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Do zoo visitors induce attentional bias effects in primates completing cognitive tasks?

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Abstract

While previous research has focused on the impact of visitors on zoo-housed animals’ behavior, here, we evaluated the impact of visitors on the performance of four zoo-housed Japanese macaques (Macaca fuscata) in a cognitive task. The macaques completed a touchscreen-based match-to-sample task in glass-sided booths at the perimeter of their enclosure, adjacent to a visitor viewing area. The task was novel to all macaques at the start of this study but over the 6-month testing period the macaques showed increased accuracy on the task, suggestive of learning. We recorded the number of visitors within the viewing area roughly every 12 trials each macaque completed. We categorized visitor counts as small (0–20), medium (21–40), and large (41–60) crowds and we considered the macaques’ response latencies and accuracy by crowd size and study period (first 3 months versus second 3 months). If visitor presence negatively influenced performance, we predicted that macaques’ accuracy would decrease but response times would increase with crowd size. We found effects of crowd size and study period on the macaques’ accuracy. In the first period, the macaques performed at chance and accuracy did not differ across crowd categories. In the second period, the macaques’ accuracy improved as compared to the first period, but their accuracy was mediated by crowd size: the macaques were significantly more accurate in the presence of small crowds than medium or large crowds. The macaques’ response latencies also varied by study period and crowd size, but we found no evidence of a response-slowing effect.

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Data are provided as supplementary materials.

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Code is provided as supplementary materials.

References

  • Bakdash JZ, Marusich LR (2017) Repeated measures correlation. Front Psychol 8:456

    PubMed  PubMed Central  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Google Scholar 

  • Bethell EJ, Holmes A, MacLarnon A, Semple S (2016) Emotion evaluation and response slowing in a non-human primate: new directions for cognitive bias measures of animal emotion? Behav Sci 6:2

    Google Scholar 

  • Blaney EC, Wells DL (2004) The influence of a camouflage net barrier on the behaviour, welfare and public perceptions of zoo-housed gorillas. Anim Welf 13:111–118

    CAS  Google Scholar 

  • Boggiani L, Addessi E, Schino G (2018) Receiving aggression triggers attention bias in tufted capuchin monkeys. Anim Behav 146:173–180

    Google Scholar 

  • Bowler MT, Buchanan-Smith H, Whiten A (2012) Assessing public engagement with science in a university research center in a national zoo. PLoS ONE 7(4):e34505

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brydges NM, Hall L, Nicolson R, Holmes MC, Hall J (2012) The effects of juvenile stress on anxiety, cognitive bias and decision making in adulthood: A rat model. PLoS ONE 7:e48143

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carder G, Semple S (2008) Visitor effects on anxiety in two captive groups of western lowland gorillas. Appl Anim Beh Sci 115:211–220

    Google Scholar 

  • Carlson S, Rama P, Artchakov D, Linnakoski I (1997) Effect of music and white noise on working memory performance in monkeys. NeuroReport 8:2853–2856

    CAS  PubMed  Google Scholar 

  • Cisler JM, Bacon AK, Williams NL (2009) Phenomenological characteristics of attentional biases towards threat: a critical review. Cognit Ther Res 33(2):221–234

    PubMed  PubMed Central  Google Scholar 

  • Clark FE (2017) Cognitive enrichment and welfare: current approaches and future directions. Anim Behav Cogn 4:52–71

    Google Scholar 

  • Cosman JD, Lowe KA, Zinke W, Woodman GF, Schall JD (2018) Prefrontal control of visual distraction. Curr Biol 28:414-420.e3

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cronin KA, Bethell EJ, Jacobson SL, Egelkamp C, Hopper LM, Ross SR (2018) Evaluating mood changes in response to anthropogenic noise with a response-slowing task in three species of zoo-housed primates. Anim Behav Cogn 5:209–221

    Google Scholar 

  • Cussen VA, Mench JA (2014) Personality predicts cognitive bias in captive psittacines, Amazona amazonica. Anim Behav 89:123–130

    Google Scholar 

  • Egelkamp CL, Ross SR (2019) A review of zoo-based cognitive research using touchscreen interfaces. Zoo Biol 38:220–235

    PubMed  Google Scholar 

  • Hampton RR (2009) Multiple demonstrations of metacognition in nonhumans: converging evidence or multiple mechanisms? Comp Cogn Behav Rev 4:17–28

    PubMed  PubMed Central  Google Scholar 

  • Hansen BK, Hopper LM, Ross SR, Fultz AL (2020) Understanding the effects of public programs on sanctuary-housed chimpanzees. Anthrozoös 33:481–495

    Google Scholar 

  • Herrelko ES, Vick SJ, Buchanan-Smith HM (2012) Cognitive research in zoo-housed chimpanzees: Influence of personality and impact on welfare. Am J Primatol 74:828–840

    PubMed  Google Scholar 

  • Hopper LM (2017) Cognitive research in zoos. Curr Opin Behav Sci 16:100–110

    Google Scholar 

  • Hopper LM, Kurtycz LM, Ross SR, Bonnie KE (2015) Captive chimpanzee foraging in a social setting A test of problem solving, flexibility, and spatial discounting. PeerJ 3:e833

    PubMed  PubMed Central  Google Scholar 

  • Hopper LM, Shender MA, Ross SR (2016) Behavioral research as physical enrichment for captive chimpanzees. Zoo Biol 35:293–297

    PubMed  Google Scholar 

  • Hopper LM, Gulli RA, Howard LH, Kano F, Krupenye C, Ryan AM, Paukner A (2020) The application of non-invasive, restraint-free eye-tracking methods for use with nonhuman primates. Behav Res Methods. https://doi.org/10.3758/s13428-020-01456-6

    Article  PubMed  Google Scholar 

  • Huguet P, Barbet I, Belletier C, Monteil J-M, Fagot J (2014) Cognitive control under social influence in baboons. J Exp Psychol Gen 143:2067–2073

    PubMed  Google Scholar 

  • Huskisson SM, Jacobson SL, Egelkamp CE, Ross SR, Hopper LM (2020) Using a touchscreen paradigm to evaluate food preferences and response to novel photographic stimuli of food in three primate species (Gorilla gorilla gorilla, Pan troglodytes, and Macaca fuscata). Int J Primatol 41:5–23

    Google Scholar 

  • Jacobson SL, Kwiatt AC, Ross SR, Cronin KA (2019) The effects of cognitive testing on the welfare of zoo-housed Japanese macaques (Macaca fuscata). Appl Anim Behav Sci 212:90–97

    Google Scholar 

  • Kret ME, Jaasma L, Bionda T, Wijnen JG (2016) Bonobos (Pan paniscus) show an attentional bias toward conspecifics’ emotions. P Natl Acad Sci USA 113:3761–3766

    CAS  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26

    Google Scholar 

  • Lee C, Verbeek E, Doyle R, Bateson M (2016) Attention bias to threat indicates anxiety differences in sheep. Biol Lett 12:20150977

    PubMed  PubMed Central  Google Scholar 

  • Lee KA, Preston AJ, Wise TB, Templer VL (2018) Testing for metacognitive responding using an odor-based delayed match-to-sample test in rats. J Vis Exp 136:e57489

    Google Scholar 

  • Leeds A, Lukas KE (2019) Monitoring the social behavior of a bachelor mandrill (Mandrillus sphinx) dyad participating in touchscreen-mediated cognitive testing. Zoo Biol 38:397–402

    PubMed  Google Scholar 

  • Leinwand JG, Huskisson SM, Egelkamp CL, Hopper LM (2020) Within- and between-species variation in the responses of three primate species to a touchscreen gambling task. Learn Motiv 71:101635

    Google Scholar 

  • Martin CF (2017) ApeTouch software suite [Computer software]. Indianapolis, IN

  • Price A, Boeving ER, Shender MA, Ross SR (2015) Understanding the effectiveness of demonstration programs. J Museum Edu 40:46–54

    Google Scholar 

  • R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org/

  • Ratcliff R (1993) Methods for dealing with reaction time outliers. Psychol Bull 114:510–532

    CAS  PubMed  Google Scholar 

  • Ross SR (2010) How cognitive studies help shape our obligation for the ethical care of chimpanzees. In: Lonsdorf EV, Ross SR, Matsuzawa T (eds) The mind of the chimpanzee. University of Chicago Press, Chicago, pp 309–319

    Google Scholar 

  • Roth AM, Cords M (2020) Zoo visitors affect sleep, displacement activities, and affiliative and aggressive behaviors in captive ebony langurs (Trachypithecus auratus). Acta Ethologica 2:1–8

    Google Scholar 

  • Sherwen SL, Hemsworth PH (2019) The visitor effect on zoo animals: implications and opportunities for zoo animal welfare. Animals 9:366

    Google Scholar 

  • Sherwen SL, Harvey TJ, Magrath ML, Butler KL, Fanson KV, Hemsworth PH (2015) Effects of visual contact with zoo visitors on black-capped capuchin welfare. Appl Anim Beh Sci 167:65–73

    Google Scholar 

  • Tu HW, Hampton RR (2013) One-trial memory and habit contribute independently to matching-to-sample performance in rhesus macaques (Macaca mulatta). J Comparat Psych 127:319–328

    Google Scholar 

  • Vonk J, Jett SE (2018) “Bear-ly” learning: Limits of abstraction in black bear cognition. Anim Behav Cogn 5:68–78

    Google Scholar 

  • Webber S, Carter M, Sherwen S, Smith W, Joukhadar Z, and Vetere F (2017) Kinecting with orangutans: Zoo visitors' empathetic responses to animals’ use of interactive technology. Proceedings of the 2017 CHI Conference on Human Factors in Computing Systems, 6075–6088.

  • Whitehouse J, Micheletta J, Powell LE, Bordier C, Waller BM (2013) The impact of cognitive testing on the welfare of group housed primates. PLoS ONE 8:11

    Google Scholar 

  • Wilson DA, Tomonaga M (2018) Exploring attentional biases towards threatening faces in chimpanzees using the dot probe task. PLoS ONE 13:e0207378

    PubMed  PubMed Central  Google Scholar 

  • Wolfensohn S, Shotton J, Bowley H, Davies S, Thompson S, Justice WSM (2018) Assessment of welfare in zoo animals: towards optimum quality of life. Animals 8:110

    Google Scholar 

  • 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

    Google Scholar 

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Acknowledgements

The authors would like to thank the animal care staff at Lincoln Park Zoo’s Regenstein Macaque Forest for the daily care for our subjects and for being supportive of our research, in particular Jill Moyse and Danielle Fogarty. We also greatly appreciate the helpful feedback offered to us by three anonymous reviewers on an earlier version of this article. We also thank the Lincoln Park Zoo Women’s Board for funding this research.

Funding

The Lincoln Park Zoo Women’s Board.

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Authors and Affiliations

Authors

Contributions

SMH: Methodology, investigation, data curation, formal analysis, visualization, writing—original draft, writing—review and editing; SRR: Funding acquisition, resources, supervision, writing—review and editing; and LMH: Conceptualization, methodology, data curation, formal analysis, funding acquisition, project administration, resources, supervision, writing—review and editing.

Corresponding author

Correspondence to Lydia M. Hopper.

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The author declares that they have no conflicts of interest.

Ethics approval

This study was approved by Lincoln Park Zoo’s Research Committee and was conducted in accordance with the American Society of Primatologists’ Principles for the Ethical Treatment of Nonhuman Primates.

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Huskisson, S.M., Ross, S.R. & Hopper, L.M. Do zoo visitors induce attentional bias effects in primates completing cognitive tasks?. Anim Cogn 24, 645–653 (2021). https://doi.org/10.1007/s10071-020-01445-5

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