Skip to main content Accessibility help
×
Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-22T10:44:45.777Z Has data issue: false hasContentIssue false

22 - Ethical Considerations in Conducting Primate Cognition Research

Published online by Cambridge University Press:  28 July 2022

Bennett L. Schwartz
Affiliation:
Florida International University
Michael J. Beran
Affiliation:
Georgia State University
Get access

Summary

As the breadth and scope of primate cognition research continues to evolve, it remains essential that the ethical considerations of such work do so as well. The evaluation of ethics is shaped by time and place and centers on a variety of factors, including the questions being asked, the methods used, the setting, and the species studied. Here, we take a pragmatic approach in examining ethical considerations as they relate to cognitive research with primates in both captive and wild settings. We encourage primatologists to consider how primates’ lives are impacted prior to, during, and following the research. In addition, we highlight the importance of considering how such research activities interface with the people who work or live alongside the primates. Thus, we aim to help guide those studying and working with primates to plan and conduct ethically sound research.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahuja, N. (2013). Macaques and biomedicine: Notes on decolonization, Polio, and changing representations of Indian rhesus in the United States, 1930–1960. In Radhakrishna, S., Huffman, M. A., & Sinha, A. (Eds.), The macaque connection (pp. 7191). Springer-Verlag.Google Scholar
Allan, A. T., Bailey, A. L., & Hill, R. A. (2020). Habituation is not neutral or equal: Individual differences in tolerance suggest an overlooked personality trait. Science Advances, 6, eaaz0870.CrossRefGoogle ScholarPubMed
Ando, C., Iwata, Y., & Yamagiwa, J. (2008). Progress of habituation of western lowland gorillas and their reaction to observers in Moukalaba-Doudou National Park, Gabon. African Study Monographs, 39, 5569.Google Scholar
Arluke, A., Sanders, C. (1996). Systems of meaning in primate labs. In Arluke, A. & Sanders, C. (Eds.), Regarding animals (pp. 107131). Temple University Press.Google Scholar
Asquith, P. J. (1989). Provisioning and the study of free-ranging primates: History, effects, and prospects. American Journal of Physical Anthropology, 32, 129158.Google Scholar
AVMA (American Veterinary Medical Association). (2020) Guidelines for the euthanasia of animals: 2020 edition. Retrieved November 24, 2020 from www.avma.org/sites/default/files/2020-01/2020-Euthanasia-Final-1-17-20.pdfGoogle Scholar
Bard, K. A., & Gardner, K. H. (1996). Influences on development in infant chimpanzees: Enculturation, temperament, and cognition. In Russon, A., Bard, K., & Parker, S. T. (Eds.), Reaching into thought: The minds of the great apes (pp. 235256). Cambridge University Press.Google Scholar
Barrett, B. J., Monteza-Moreno, C. M., Dogandžić, T., Zwyns, N., Ibáñez, A., & Crofoot, M. C. (2018). Habitual stone-tool-aided extractive foraging in white-faced capuchins, Cebus capucinus. Royal Society Open Science, 5, 181002.Google Scholar
Bayne, K. (2002). Development of the human–research animal bond and its impact on animal well-being. ILAR Journal, 43, 49.CrossRefGoogle ScholarPubMed
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. Marine Ecology Progress Series, 395, 177185.CrossRefGoogle Scholar
Berger, J. (1980). Why look at animals? In Berger, J. (Ed.), About looking (pp. 328). Random House.Google Scholar
Bermejo, M., Rodríguez-Teijeiro, J. D., Illera, G., Barroso, A., Vilà, C., & Walsh, P. D. (2006). Ebola outbreak killed 5000 gorillas. Science, 314, 15641564.CrossRefGoogle ScholarPubMed
Bethell, E. J., Holmes, A., MacLarnon, A., & Semple, S. (2012). Cognitive bias in a non-human primate: Husbandry procedures influence cognitive indicators of psychological well-being in captive rhesus macaques. Animal Welfare, 21, 185195.CrossRefGoogle Scholar
Bezanson, M., & McNamara, A. (2019). The what and where of primate field research may be failing primate conservation. Evolutionary Anthropology: Issues, News, and Reviews, 28, 166178.Google Scholar
Bezerra, B. M., Bastos, M., Souto, A., Keasey, M. P., Eason, P., Schiel, N., & Jones, G. (2014). Camera trap observations of nonhabituated critically endangered wild blonde capuchins, Sapajus flavius (formerly Cebus flavius). International Journal of Primatology, 35, 895907.Google Scholar
Blair, M. E. (2019). Toward more equitable and inclusive spaces for primatology and primate conservation. International Journal of Primatology, 40, 462464.CrossRefGoogle Scholar
Bliss-Moreau, E., Theil, J. H., & Moadab, G. (2013). Efficient cooperative restraint training with rhesus macaques. Journal of Applied Animal Welfare Science, 16, 98117.CrossRefGoogle ScholarPubMed
Bloomsmith, M. A., Lambeth, S. P., Stone, A. M., & Laule, G. E. (1997). Comparing two types of human interaction as enrichment for chimpanzees. American Journal of Primatology, 42, 96.Google Scholar
Bloomsmith, M. A., Perlman, J. E., Hutchinson, E., & Sharpless, M. (2018). Behavioral management programs to promote laboratory animal welfare. In Management of animal care and use programs in research, education, and testing. CRC Press/Taylor & Francis.Google Scholar
Boesch, C., Kalan, A. K., Mundry, R., Arandjelovic, M., Pika, S., Dieguez, P., … & Eno-Nku, M. (2020). Chimpanzee ethnography reveals unexpected cultural diversity. Nature Human Behaviour, 4, 910916.Google Scholar
Boyer-Ontl, K. M., & Pruetz, J. D. (2014). Giving the forest eyes: The benefits of using camera traps to study unhabituated chimpanzees (Pan troglodytes verus) in southeastern Senegal. International Journal of Primatology, 35, 881894.Google Scholar
Brando, S., & Buchanan-Smith, H. M. (2018). The 24/7 approach to promoting optimal welfare for captive wild animals. Behavioural Processes 156, 8395.Google Scholar
Brent, L. (2004). Solutions for research chimpanzees. Lab Animal, 33, 3743.Google Scholar
Broom, D. M., & Johnson, K. G. (2019). Stress and animal welfare: Key issues in the biology of humans and other animals (second edition). Springer Nature.Google Scholar
Brosnan, S. F., & de Waal, F. B. M. (2003). Monkeys reject unequal pay. Nature, 425, 297299.CrossRefGoogle ScholarPubMed
Brosnan, S. F., Hopper, L. M., Richey, S., Freeman, H. D., Talbot, C. F., Gosling, S., Lambeth, S. P., & Schapiro, S. J. (2015). Personality influences responses to inequity and contrast in chimpanzees. Animal Behaviour, 101, 7587.CrossRefGoogle ScholarPubMed
Brosnan, S. F., Parris, A., Beran, M. J., Flemming, T., Heimbauer, L., Talbot, C. F., Lambeth, S. P., Schapiro, S. J., & Wilson, B. J. (2011). Responses to the Assurance game in monkeys, apes, and humans using equivalent procedures. Proceedings of the National Academy of Sciences, 108, 34423447.Google Scholar
Bshary, R. (2001). Diana monkeys, Cercopithecus diana, adjust their anti-predator response behaviour to human hunting strategies. Behavioral Ecology and Sociobiology, 50, 251256.CrossRefGoogle Scholar
Calapai, A., Berger, M., Niessing, M., Heisig, K., Brockhausen, R., Treue, S., & Gail, A. (2017). A cage-based training, cognitive testing and enrichment system optimized for rhesus macaques in neuroscience research. Behavior Research Methods, 49, 3545.Google Scholar
Carter, A. J., Marshall, H. H., Heinsohn, R., & Cowlishaw, G. (2014). Personality predicts the propensity for social learning in a wild primate. PeerJ, 2, e283.CrossRefGoogle Scholar
Cassidy, L. C., Hannibal, D. L., Semple, S., & McCowan, B. (2020). Improved behavioral indices of welfare in continuous compared to intermittent pair-housing in adult female rhesus macaques (Macaca mulatta). American Journal of Primatology, 82, e23189.CrossRefGoogle ScholarPubMed
CCAC (1998). CCAC guidelines on choosing an appropriate endpoint in experiments using animals for research, teaching, and testing. Retrieved November 24, 2020 from www.ccac.ca/Documents/Standards/Guidelines/Appropriate_endpoint.pdfGoogle Scholar
CFR 21 §58 (2020). Good laboratory practice for nonclinical laboratory studies.Google Scholar
Chauhan, A., & Pirta, R. S. (2010). Agonistic interactions between humans and two species of monkeys (rhesus monkey Macaca mulatta and hanuman langur Semnopithecus entellus) in Shimla, Himachal Pradesh. Journal of Psychology, 1, 914.Google Scholar
Chelluri, G. I., Ross, S. R., & Wagner, K. E. (2013). Behavioral correlates and welfare implications of informal interactions between caretakers and zoo-housed chimpanzees and gorillas. Applied Animal Behaviour Science, 147, 306315.CrossRefGoogle Scholar
Cheney, D. L., & Seyfarth, R. M. (1982). How vervet monkeys perceive their grunts: Field playback experiments. Animal Behaviour, 30, 739751.Google Scholar
Cheyne, S. M., Neale, C. J., Thompson, C., Wilcox, C. H., Smith, Y. C. E., & Smith, D. A. E. (2018). Down from the treetops: Red langur (Presbytis rubicunda) terrestrial behavior. Primates, 59, 437448.CrossRefGoogle ScholarPubMed
Clark, F. E. (2011). Great ape cognition and captive care: Can cognitive challenges enhance well-being? Applied Animal Behaviour Science, 135, 112.Google Scholar
Clarke, E., Reichard, U. H., & Zuberbühler, K. (2012). The anti-predator behaviour of wild white-handed gibbons (Hylobates lar). Behavioral Ecology and Sociobiology, 66, 8596.CrossRefGoogle Scholar
Croes, B. M., Laurance, W. F., Lahm, S. A., Tchignoumba, L., Alonso, A., Lee, M. E., … & Buij, R. (2007). The influence of hunting on antipredator behavior in Central African monkeys and duikers. Biotropica, 39, 257263.Google Scholar
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. Animal Behaviour, 80, 475480.CrossRefGoogle Scholar
Crofts, H. S., Muggleton, N. G., Bowditch, A. P., Pearce, P. C., Nutt, D. J., & Scott, E. A. M. (1999). Home cage presentation of complex discrimination tasks to marmosets and rhesus monkeys. Laboratory Animals, 33, 207214.Google Scholar
Cronin, K. A. (2016). Unnatural paradigm calls into question whether macaques’ social decisions represent empathy. Proceedings of the National Academy of Sciences, 113, E1331.CrossRefGoogle ScholarPubMed
Cronin, K. A., Jacobson, S. L., Bonnie, K. E., & Hopper, L. M. (2017). Studying primate cognition in a social setting to improve validity and welfare: A literature review highlighting successful approaches. PeerJ, 5, e3649.Google Scholar
Cunningham, E. P., Unwin, S., & Setchell, J. M. (2015). Darting primates in the field: A review of reporting trends and a survey of practices and their effect on the primates involved. International Journal of Primatology, 36, 911932.Google Scholar
Cuthill, I. (1991). Field experiments in animal behaviour: Methods and ethics. Animal Behaviour, 42, 10071014.Google Scholar
Damerius, L. A., Forss, S. I., Kosonen, Z. K., Willems, E. P., Burkart, J. M., Call, J., … & Van Schaik, C. P. (2017). Orientation toward humans predicts cognitive performance in orangutans. Scientific Reports, 7, 112.Google Scholar
Das, S., & Lowe, M. (2018). Nature read in black and white: Decolonial approaches to interpreting natural history collections. Journal of Natural Science Collections, 6, 414.Google Scholar
Davenport, R. K., Rogers, C. M., & Rumbaugh, D. M. (1973). Long-term cognitive deficits in chimpanzees associated with early impoverished rearing. Developmental Psychology, 9, 343347.Google Scholar
de Azevedo Fernandes, N. C. C., Cunha, M. S., Guerra, J. M., Réssio, R. A., dos Santos Cirqueira, C., Iglezias, S. D. A., … & Díaz-Delgado, J. (2017). Outbreak of yellow fever among nonhuman primates, Espirito Santo, Brazil, 2017. Emerging Infectious Diseases, 23, 20382041.CrossRefGoogle Scholar
Dettmer, A. M., Heckman, J. J., Pantano, J., Ronda, V., & Suomi, S. J. (2020). Intergenerational effects of early-life advantage: Lessons from a primate study (No. w27737). National Bureau of Economic Research.Google Scholar
Dollins, F. L. (1999). A look back in the mirror: Perspectives on animals and ethics. In Dollins, F. L. (Ed.), Attitudes to animals: Views in animal welfare (pp. 311). Cambridge University Press.CrossRefGoogle Scholar
Duarte, M. H. L., Kaizer, M. C., Young, R. J., Rodrigues, M., & Sousa-Lima, R. S. (2018). Mining noise affects loud call structures and emission patterns of wild black-fronted titi monkeys. Primates, 59, 8997.Google Scholar
Dunay, E., Apakupakul, K., Leard, S., Palmer, J. L., & Deem, S. L. (2018). Pathogen transmission from humans to great apes is a growing threat to primate conservation. EcoHealth, 15, 148162.CrossRefGoogle ScholarPubMed
Dunbar, R. I. (1998). The social brain hypothesis. Evolutionary Anthropology: Issues, News, and Reviews, 6, 178190.Google Scholar
Egelkamp, C. L., & Ross, S. R. (2019). A review of zoo-based cognitive research using touchscreen interfaces. Zoo Biology, 38, 220235.Google Scholar
Estienne, V., Stephens, C., & Boesch, C. (2017). Extraction of honey from underground bee nests by central African chimpanzees (Pan troglodytes troglodytes) in Loango National Park, Gabon: Techniques and individual differences. American Journal of Primatology, 79, e22672.Google Scholar
Estrada, A., Garber, P. A., & Chaudhary, A. (2019). Expanding global commodities trade and consumption place the world’s primates at risk of extinction. PeerJ, 7, e7068.Google Scholar
Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., Di Fiore, A., … & Rovero, F. (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances, 3, e1600946.Google Scholar
Fagot, J., Gullstrand, J., Kemp, C., Defilles, C., & Mekaouche, M. (2014). Effects of freely accessible computerized test systems on the spontaneous behaviors and stress level of Guinea baboons (Papio papio). American Journal of Primatology, 76, 5664.CrossRefGoogle ScholarPubMed
Fagot, J., & Paleressompoulle, D. (2009). Automatic testing of cognitive performance in baboons maintained in social groups. Behavior Research Methods, 41(2), 396404.Google Scholar
Fedigan, L. M. (2010). Ethical issues faced by field primatologists: Asking the relevant questions. American Journal of Primatology, 72, 754771.Google Scholar
Fennell, D. A. (2008). Ecotourism and the myth of indigenous stewardship. Journal of Sustainable Tourism, 16(2), 129149.Google Scholar
Fernandez-Duque, E., & Rotundo, M. (2003). Field methods for capturing and marking Azarai night monkeys. International Journal of Primatology, 24, 11131120.Google Scholar
Fischer, J., Noser, R., & Hammerschmidt, K. (2013). Bioacoustic field research: A primer to acoustic analyses and playback experiments with primates. American Journal of Primatology, 75, 643663.Google Scholar
Fleury, E. (2017). Money for monkeys, and more: Ensuring sanctuary retirement of nonhuman primates. Animal Studies Journal, 6, 3054.Google Scholar
Forss, S., Motes-Rodrigo, A., Hrubesch, C., & Tennie, C. (2020). Chimpanzees’ (Pan troglodytes) problem-solving skills are influenced by housing facilities and captive care duration. PeerJ, 8, e10263.Google Scholar
Fruteau, C., van Damme, E., & Noë, R. (2013). Vervet monkeys solve a multiplayer “Forbidden Circle Game” by queuing to learn restraint. Current Biology, 23, 665670Google Scholar
Fuentes, A. (2004). Is monkey business a valid enterprise? The political ecology of macaque “ecotourism.” Folia Primatologica, 75, 4344.Google Scholar
Gazes, R. P., Brown, E. K., Basile, B. M., & Hampton, R. R. (2013). Automated cognitive testing of monkeys in social groups yields results comparable to individual laboratory-based testing. Animal Cognition, 16, 445458.Google Scholar
Gazes, R. P., Lutz, M. C., Meyer, M. J., Hassett, T. C., & Hampton, R. R. (2019). Influences of demographic, seasonal, and social factors on automated touchscreen computer use by rhesus monkeys (Macaca mulatta) in a large naturalistic group. PLoS ONE, 14, e0215060.Google Scholar
Gewin, V. (2021). Respect and representation. Nature, 589, 315317.Google Scholar
Gilardi, K. V., Gillespie, T. R., Leendertz, F. H., Macfie, E. J., Travis, D. A., Whittier, C. A., & Williamson, E. A. (2015). Best practice guidelines for health monitoring and disease control in great ape populations. Occasional Papers of the IUCN Species Survival Commission, 56.Google Scholar
Glander, K. E. (2013). Darting, anesthesia, and handling. In Sterling, E. J., Bynum, N., & Blair, M. E. (Eds.), Primate ecology and conservation: A handbook of techniques (pp. 2739). Oxford University Press.CrossRefGoogle Scholar
Goldsmith, M. (2005). Habituating primates for field study: Ethical considerations for African great apes. In Turner, T. R. (Ed.), Biological anthropology and ethics: From repatriation to genetic identity (pp. 4964). State University of New York Press Press.Google Scholar
Gonçalves, A., & Carvalho, S. (2019). Death among primates: A critical review of non-human primate interactions towards their dead and dying. Biological Reviews, 94, 15021529.Google Scholar
Goodall, J. (1971). In the shadow of man. Houghton Mifflin Harcourt.Google Scholar
Graham, M. (2017). Positive reinforcement training and research. In Schapiro, S. J. (Ed.), Handbook of primate behavioral management. (pp. 187200). CRC Press.Google Scholar
Green, V. M., & Gabriel, K. I. (2020). Researchers’ ethical concerns regarding habituating wild-nonhuman primates and perceived ethical duties to their subjects: Results of an online survey. American Journal of Primatology, 82, e23178.CrossRefGoogle ScholarPubMed
Greer, D., Maisels, F., Morgan, D., Sanz, C., & Williamson, E. A. (2013). Great apes and FSC: implementing “ape friendly” practices in Central African’s logging concessions. Occasional Paper of the IUCN Species Survival Commission.Google Scholar
Griffin, G. A., & Harlow, H. F. (1966). Effects of three months of total social deprivation on social adjustment and learning in the rhesus monkey. Child Development, 37, 533547.Google Scholar
Griggs, D. J., Bloch, J., Chavan, S., Coubrough, K. M., Conley, W., Morrisroe, K., & Yazdan-Shahmorad, A. (2020). Autonomous cage-side system for remote training of non-human primates. Journal of Neuroscience Methods, 108969.Google Scholar
Gruber, T., Muller, M. N., Strimling, P., Wrangham, R., & Zuberbühler, K. (2009). Wild chimpanzees rely on cultural knowledge to solve an experimental honey acquisition task. Current Biology, 19, 18061810.Google Scholar
Gruen, L., Fultz, A., & Pruetz, J. (2013). Ethical issues in African great ape field studies. ILAR Journal, 54, 2432.Google Scholar
Gunhold, T., Whiten, A., & Bugnyar, T. (2014). Video demonstrations seed alternative problem-solving techniques in wild common marmosets. Biology Letters, 10, 20140439.Google Scholar
Hansen, B. K., Hopper, L. M., Fultz, A. L., & Ross, S. R. (2020). Understanding the behavior of sanctuary-housed chimpanzees during public programs. Anthrozoös, 33, 481495.Google Scholar
Hanson, K. T., & Riley, E. P. (2017). Beyond neutrality: The human–primate interface during the habituation process. International Journal of Primatology, 39, 852877.Google Scholar
Haraway, D. (1989). Primate visions: Gender, race, and nature in the world of modern science. Routledge.Google Scholar
Hartel, J. A., Otali, E., Machanda, Z., Wrangham, R. W., & Ross, E. (2020). Holistic approach for conservation of chimpanzees in Kibale National Park, Uganda. In Hopper, L. M. & Ross, S. R. (Eds.), Chimpanzees in context: A comparative perspective on chimpanzee behavior, cognition, conservation, and welfare. (pp. 612643). The University of Chicago Press.Google Scholar
Hau, J. (1999). Humane endpoints and the importance of training. In Hendriksen, C. F. M. & Morton, D. B. (Eds.), Humane endpoints in animal experiments for biomedical research (pp. 7174). Royal Society of Medicine Press.Google Scholar
Herrelko, E., Vick, S. J., & Buchanan-Smith, H. M. (2012). Cognitive research in zoo-housed chimpanzees: Influence of personality and impact on welfare. American Journal of Primatology, 74, 828840.Google Scholar
Hill, C. M. (2002). Primate conservation and local communities – Ethical issues and debates. American Anthropologist, 104, 11841194.Google Scholar
Hirata, S., Morimura, K., Watanuki, K., & Ross, S. R. (2020). The establishment of sanctuaries for former laboratory chimpanzees: Challenges, successes, and cross-cultural context. In Hopper, L. M. & Ross, S. R. (Eds.), Chimpanzees in context: A comparative perspective on chimpanzee behavior, cognition, conservation, and welfare (pp. 208232). The University of Chicago Press.CrossRefGoogle Scholar
Hopper, L. M., Fernandez-Duque, E., & Williams, L. E. (2019). Testing the weekend effect hypothesis: Time of day and lunar phase better predict the timing of births in laboratory-housed primates than day of week. American Journal of Primatology, 81, e23026.Google Scholar
Hopper, L. M., Gulli, R. A., Howard, L. H., Kano, F., Krupenye, C., Ryan, A. M., & Paukner, A. (2021). The application of non-invasive, restraint-free eye-tracking methods for use with nonhuman primates. Behavior Research Methods, 53, 10031030.Google Scholar
Hopper, L. M., Shender, M. A., & Ross, S. R. (2016). Behavioral research as physical enrichment for captive chimpanzees. Zoo Biology, 35, 293297.Google Scholar
Huskisson, S. M., Ross, S. R., & Hopper, L. M. (2021). Do zoo visitors induce attentional bias effects in primates completing cognitive tasks? Animal Cognition, 24, 645653.Google Scholar
Hvenegaard, G. T. (2014). Economic aspects of primate-focused tourism associated with primate conservation. In Russon, A. E. & Wallis, J. (Eds.), Primate tourism: A tool for conservation? (pp. 259277). Cambridge University Press.Google Scholar
Jack, K. M., Lenz, B. B., Healan, E., Rudman, S., Schoof, V. A., & Fedigan, L. (2008). The effects of observer presence on the behavior of Cebus capucinus in Costa Rica. American Journal of Primatology, 70, 490494.Google Scholar
Jacobson, S. L., Freeman, H. D., Santymire, R. M., & Ross, S. R. (2017). Atypical experiences of captive chimpanzees (Pan troglodytes) are associated with higher hair cortisol concentrations as adults. Royal Society Open Science, 4, 170932.Google Scholar
Jacobson, S. L., Kwiatt, A. C., Ross, S. R., & Cronin, K. A. (2019). The effects of cognitive testing on the welfare of zoo-housed Japanese macaques (Macaca fuscata). Applied Animal Behaviour Science, 212, 9097.Google Scholar
Joly, M., Scheumann, M., & Zimmermann, E. (2008). Wild mouse lemurs revisit artificial feeding platforms: Implications for field experiments on sensory and cognitive abilities in small primates. American Journal of Primatology, 70, 892896.Google Scholar
Junker, J., Petrovan, S. O., Arroyo-RodrÍguez, V., Boonratana, R., Byler, D., Chapman, C. A., … & Cowlishaw, G. (2020). A severe lack of evidence limits effective conservation of the world’s primates. BioScience, 70, 794803.Google Scholar
Kaisin, O., Fuzessy, L., Poncin, P., Brotcorne, F., & Culot, L. (2021). Meta-analysis of anthropogenic impacts on physiological stress in wild primates. Conservation Biology, 35, 101114.Google Scholar
Kawai, M. (1965). Newly acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima islet. Primates, 6, 130.Google Scholar
Kempes, M. M., Gulickx, M. M. C., van Daalen, H. J. C., Louwerse, A. L., & Sterck, E. H. M. (2008). Social competence is reduced in socially deprived rhesus monkeys (Macaca mulatta). Journal of Comparative Psychology, 122, 6267.Google Scholar
Kerwin, A. M. (2006). Overcoming the barriers to the retirement of Old and New World monkeys from research facilities. Journal of Applied Animal Welfare Science, 9, 337347.Google Scholar
Kim-McCormack, N. N., Smith, C. L., & Behie, A. M. (2016). Is interactive technology a relevant and effective enrichment for captive great apes? Applied Animal Behaviour Science, 185, 18.Google Scholar
Kühl, H. S., Boesch, C., Kulik, L., Haas, F., Arandjelovic, M., Dieguez, P., … & Ayimisin, E. A. (2019). Human impact erodes chimpanzee behavioral diversity. Science, 363, 14531455.Google Scholar
Lambeth, S. P., Bloomsmith, M. A., & Alford, P. L. (1997). Effects of human activity on chimpanzee wounding. Zoo Biology, 16, 327333.Google Scholar
Lankau, E. W., Turner, P. V., Mullan, R. J., & Galland, G. G. (2014). Worker health and safety practices in research facilities using nonhuman primates, North America. Emerging Infectious Diseases, 20, 1589.Google Scholar
Lappan, S., Malaivijitnond, S., Radhakrishna, S., Riley, E. P., & Ruppert, N. (2020). The human–primate interface in the New Normal: Challenges and opportunities for primatologists in the COVID-19 era and beyond. American Journal of Primatology, 82, e23176.Google Scholar
Laule, G. E., Bloomsmith, M. A., & Schapiro, S. J. (2003). The use of positive reinforcement training techniques to enhance the care, management, and welfare of primates in the laboratory. Journal of Applied Animal Welfare Science, 6, 163173.Google Scholar
Lee, D. N. (2020) Diversity and inclusion activism in animal behaviour and the ABS: A historical view from the U.S.A. Animal Behaviour, 164, 273280.CrossRefGoogle Scholar
Luncz, L. V., Falótico, T., Pascual-Garrido, A., Corat, C., Mosley, H., & Haslam, M. (2016). Wild capuchin monkeys adjust stone tools according to changing nut properties. Scientific Reports, 6, 33089.Google Scholar
Lutz, C., Well, A., & Novak, M. (2003). Stereotypic and self-injurious behavior in rhesus macaques: A survey and retrospective analysis of environment and early experience. American Journal of Primatology, 60, 115.Google Scholar
Macfie, E. J., & Williamson, E. A. (2010). Best practice guidelines for great ape tourism. IUCN/SSC Primate Specialist Group (PSG). https://portals.iucn.org/library/sites/library/files/documents/SSC-OP-038.pdfGoogle Scholar
MacKinnon, K. C., & Riley, E. P. (2010). Field primatology of today: Current ethical issues. American Journal of Primatology, 72, 749753.Google Scholar
MacKinnon, K. C., & Riley, E. P. (2013). Contemporary ethical issues in field primatology. In MacClancy, J., & Fuentes, A. (Eds.), Ethics in the field: Contemporary challenges (pp. 98107). Berghahn Books.Google Scholar
Maestripieri, D. (2005). Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proceedings of the National Academy of Sciences USA, 102, 97269729.Google Scholar
Marty, P. R., Beisner, B., Kaburu, S. S., Balasubramaniam, K., Bliss-Moreau, E., Ruppert, N., … & McCowan, B. (2019). Time constraints imposed by anthropogenic environments alter social behaviour in longtailed macaques. Animal Behaviour, 150, 157165.Google Scholar
Mason, S., Premereur, E., Pelekanos, V., Emberton, A., Honess, P., & Mitchell, A. S. (2019). Effective chair training methods for neuroscience research involving rhesus macaques (Macaca mulatta). Journal of Neuroscience Methods, 317, 8293.Google Scholar
Matsuzawa, T. (2016). Euthanasia is not an option: 10 years’ care of a chimpanzee with acute tetraparesis. Primates, 57, 291293.Google Scholar
McAndrew, R., & Helms Tillery, S. I. (2016). Laboratory primates: Their lives in and after research. Temperature, 3, 502508.CrossRefGoogle ScholarPubMed
McKinley, J. (2004). Training in a laboratory environment: Methods, effectiveness and welfare implications for two species of primate. Doctoral thesis, University of Stirling. http://hdl.handle.net/1893/23412Google Scholar
Morgan, D., Strindberg, S., Winston, W., Stephens, C. R., Traub, C., Ayina, C. E., Ndolo Ebika, S. T., Mayoukou, W., Koni, D., Iyenguet, F., & Sanz, C. M. (2019). Impacts of selective logging and associated anthropogenic disturbance on intact forest landscapes and apes of northern Congo. Frontiers in Forests and Global Change, 2, 113.Google Scholar
Muehlenbein, M. P., & Ancrenaz, M. (2009). Minimizing pathogen transmission at primate ecotourism destinations: The need for input from travel medicine. Journal of Travel Medicine, 16, 229232.Google Scholar
Murphy, H. W., Miller, M, Ramer, J., Travis, D., Barbiers, R., Wolfe, N. D., & Switzer, W. M. (2006). Implications of simian retroviruses for captive primate population management and the occupational safely of primate handlers. Journal of Zoo and Wildlife Medicine, 37, 219233.Google Scholar
Narat, V., Pennec, F., Simmen, B., Ngawolo, J. C. B., & Krief, S. (2015). Bonobo habituation in a forest-savanna mosaic habitat: Influence of ape species, habitat type, and sociocultural context. Primates, 56, 339349.Google Scholar
Nash, L. T. (2005). Studies of primates in the field and in captivity: similarities and differences in ethical concerns. In Turner, T. R. (Ed.), Biological anthropology and ethics: From repatriation to genetic identity (pp. 2748). State University of New York Press Press.Google Scholar
NIH (2019). Guidelines for endpoints in animal study proposals. Retrieved November 24, 2020 from: https://oacu.oir.nih.gov/sites/default/files/uploads/arac-guidelines/b13_endpoints_guidelines.pdfGoogle Scholar
Non Human Primate COVID-19 Information Hub (2020). Information. Retrieved November 19, 2020 from: https://umnadvet.instructure.com/courses/324Google Scholar
Noon, C. (1999). Chimpanzees and retirement. Journal of Applied Animal Welfare Science, 2, 141146.Google Scholar
NRC (1997). National Research Council (US) Committee on Long-Term Care of Chimpanzees. Chimpanzees in Research: Strategies for their ethical care, management, and use. National Academies Press (US). Retrieved November 24, 2020 from www.ncbi.nlm.nih.gov/books/NBK109756/Google Scholar
Parreñas, J. S. (2018). Decolonising extinction: The work of care in orangutan rehabilitation. Duke University Press.Google Scholar
Pebsworth, P. A., & LaFleur, M. (2014). Advancing primate research and conservation through the use of camera traps: Introduction to the special issue. International Journal of Primatology, 35, 825840.Google Scholar
Pelé, M., Georges, J., Matsuzawa, T., & Sueur, C. (2021). Perceptions of human–animal relationships and their impacts on animal ethics, law and research. Frontiers in Psychology, 11, 631238.Google Scholar
Perdue, B. M., Evans, T. A., Washburn, D. A., Rumbaugh, D. M., & Beran, M. J. (2014). Do monkeys choose to choose? Learning & Behavior, 42, 164175.CrossRefGoogle ScholarPubMed
Perlman, J. E., Horner, V., Bloomsmith, M. A., Lambeth, S. P., Schapiro, S. J., (2010). Positive reinforcement training, social learning and chimpanzee welfare. In Lonsdorf, E. V., Ross, S. R., & Matsuzawa, T. (Eds.), The mind of the chimpanzee: Ecological and experimental perspectives (pp. 320331). The University of Chicago Press.Google Scholar
Poole, T. B. (1988). Behaviour, housing and welfare of non-human primates. In Beynen, A., & Solleveld, H. A. (Eds.), New developments in biosciences: Their implications for laboratory animal science (pp. 231237). Springer.Google Scholar
Prescott, M. J. (2010). Ethics of primate use. Advances in Science and Research, 5, 1120.Google Scholar
Prescott, M. J. (2020). Ethical and welfare implications of genetically altered non-human primates for biomedical research. Journal of Applied Animal Ethics Research, 2, 151176.Google Scholar
Prescott, M. J., Brown, V. J., Flecknell, P. A., Gaffan, D., Garrod, K., Lemon, R. N., ... & Whitfield, L. (2010). Refinement of the use of food and fluid control as motivational tools for macaques used in behavioural neuroscience research: Report of a Working Group of the NC3Rs. Journal of Neuroscience Methods, 193(2), 167188.Google Scholar
Prescott, M. J., & Buchanan-Smith, H. M. (2003). Training nonhuman primates using positive reinforcement techniques. Journal of Applied Animal Welfare Science, 6, 157161.CrossRefGoogle ScholarPubMed
Prescott, M. J., & Lidster, K. (2017). Improving quality of science through better animal welfare: The NC3Rs strategy. Lab Animal 46, 152156.CrossRefGoogle ScholarPubMed
Priston, N. E., & McLennan, M. R. (2013). Managing humans, managing macaques: Human–macaque conflict in Asia and Africa. In Radhakrishna, S., Huffman, M. A., & Sinha, A. (Eds.), The macaque connection (pp. 225250). Springer.Google Scholar
Rasmussen, D. R. (1991). Observer influence on range use of Macaca arctoides after 14 years of observation? Laboratory Primate Newsletter, 30, 611.Google Scholar
Rasmussen, D. R. (1998). Changes in range use of Geoffroy’s tamarins (Saguinus geoffroyi) associated with habituation to observers. Folia Primatologica, 69, 153159.Google Scholar
Reid, M. J. (2020). Is 2020 the year when primatologists should cancel fieldwork? American Journal of Primatology, 82, e23161.Google Scholar
Rennie, A. E., & Buchanan-Smith, H. M. (2006). Refinement of the use of non-human primates in scientific research. Part I: The influence of humans. Animal Welfare, 15, 203213.Google Scholar
Riedler, B., Millesi, E., & Pratje, P. H. (2010). Adaptation to forest life during the reintroduction process of immature Pongo abelii. International Journal of Primatology, 31, 647663.Google Scholar
Riley, E. P., & Bezanson, M. (2018). Ethics of primate fieldwork: Toward an ethically engaged primatology. Annual Review of Anthropology, 47, 493512.Google Scholar
Riley, E. P., MacKinnon, K. C., Fernandez-Duque, E., Setchell, J. M., & Garber, P. A. (2014). Code of best practices for field primatology. Resource document International Primatoloplogical Society, American Society of Primatologists. www.asp.org/resources/docs/Code%20of_Best_Practices%20Oct%202014.pdfGoogle Scholar
Robins, J. G., Husson, S., Fahroni, A., Singleton, I., Nowak, M. G., Fluch, G., … & Hicks, N. (2019). Implanted radio telemetry in orangutan reintroduction and post-release monitoring and its application in other ape species. Frontiers in Veterinary Science, 6, 111.Google Scholar
Rodrigues, M. A. (2020). Neocolonial narratives of primate conservation 25th May 2020. IUCN Primate Specialist Group Section for Human Primate Interactions. Retrieved November 24, 2020 from: https://human-primate-interactions.org/blog/Google Scholar
Ross, S. R. (2010). How cognitive studies help shape our obligation for ethical care of chimpanzees. In Lonsdorf, E. V., Ross, S. R., & Matsuzawa, T. (Eds.), The mind of the chimpanzee: Ecological and experimental perspectives (pp. 309319). The University of Chicago Press.Google Scholar
Ross, S. R., & Leinwand, J. G. (2020). A review of research in primate sanctuaries. Biology Letters, 16, 20200033.Google Scholar
Rubis, J. M. (2020). The orang utan is not an indigenous name: Knowing and naming the maias as a decolonizing epistemology. Cultural Studies, 34, 811830.Google Scholar
Sabuhoro, E., Wright, B., Munanura, I. E., Nyakabwa, I. N., & Nibigira, C. (2017). The potential of ecotourism opportunities to generate support for mountain gorilla conservation among local communities neighboring Volcanoes National Park in Rwanda. Journal of Ecotourism, 20, 117.Google Scholar
Sánchez, M. M., Hearn, E. F., Do, D., Rilling, J. K., & Herndon, J. G. (1998). Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys. Brain Research, 812, 3849.Google Scholar
Sands, S. F., & Wright, A. A. (1982). Monkey and human pictorial memory scanning. Science, 216, 13331334.Google Scholar
Schapiro, S. J. (2000). A few new developments in primate housing and husbandry. Scandinavian Journal of Laboratory Animal Sciences, 27, 103110.Google Scholar
Schapiro, S. J., Neal Webb, S. J., Mulholland, M. M., & Lambeth, S. P. (2021). Behavioral management is a key component of ethical research. ILAR Journal, ilaa023.Google Scholar
Sengupta, A., McConkey, K. R., & Radhakrishna, S. (2015). Primates, provisioning and plants: Impacts of human cultural behaviours on primate ecological functions. PLoS ONE, 10, e0140961.Google Scholar
Setchell, J. (2019). Studying primates: How to design, conduct and report primatological research. Cambridge University Press.Google Scholar
Sha, J. C. H., Gumert, M. D., Lee, B. P. Y., Jones-Engel, L., Chan, S., & Fuentes, A. (2009). Macaque–human interactions and the societal perceptions of macaques in Singapore. American Journal of Primatology, 71, 825839.Google Scholar
Sherwen, S. L., & Hemsworth, P. H. (2019). The visitor effect on zoo animals: Implications and opportunities for zoo animal welfare. Animals, 9, 366.Google Scholar
Shutt, K., Heistermann, M., Kasim, A., Todd, A., Kalousova, B., Profosouva, I., … & Setchell, J. M. (2014). Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: Implications for conservation management. Biological Conservation, 172, 7279.Google Scholar
Sommer, V. (1993). Father-son recognition in Hanuman langurs (Presbytis entellus) – a field experiment in India. Primates, 34, 217–21.Google Scholar
Sommer, V., Adanu, J., Faucher, I., & Fowler, A. (2003). Nigerian chimpanzees (Pan troglodytes vellerosus) at Gashaka: Two years of habituation efforts. Folia Primatologica, 75(5), 295316.Google Scholar
Spenceley, A., Habyalimana, S., Tusabe, R., & Mariza, D. (2010). Benefits to the poor from gorilla tourism in Rwanda. Development Southern Africa, 27, 647662.Google Scholar
Strier, K. B. (2010). Long-term field studies: Positive impacts and unintended consequences. American Journal of Primatology, 72, 772778.Google Scholar
Sugiyama, Y. (2015). Influence of provisioning on primate behavior and primate studies. Mammalia, 79, 255265.Google Scholar
Tomasello, M., & Call, J. (2011). Methodological challenges in the study of primate cognition. Science, 334, 12271228.Google Scholar
Tulip, J., Zimmermann, J. B., Farningham, D., & Jackson, A. (2017). An automated system for positive reinforcement training of group-housed macaque monkeys at breeding and research facilities. Journal of Neuroscience Methods, 285, 618.Google Scholar
USDA (2019) Animal Welfare Act and Animal Welfare Regulations. Retrieved August 24, 2020 from: www.aphis.usda.gov/animal_welfare/downloads/AC_BlueBook_AWA_508_comp_version.pdfGoogle Scholar
van de Waal, E., & Bshary, R. (2010) Contact with human facilities appears to enhance technical skills in wild vervet monkeys (Chlorocebus aethiops). Folia Primatologica, 81, 282291.Google Scholar
Vermilyea, S. C., Babinski, A., Tran, N., To, S., Guthrie, S., Kluss, J. H., Schmidt, J. K., Wiepz, G. J., Meyer, M. G., Murphy, M. E., & Cookson, M. R. (2020). In vitro CRISPR/Cas9-directed gene editing to model LRRK2 G2019S Parkinson’s Disease in common marmosets. Scientific Reports, 10, 3447.Google Scholar
Vicente-Alonso, S., Sánchez-Sánchez, L., & Álvarez Solas, S. (2021). On the way to systematize habituation: A protocol to minimize the effects of observer presence on wild groups of Leontocebus lagonotus. Primates, 62(2), 407415.Google Scholar
Visalberghi, E., & Anderson, J. (2008). Fair game for chimpanzees. Science, 319, 282283.Google Scholar
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. Animal Cognition, 19, 343350.Google Scholar
Waitt, C., Buchanan-Smith, H. M., & Morris, K. (2002). The effects of caretaker–primate relationships on primates in the laboratory. Journal of Applied Animal Welfare Science, 5, 309319.Google Scholar
Wallis, J., & Lee, D. R. (1999). Primate conservation: The prevention of disease transmission. International Journal of Primatology, 20, 803826.Google Scholar
Washburn, D. A., Hopkins, W. D., & Rumbaugh, D. M. (1991). Perceived control in rhesus monkeys (Macaca mulatta): Enhanced video-task performance. Journal of Experimental Psychology: Animal Behavior Processes, 17, 123129.Google Scholar
Wheeler, B. C., & Hammerschmidt, K. (2013). Proximate factors underpinning receiver responses to deceptive false alarm calls in wild tufted capuchin monkeys: Is it counterdeception? American Journal of Primatology, 75, 715725.Google Scholar
Whitehouse, J., Micheletta, J., Powell, L. E., Bordier, C., & Waller, B. M. (2013). The impact of cognitive testing on the welfare of group housed primates. PLoS ONE, 8, e78308.Google Scholar
Williams, J. M., Lonsdorf, E. V., Wilson, M. L., Schumacher-Stankey, J., Goodall, J., & Pusey, A. E. (2008). Causes of death in the Kasekela chimpanzees of Gombe National Park, Tanzania. American Journal of Primatology, 70, 766777.CrossRefGoogle ScholarPubMed
Williamson, E. A., & Feistner, A. T. C. (2011). Habituating primates: Processes, techniques, variables and ethics. In Setchell, J. M. & Curtis, D. J. (Eds.), Field and laboratory methods in primatology: A practical guide (2nd ed., pp. 2539). Cambridge University Press.Google Scholar
Wilson, R. P., & McMahon, C. R. (2006). Measuring devices on wild animals: What constitutes acceptable practice? Frontiers in Ecology and the Environment, 4(3), 147154.Google Scholar
Wilson, S. D. (n.d.) Animals and ethics. The internet encyclopedia of philosophy. Retrieved January 25, 2021 from: www.iep.utm.edu/Google Scholar
Wolfe, L. D. (2005). Field primatologists: Duties, rights and obligations. In Turner, T. R. (Ed.), Biological anthropology and ethics: From repatriation to genetic identity (pp. 1526). State University of New York Press Press.Google Scholar
Woodford, M. H., Butynski, T. M., & Karesh, W. B. (2002). Habituating the great apes: The disease risks. Oryx, 36, 153160.Google Scholar
Yamanashi, Y., & Hayashi, M. (2011). Assessing the effects of cognitive experiments on the welfare of captive chimpanzees (Pan troglodytes) by direct comparison of activity budget between wild and captive chimpanzees. American Journal of Primatology, 73, 12311238.Google Scholar
Yamanashi, Y., & Matsuzawa, T. (2010). Emotional consequences when chimpanzees (Pan troglodytes) face challenges: Individual differences in self-directed behaviours during cognitive tasks. Animal Welfare, 19, 2530.Google Scholar
Zhang, B. (2017). Consequences of early adverse rearing experience (EARE) on development: Insights from non-human primate studies. Zoological Research, 38, 7.Google Scholar
Zuberbühler, K. (2014). Experimental field studies with non-human primates. Current Opinion in Neurobiology, 28, 150156.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×