Northern yellow-cheeked crested gibbons (Nomascus annamensis) travel and scan more at the cost of rest when in the presence of tourists

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  • 1 School of Archaeology and Anthropology, Australian National University, Canberra, Australia

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Abstract

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.

  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • Fuentes, A. (2000) Hylobatid communities: changing views on pair bonding and social organization in hominoids. Am. J. Phys. Anthropol., 113, 33-60.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • Newsome, D., Moore, S.A. & Dowling, R.K. (2013) Natural Area Tourism: Ecology, Impacts and Management. 2nd Edition. Channel View Publications, Bristol, UK.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • Twining-Ward, L., Li, W., Bhammar, H. & Wright, E. (2018) Supporting Sustainable Livelihoods Through Wildlife Tourism. World Bank, Washington, DC, USA.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation
  • 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.

    • Search Google Scholar
    • Export Citation

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