthropol., 140, 603-614. DOI:10.1002/ajpa.21082.
Martin, P. & Bateson, P. (1986) Measuring Behaviour: an Introductory Guide. Cambridge University Press, Cambridge, UK.
Möstl, E. & Palme, R. (2002) Hormones as indicators of stress. Domest. Anim. Endocrinol., 23, 67-74. DOI:10.1016/S0739-7240(02)00146-7.
Muehlenbein, M.P. & Wallis, J. (2014) Considering risks of pathogen transmission associated with primate-based tourism. In: A.E. Russon & J. Wallis (Eds) Primate Tourism: a Tool for Conservation?, pp. 278-287. Cambridge University Press, Cambridge, UK.
Muehlenbein, M.P., Ancrenaz, M., Sakong, R., Ambu, L., Prall, S., Fuller, G. & Raghanti, M.A. (2012) Ape conservation physiology: fecal glucocorticoid responses in wild Pongo pygmaeus morio following human visitation. PLoS One, 7, e33357. DOI:10.1371/journal.pone.0033357.
Muth, C., Bales, K.L., Hinde, K., Maninger, N., Mendoza, S.P. & Ferrer, E. (2016) Alternative models for small samples in psychological research: applying linear mixed effects models and generalized estimating equations to repeated measures data. Educ. Psychol. Meas., 76, 64-87. DOI:10.1177/0013164415580432.
Muyambi, F. (2005) The impact of tourism on the behaviour of mountain gorillas. Gorilla J., 30, 14-15.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853-858. DOI:10.1038/35002501.
Newsome, D., Moore, S.A. & Dowling, R.K. (2013) Natural Area Tourism: Ecology, Impacts and Management. 2nd Edition. Channel View Publications, Bristol, UK.
Patrono, L.V., Samuni, L., Corman, V.M., Nourifar, L., Röthemeier, C., Wittig, R.M., Drosten, C., Calvignac-Spencer, S. & Leendertz, F.H. (2018) Human coronavirus OC43 outbreak in wild chimpanzees, Côte d’Ivoire, 2016 correspondence. Emerg. Microbes Infect., 7, 1-4. DOI:10.1038/s41426-018-0121-2.
R Core Team (2019) R: a language and environment for statistical computing. Available at https://www.r-project.org.
Ramachandra, A., Uraguchi, A. & Rawson, B.M. (2012) Veun Sai-Siem Pang Conservation Area: REDD+ Pre-feasibility Study. Conservation International, Phnom Penh, Cambodia.
Rawson, B.M., Insua-Cao, P., Manh Ha, N., Ngoc Thinh, V., Minh Duc, H., Mahood, S., Geissmann, T. & Roos, C. (2011) The Conservation Status of Gibbons in Vietnam. Fauna Flora International & Conservation International, Hanoi, Vietnam.
Rawson, B.M., Reiter, C.N., Masphal, K., Morales, M. & Omaliss, K. (2012) Veun Sai-Siem Pang Conservation Area: Biodiversity Values and Conservation Plan. Conservation International, Phnom Penh, Cambodia.
Reichard, U.H., Ganpanakngan, M. & Barelli, C. (2012) White-handed gibbons of Khao Yai: social flexibility, complex reproductive strategies, and a slow life history. In: P. Kappeler & D. Watts (Eds) Long-Term Field Studies of Primates, pp. 237-258. Springer-Verlag, Berlin, Germany.
Reichard, U.H., Barelli, C., Hirohisa, H. & Nowak, M.G. (2016) The evolution of gibbons and siamang. In: U.H. Reichard, H. Hirohisa & C. Barelli (Eds) Evolution of Gibbons and Siamang. Developments in Primatology: Progress and Prospects, pp. 3-43. Springer, New York, NY, USA.
Reisland, M.A. & Lambert, J.E. (2016) Sympatric apes in sacred forests: shared space and habitat use by humans and endangered Javan gibbons (Hylobates moloch). PLoS One, 11, e0146891. DOI:10.1371/journal.pone.0146891.
Shutt, K., Heistermann, M., Kasim, A., Todd, A., Kalousova, B., Profosouva, I., Petrzelkova, K., Fuh, T., Dicky, J.-F., Bopalanzognako, J.-B. & Setchell, J.M. (2014) Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: implications for conservation management. Biol. Conserv., 172, 72-79. DOI:10.1016/j.biocon.2014.02.014.
Sojka, P.A., Ploog, C.L., Garner, M.M., Kiupel, M., Kuypers, J. & Huynh, T. (2020) Acute human orthopneumovirus infection in a captive white-handed Gibbon. J. Vet. Diagn. Invest. DOI:10.1177/1040638720910521.
Strum, S.C. & Manzolillo Nightingale, D.L. (2014) Baboon ecotourism in the larger context. In: A.E. Russon & J. Wallis (Eds) Primate Tourism: a Tool for Conservation?, pp. 155-175. Cambridge University Press, Cambridge, UK.
Treves, A. (2005) Tourist impacts on the behavior of black howling monkeys (Alouatta pigra) at Lamanai, Belize. In: J.D. Paterson & J. Wallis (Eds) Commensalism and Conflict: the Human–Primate Interface, pp. 147-167. American Society of Primatologists, Norman, OK, USA.
Twining-Ward, L., Li, W., Bhammar, H. & Wright, E. (2018) Supporting Sustainable Livelihoods Through Wildlife Tourism. World Bank, Washington, DC, USA.
UNWTO (2018) UNWTO Tourism Highlights: 2018 Edition. World Tourism Organization (UNWTO), Madrid, Spain.
Wagner, K.E., Hopper, L.M. & Ross, S.R. (2016) Asymmetries in the production of self-directed behavior by chimpanzees and gorillas during a computerized cognitive test. Anim. Cogn., 19, 343-350. DOI:10.1007/s10071-015-0937-2.
Wright, P.C., Andriamihaja, B., King, S.J., Guerriero, J. & Hubbard, J. (2014) Lemurs and tourism in Ranomafana National Park, Madagascar: economic boom and other consequences. In: A.E. Russon & J. Wallis (Eds) Primate Tourism: a Tool for Conservation?, pp. 123-146. Cambridge University Press, Cambridge, UK.
Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. & Smith, G.M. (2009) Mixed Effects Models and Extensions in Ecology with R. Springer Science & Business Media, New York, NY, USA.
All Time | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 833 | 221 | 26 |
Full Text Views | 97 | 39 | 0 |
PDF Views & Downloads | 72 | 16 | 0 |
The tourism sector is a fast-growing contributor to the global economy, and nature-based tourism (NBT), particularly in Asia and Africa, is booming. Through the creation of jobs and revenue NBT has the potential to combat deforestation in regions that are economically poor, but of high biodiversity value. Inspired by the success of gorilla tourism in Uganda and Rwanda, several gibbon tourism projects have been initiated in Southeast Asia and China. Despite the existence of these programmes, no research has been done to investigate the impact of tourism on the behaviour of gibbons. To address this, we collected observational data on a group of northern yellow-cheeked crested gibbons (Nomascus annamensis) at Veun Sai-Siem Pang National Park (VSSPNP), Cambodia, in the presence and absence of tourists. We found there was a significant increase in the amount of time individuals spent scanning their environment and travelling at the cost of rest when in the presence of tourists. We also found that individuals were significantly more likely to self-groom in the presence of tourists. These results highlight the importance of scientific research in implementing successful, low-impact NBT programmes that consider animal behavioural changes. We are continuing to collect data on gibbons at VSSPNP and at Mt. Gaoligong National Nature Reserve, China with the aim of extending the IUCN’s best-practice guidelines for great-ape tourism to include the small apes.
All Time | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 833 | 221 | 26 |
Full Text Views | 97 | 39 | 0 |
PDF Views & Downloads | 72 | 16 | 0 |