Abstract
There is an assumption that apparent tolerance of tourists at long-running primate tourism sites indicates habituation and that as a result primates no longer experience negative consequences of prolonged exposure to visitors. We examined effects of tourist presence on stress-related behavior in three groups of critically endangered, wild crested macaques (Macaca nigra) exposed to different intensities of tourism in Tangkoko Nature Reserve, Sulawesi, Indonesia. Group R2 has been exposed to research + intensive tourism for over 3 decades, R1 to research + less intensive tourism (1 decade), and PB1 to research only. Almost 740 h of data were collected from 33 adults via focal animal, all occurrence, and 1/0 sampling. All data were analyzed with general linear mixed models. Behavior appeared to be inhibited when tourists were in the forest, but not within groups; all groups vocalized less, exhibited fewer sexual behaviors and displayed fewer self-directed behaviors in months with greater numbers of tourists. When tourists were present vs. absent within groups, females displayed less affiliation, and males and females displayed more aggression, consistent with responses to uncertainty in the presence of tourists. Our results indicate that crested macaque groups exposed to tourism even for decades may not fully habituate to tourists. We tentatively suggest that their behavioral responses to tourists resemble typical responses of primates to perceived predators posing varying degrees of risk.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
Literature Cited
Aguilar-Melo AR, Andresen E, Cristóbal-Azkarate J, Arroyo-Rodríguez V, Chavira R, Schondube J, Cuarón AD (2013) Behavioral and physiological responses to subgroup size and number of people in howler monkeys inhabiting a forest fragment used for nature-based tourism. Am J Primatol 75(11):1108–1116
Balasubramaniam KN, Marty PR, Arlet ME, Beisner BA, Kaburu SSK, Bliss-Moreau E, Kodandaramaiah U, McCowan B (2020a) Impact of anthropogenic factors on affiliative behaviors among bonnet macaques. Am J Phys Anthropol 171:704–717
Balasubramaniam KN, Marty PR, Samartino S, Sobrino A, Gill T, Ismail M, Saha R, Beisner BA, Beisner BA, Kaburu SSK, Bliss-Moreau E, Arlet ME, Ruppert N, Ismail A, Sah SAM, Mohan L, Rattan SK, Kodandaramaiah U, McCowan B (2020b) Impact of individual demographic and social factors on human–wildlife interactions: a comparative study of three macaque species. Sci Rep 10:21991. https://doi.org/10.1038/s41598-020-78881-3
Barros M, de Souza Silva MA, Huston JP, Tomaz C (2004) Multibehavioral analysis of fear and anxiety before, during, and after experimentally induced predatory stress in Callithrix penicillata. Pharmacol Biochem Behav 78(2):357–367
Beale CM, Monaghan P (2004) Human disturbance: people as predation-free predators? J Appl Ecol 41:335–343
Beauchamp G (2015). Animal vigilance: monitoring predators and competitors
Beehner JC, Bergman TJ (2017) The next step for stress research in primates: to identify relationships between glucocorticoid secretion and fitness. Horm Behav 91:68–83
Behie AM, Pavelka MS, Chapman CA (2010) Sources of variation in fecal cortisol levels in howler monkeys in Belize. Am J Primatol 72(7):600–606
Bejder L, Samuels A, Whitehead H, Finn H, Allen S (2009) Impact assessment research: use and misuse of habituation, sensitisation and tolerance in describing wildlife responses to anthropogenic stimuli. Mar Ecol Prog Ser 395:177–185
Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM, Whitten PL (2005) Correlates of stress in free-ranging male chacma baboons, Papio hamadryas ursinus. Anim Behav 70(3):703–713
Blumstein D (2016) Habituation and sensitization: new thoughts about old ideas. Anim Behav 120:255–262
Blurton Jones NG (1968) Observations and experiments on causation of threat displays of the great tit (Parus major). Anim Behav Monogr 1(2):73–158
Cañadas Santiago S, Dias PAD, Garau S, Coyohua Fuentes A, Chavira Ramírez DR, Canales Espinosa D, Rangel Negrín A (2019) Behavioral and physiological stress responses to local spatial disturbance and human activities by howler monkeys at Los Tuxtlas, Mexico. Anim Conserv 23:297–306
Cavigelli SA, Caruso MJ (2015) Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics. Philos Trans R Soc B Biol Sci 370(1669):20140103
Chamove AS, Hosey GR, Schaetzel P (1988) Visitors excite primates in zoos. Zoo Biol 7:359–369
Cheney DL, Seyfarth RM (1981) Selective forces affecting the predator alarm calls of vervet monkeys. Behaviour 76(1–2):25–61
Clarke MR, Harrison RM, Didier ES (1996) Behavioral, immunological, and hormonal responses associated with social change in rhesus monkeys (Macaca mulatta). Am J Primatol 39:223–233
Coleman K (2012) Individual differences in temperament and behavioral management practices for nonhuman primates. Appl Anim Behav Sci 137:106–113
Danish L, Kerhoas D, Bertrand D, Febriyanti DY, Engelhardt A (2017) Macaca nigra (Desmarest, 1822). In: Schwitzer C, Mittermeier RA, Rylands AB, Chiozza F, Williamson EA, Macfie EJ, Wallis J, Cotton A (eds) Primates in peril: the world’s 25 most endangered primates 2016–2018. IUCN SSC Primate Specialist Group (PSG)/International Primatological Society (IPS)/Conservation International (CI), and Bristol Zoological Society, Arlington, pp 64–67
Duboscq J, Micheletta J, Agil M, Hodges K, Thierry B, Engelhardt A (2013) Social tolerance in wild female crested macaques (Macaca nigra) in Tangkoko-Batuangus Nature Reserve, Sulawesi, Indonesia. Am J Primatol 75(4):361–375
Duboscq J, Romano V, Sueur C, MacIntosh AJJ (2016) Scratch that itch: revisiting links between self-directed behaviour and parasitological, social and environmental factors in a free-ranging primate. R Soc Open Sci 3:160571
Elston DA, Moss R, Boulinier T, Arrowsmith C, Lambin X (2001) Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122(5):563–569
Engelhardt A, Perwitasari-Farajallah D (2008) Reproductive biology of Sulawesi crested black macaques (Macaca nigra). Folia Primatol 79:326
Engelhardt A, Heistermann M, Agil M, Perwitasari-Farajallah D, Higham J (2011) A despotic mating system in a socially tolerant primate, the crested macaque. Unpublished
Fichtel C, Kraus C, Ganswindt A, Heistermann M (2007) Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux’s sifakas (Propithecus verreauxi). Horm Behav 51(5):640–648
Foley CAH, Papageorge S, Wasser SK (2001) Noninvasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants. Conserv Biol 15:1134–1142
Frid A, Dill LM (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6(1):11
Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Belknap Press of Harvard University Press, Cambridge, MA
Hahn-Holbrook J, Holt-Lunstad J, Holbrook C, Coyne SM, Lawson ET (2011) Maternal defense: breast feeding increases aggression by reducing stress. Psychol Sci 22(10):1288–1295
Hanson KT, Riley E (2017) Beyond neutrality: the human–primate interface during the habituation process. Int J Primatol 39:852–877
Higham JP, Maclarnon AM, Heistermann M, Ross C, Semple S (2009) Rates of self-directed behaviour and faecal glucocorticoid levels are not correlated in female wild olive baboons (Papio hamadryas anubis). Stress 12(6):526–532
Hilser H, Sampson H, Melfi V, Tasirin JS (2013) Sulawesi crested black macaque Macaca nigra species action plan: draft 1. Selamatkan Yaki/Pacific Institute, Manado
Hinde RA (1970) Animal behaviour: a synthesis of ethology and comparative psychology. McGraw-Hill, New York
Hinde RA (1974) Biological bases of human social behaviour. McGraw-Hill, New York
IUCN (2022) IUCN red list of threatened species. Version 2020–2. www.iucnredlist.org. Downloaded 18 Sept 2022
Jack KM, Lenz BB, Healan E, Rudman S, Schoof VA, Fedigan L (2008) The effects of observer presence on the behavior of Cebus capucinus in Costa Rica. Am J Primatol 70:490–494
Johns BG (1996) Responses of chimpanzees to habituation and tourism in the Kibale Forest, Uganda. Biol Conserv 78:257–262
Kinnaird MF, O’Brien TG (1996) Ecotourism in the Tangkoko DuaSudara Nature Reserve: opening Pandora’s box? Oryx 30(1):65–73
Knight J (2009) Making wildlife viewable: habituation and attraction. Soc Anim 17:167–184
Kyes R, Iskandar E, Onibala J, Paputungan U, Laatung S, Huettmann F (2012) Long-term population survey of the Sulawesi Black Macaques (Macaca nigra) at Tangkoko Nature Reserve, North Sulawesi, Indonesia. Am J Primatol 75(1):88–94
Laméris DW, van Berlo E, Sterck EH, Bionda T, Kret ME (2020) Low relationship quality predicts scratch contagion during tense situations in orangutans (Pongo pygmaeus). Am J Primatol 82:e23138
Leasor H, Macgregor O (2014) Proboscis monkey tourism. In: Russon A, Wallis J (eds) Primate tourism: a tool for conservation? Cambridge University Press, Cambridge, pp 56–75
MacDougall-Shackleton SA, Bonier F, Romero LM, Moore IT (2019) Glucocorticoids and “stress” are not synonymous. Integr Org Biol 1(1):obz017
MacKinnon J, MacKinnon K (1980) The behavior of wild spectral tarsiers. Int J Primatol 1:361–379
Maestripieri D, Schino G, Aurel F, Troisi A (1992) A modest proposal: displacement activities as an indicator of emotions in primates. Anim Behav 44:967–979
Maréchal L, Semple S, Majolo B, Qarro M, Heistermann M, MacLarnon A (2011) Impacts of tourism on anxiety and physiological stress levels in wild male Barbary macaques. Biol Conserv 144(9):2188–2193
Maréchal L, Semple S, Majolo B, MacLarnon A (2016) Assessing the effects of tourist provisioning on the health of wild Barbary macaques in Morocco. PLoS One 11(5):e0155920
Martin JGA, Réale D (2008) Animal temperament and human disturbance: implications for the response of wildlife to tourism. Behav Process 77(1):66–72
Marty PR, Hodges K, Heistermann M, Agil M, Engelhardt A (2017a) Is social dispersal stressful? A study in male crested macaques (Macaca nigra). Horm Behav 87:62–68
Marty PR, Hodges K, Agil M, Engelhardt A (2017b) Alpha male replacements and delayed dispersal in crested macaques (Macaca nigra). Am J Primatol 79(7):e22448
Marty PR, Beisner B, Kaburu SSK, Balasubramaniam K, Bliss-Moreau E, Nadine Ruppert N, Sah SAM, Ismail A, Arlet ME, Atwill ER, McCowan B (2019) Time constraints imposed by anthropogenic environments alter social behaviour in longtailed macaques. Anim Behav 150:157–165
Matheson MD, Sheeran LK, Li JH, Wagner RS (2006) Tourist impact on Tibetan macaques. Anthrozoös 19(2):158–167
McDougall P (2012) Is passive observation of habituated animals truly passive?. J Ethol 30:219–223. https://doi.org/10.1007/s10164-011-0313-x
Mitchell G, Obradovich S, Herring F (1991) Threats to observers, keepers, visitors, and others by zoo mangabeys (Cercocebus galeritus chrysogaster). Primates 34(4):515–552
Moberg GP (2000) Biological response to stress: implications for animal welfare. In: Moberg GP, Mench JA (eds) The biology of human stress. CABI Publishing, Wallingford, pp 123–146
Muller K (1992) Underwater Indonesia. A guide to the world’s greatest diving. Periplus Editions, Singapore
Muller MN, Wrangham RW (2004) Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behav Ecol Sociobiol 55:332–340
Munck A, Guyre PM, Holbrook NI (1984) Physiological functions of glucocorticoids in stress and their relationship to pharmacological actions. Endocrinol Rev 5:25–44
Nakamichi M, Koyama N (2000) Intra-troop affiliative relationships of females with newborn infants in wild ring-tailed lemurs (Lemur catta). Am J Primatol 50:187–203
Natural Resources Management Project (1993) Ecotourism development in Bunaken National Park and North Sulawesi. Report no. 30 to Associates in Rural Development for Office of Agro-Enterprise and Environment, AID contract no. 497–0362
Neal SJ, Caine NG (2016) Scratching under positive and negative arousal in common marmosets (Callithrix jacchus). Am J Primatol 78:216–226
O’Brien TG, Kinnaird MF (1997) Behavior, diet, and movements of the Sulawesi Crested Black Macaque (Macaca nigra). Int J Primatol 18(3):321–351
Palacios JFG, Engelhardt A, Agil A, Hodges K, Bogia R, Waltert M (2011) Status of, and conservation recommendations for, the critically endangered crested black macaque Macaca nigra in Tangkoko, Indonesia. Oryx 46:290–297
Palagi E, Norscia I (2011) Scratching around stress: hierarchy and reconciliation make the difference in wild brown lemurs (Eulemur fulvus). Stress 14:93–97
Paulsen D (2009) The behavioral and physiological effects of ecotourism on the Sulawesi black macaques at the Tangkoko Nature Reserve, North Sulawesi, Indonesia. (Doctoral Dissertation), University of Washington
Pérez-Galicia S, Miranda-Anaya M, Canales-Espinosa D, Muñoz-Delgado J (2017) Visitor effect on the behavior of a group of spider monkeys (Ateles geoffroyi) maintained at an island in Lake Catemaco, Veracruz/Mexico. Zoo Biol 36:360–366
Pride RE (2005) Foraging success, agonism, and predator alarms: behavioral predictors of cortisol in Lemur catta. Int J Primatol 26:295–319
Rangel-Negrín A, Coyohua-Fuentes A, Chavira R, Canales-Espinosa D, Dias PAD (2014) Primates living outside protected habitats are more stressed: the case of black howler monkeys in the Yucatán Peninsula. PLoS One 9(11):e112329
Reed C, O’Brien TG, Kinnaird MF (1997) Male social behavior and dominance hierarchy in the Sulawesi Crested Black Macaque (Macaca nigra). Int J Primatol 18(2):247–260
Rhee S, Kitchener D, Brown T, Merrill R, Dilts R, Tighe S, USAID-Indonesia (2004) Report on Biodiversity and Tropical Forests in Indonesia. Submitted in Accordance with Foreign Assistance Act Sections 118/119, 1–316. Retrieved from http://www.irgltd.com/Resources/Publications/ANE/2004-02 Indonesia Biodiversity and Tropical Forest.pdf
Riley E (2010) The endemic seven: four decades of research on the Sulawesi macaque. Evol Anthropol 19:22–36
Roelofs K (2017) Freeze for action: neurobiological mechanisms in animal and human freezing. Philos Trans R Soc Lond Ser B Biol Sci 372(1718):20160206
Rosenbaum B, O’Brien TG, Kinnaird M, Supriatna J (1998) Population densities of Sulawesi crested black macaques (Macaca nigra) on Bacan and Sulawesi, Indonesia: effects of habitat disturbance and hunting. Am J Primatol 44:89–106
Rowell TE, Hinde RA (1963) Responses of rhesus monkeys to mildly stressful situations. Anim Behav 11:235–243
Sapolsky RM (1986) Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). Am J Primatol 11:217–227
Sapolsky RM (1992) Stress, the aging brain, and the mechanisms of neuron death. MIT Press, London
Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652
Sapolsky R, Romero L, Munck A (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21(1):55–89
Sari IR (2013) Anthropogenic effects on habitat use, activity budget, and energy balance in Macaca nigra at Tangkoko Nature Reserve, North Sulawesi, Indonesia (Master’s thesis). Georg-August University Göttingen
Schel A, Zuberbühler K (2009) Responses to leopards are independent of experience in Guereza colobus monkeys. Behaviour 146:1709–1737
Schino G, Perretta G, Taglioni AM, Monaco V, Troisi A (1996) Primate displacement activities as an ethnopharmacological model of anxiety. Anxiety 2:238–263
Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166(4):869–887
Shutt K, Heistermann M, Kasim A, Todd A, Kalousova B, Profosouva I, Petrzelkova K, Fuh T, Dicky J, Bopalanzognako J, Setchell JM (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
Stanford CB (2002) Avoiding predators: expectations and evidence in primate antipredator behavior. Int J Primatol 23(4):741–757
Sugardjito J, Southwick CJ, Supriatna J, Kohlhass A, Baker S, Erwin J, Froehlich J, Lerche N (1989) Population survey of macaques in Northern Sulawesi. Am J Primatol 18:285–301
Supriatna J, Andayani N (2008) Macaca nigra. The IUCN red list of threatened species 2008: e.T12556A3357272
Supriatna J, Shekelle M, Fuad HA, Winarni NL, Dwiyahreni AA, Farid M, Sri Mariati, Margules C, Prakoso B, Zakaria Z (2020) Deforestation on the Indonesian island of Sulawesi and the loss of primate habitat. Glob Ecol Conserv 24:e01205
Troisi A (2002) Displacement activities as a behavioral measure of stress in nonhuman primates and human subjects. Stress 5:47–54
Troisi A, Schino G, D’Antoni M, Pandolfi N, Aureli F, D’Amato FR (1991) Scratching as a behavioral index of anxiety in macaque mothers. Behav Neural Biol 56(3):307–313
Tutin CEG, Fernandez M (1991) Responses of wild chimpanzees and gorillas to the arrival of primatologists: behaviour observed during habituation. In: Box HO (ed) Primate responses to environmental change. Springer, Dordrecht
Tyrrell M, Berman CM, Duboscq J, Agil M, Sutrisno T (2020) Avoidant social style among wild crested macaque males (Macaca nigra) in Tangkoko Nature Reserve, Sulawesi, Indonesia. Behaviour 157(5):451–491
Ulyan MJ, Burrows AE, Buzzell CA, Raghanti MA, Marcinkiewicz JL, Phillips KA (2006) The effects of predictable and unpredictable feeding schedules on the behavior and physiology of captive brown capuchins (Cebus apella). Appl Anim Behav Sci 101(1–2):154–160
Ventura R, Majolo B, Schino G, Hardie S (2005) Differential effects of ambient temperature and humidity on allogrooming, self-grooming, and scratching in wild Japanese macaques. Am J Phys Anthropol 126:453–457
Weingrill T, Gray DA, Barrett L, Henzi SP (2003) Fecal cortisol levels in free-ranging female chacmas baboons: relationship to dominance, reproductive state and environmental factors. Horm Behav 45:259–269
Whitehouse J, Micheletta J, Waller B (2017) Stress behaviours buffer macaques from aggression. Sci Rep 7:11083
Williamson E, Feistner A (2011) Habituating primates: processes, techniques, variables and ethics. In: Setchell J, Curtis D (eds) Field and laboratory methods in primatology: a practical guide. Cambridge University Press, Cambridge, pp 33–50
Wittig RM, Crockford C, Lehmann J, Whitten PL, Seyfarth RM, Cheney DL (2008) Focused grooming networks and stress alleviation in wild female baboons. Horm Behav 54(1):170–177
Woods JM, Ross SR, Cronin KA (2019) The social rank of zoo-housed Japanese Macaques is a predictor of visitor-directed aggression. Animals 9:316
Yamagiwa J (2011) Ecological anthropology and primatology: fieldwork practices and mutual benefits. In: MacClancey J, Fuentes A (eds) Centralizing fieldwork: critical perspectives from primatology, biological and social anthropology. Berghahn Books, pp 84–103
Acknowledgements
We gratefully acknowledge all the guides, rangers, and people who work within and in connection with Tangkoko, specifically the Indonesian Government, Balai Konservasi Sumber Daya Alam (Conservation of Natural Resources in North Sulawesi), Kementerian Riset dan Teknologi (Indonesian Ministry of Research and Technology), Direktorat Jenderal Konservasi Sumber Daya Alam dan Ekosistem (Indonesian Directorate General of Nature Resources and Ecosystem Conservation), The American Indonesian Exchange Foundation, Macaca Nigra Project Team, Selamatkan Yaki, Tasikoki, and Tangkoko Conservation Education. D. Bertrand would personally like to thank her Anthropogenic Stress team, without whom, none of this data collection at Tangkoko would have been possible: Uni Suiah, Yuliana Sheza, Nur Aoliya, Mary Zuromskis, Kayla Wood, Rachel Sinsheimer. And she would also like to thank Dr. Lisa Danish and Dr. Jennifer Marciniak. A very special thank you goes to all of our funders: The National Science Foundation, Fulbright, Rufford Foundation, Chester Zoo, Nacey Maggioncalda Foundation, Primate Conservation Inc., University at Buffalo Anthropology Department, Nila T. Gnamm Research Fund, and the Mark Diamond Research Fund.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Bertrand, D.A., Berman, C.M., Agil, M., Sutiah, U., Engelhardt, A. (2022). Rethinking Tolerance to Tourism: Behavioral Responses by Wild Crested Macaques (Macaca nigra) to Tourists. In: Gursky, S.L., Supriatna, J., Achorn, A. (eds) Ecotourism and Indonesia's Primates. Developments in Primatology: Progress and Prospects. Springer, Cham. https://doi.org/10.1007/978-3-031-14919-1_4
Download citation
DOI: https://doi.org/10.1007/978-3-031-14919-1_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-14918-4
Online ISBN: 978-3-031-14919-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)