Estimating the cardiac signals of chimpanzees using a digital camera: validation and application of a novel non-invasive method for primate research.
Comparative psychology
Contact-free
Heart rate
Signal processing
Journal
Behavior research methods
ISSN: 1554-3528
Titre abrégé: Behav Res Methods
Pays: United States
ID NLM: 101244316
Informations de publication
Date de publication:
30 May 2023
30 May 2023
Historique:
accepted:
24
04
2023
medline:
30
5
2023
pubmed:
30
5
2023
entrez:
30
5
2023
Statut:
aheadofprint
Résumé
Cardiac measures such as heart rate measurements are important indicators of both physiological and psychological states. However, despite their extraordinary potential, their use is restricted in comparative psychology because traditionally cardiac measures involved the attachment of sensors to the participant's body, which, in the case of undomesticated animals such as nonhuman primates, is usually only possible during anesthesia or after extensive training. Here, we validate and apply a camera-based system that enables contact-free detection of animals' heart rates. The system automatically detects and estimates the cardiac signals from cyclic change in the hue of the facial area of a chimpanzee. In Study 1, we recorded the heart rate of chimpanzees using the new technology, while simultaneously measuring heart rate using classic PPG (photoplethysmography) finger sensors. We found that both methods were in good agreement. In Study 2, we applied our new method to measure chimpanzees' heart rate in response to seeing different types of video scenes (groupmates in an agonistic interaction, conspecific strangers feeding, nature videos, etc.). Heart rates changed during video presentation, depending on the video content: Agonistic interactions and conspecific strangers feeding lead to accelerated heart rate relative to baseline, indicating increased emotional arousal. Nature videos lead to decelerated heart rate relative to baseline, indicating a relaxing effect or heightened attention caused by these stimuli. Our results show that the new contact-free technology can reliably assess the heart rate of unrestrained chimpanzees, and most likely other primates. Furthermore, our technique opens up new avenues of research within comparative psychology and facilitates the health management of captive individuals.
Identifiants
pubmed: 37249898
doi: 10.3758/s13428-023-02136-y
pii: 10.3758/s13428-023-02136-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s).
Références
Aiello, S. E. (2016). The Merck veterinary manual (p. 3325). White Station, NJ, USA: Merck & Company, Incorporated.
Al-Naji, A., Gibson, K., Lee, S.-H., & Chahl, J. (2017a). Monitoring of cardiorespiratory signal: Principles of remote measurements and review of methods. IEEE Access, 5, 15776–15790.
doi: 10.1109/ACCESS.2017.2735419
Al-Naji, A., Gibson, K., Lee, S.-H., & Chahl, J. (2017b). Real-time apnoea monitoring of children using the Microsoft Kinect sensor: A pilot study. Sensors, 17, 286.
pubmed: 28165382
pmcid: 5336086
doi: 10.3390/s17020286
Al-Naji, A., Perera, A., & Chahl, J. (2017c). Remote monitoring of cardiorespiratory signals from a hovering unmanned aerial vehicle. Biomedical Engineering Online (16), 101.
Al-Naji, A., Tao, Y., Smith, I., & Chahl, J. (2019). A pilot study for estimating the cardiopulmonary signals of diverse exotic animals using a digital camera. Sensors, 19, 5445.
pubmed: 31835550
pmcid: 6960731
doi: 10.3390/s19245445
Aureli, F., Preston, S. D., & de Waal, F. (1999). Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): A pilot study. Journal of Comparative Psychology, 113, 59.
pubmed: 10098269
doi: 10.1037/0735-7036.113.1.59
Balakrishnan, G. D. F. (2013). Detecting pulse from head motions in video[C]. Proceedings of the IEEE conference on computer vision and pattern recognition., 3430–3437.
Barr, D. (2013). Random effects structure for testing mixed-effects models. Frontiers in Psychology, 4, 328.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, Articles, 67, 1–48. https://doi.org/10.18637/jss.v067.i01
doi: 10.18637/jss.v067.i01
Bernardi, L., Porta, C., & Sleight, P. (2006). Cardiovascular, cerebrovascular, and respiratory changes induced by different types of music in musicians and non-musicians: The importance of silence. Heart, 92, 445–452.
pubmed: 16199412
doi: 10.1136/hrt.2005.064600
Berntson, G. G. (1984). Cardiac startle and orienting responses in the great apes. Behavioral Neuroscience, 98(5), 914–918. https://doi.org/10.1037/0735-7044.98.5.914
doi: 10.1037/0735-7044.98.5.914
pubmed: 6487420
Berntson, G. G. (1989). Specificity of the cardiac response to conspecific vocalizations in the chimpanzee. Behavioral Neuroscience, 103, 235–245.
pubmed: 2706070
doi: 10.1037/0735-7044.103.2.235
Berntson, G. G., Boysen, S. T., Bauer, H. R., & Torello, M. S. (1989). Conspecific screams and laughter: Cardiac and behavioral reactions of infant chimpanzees. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology, 22, 771–787.
doi: 10.1002/dev.420220803
Bliss-Moreau, E., Machado, C. J., & Amaral, D. G. (2013). Macaque cardiac physiology is sensitive to the valence of passively viewed sensory stimuli. PLoS One, 8, e71170.
pubmed: 23940712
pmcid: 3734104
doi: 10.1371/journal.pone.0071170
Boesch, C., Crockford, C., Herbinger, I., Wittig, R., Moebius, Y., & Normand, E. (2008). Intergroup conflicts among chimpanzees in Taı̈ National Park: Lethal violence and the female perspective. American Journal of Primatology: Official Journal of the American Society of Primatologists, 70, 519–532.
doi: 10.1002/ajp.20524
Bolme, D. S., Beveridge, J. R., Draper, B. A., & Lui, Y. M. (2010). Visual object tracking using adaptive correlation filters. 2010 IEEE computer society conference on computer vision and pattern recognition, (pp. 2544–2550).
Boysen, S. T., & Berntson, G. G. (1986). Cardiac correlates of individual recognition in the chimpanzee (pan troglodytes). Journal of Comparative Psychology, 100, 321.
pubmed: 3769449
doi: 10.1037/0735-7036.100.3.321
Boysen, S. T., & Berntson, G. G. (1989). Conspecific recognition in the chimpanzee (pan troglodytes): Cardiac responses to significant others. Journal of Comparative Psychology, 103, 215.
pubmed: 2776418
doi: 10.1037/0735-7036.103.3.215
Bräuer, J., & Call, J. (2011). The magic cup: Great apes and domestic dogs (Canis familiaris) individuate objects according to their properties. Journal of Comparative Psychology, 125, 353.
pubmed: 21574687
doi: 10.1037/a0023009
Brez, C. C., & Colombo, J. (2012). Your eyes say “no,” but your heart says “yes”: Behavioral and psychophysiological indices in infant quantitative processing. Infancy, 17, 445–454.
doi: 10.1111/j.1532-7078.2011.00094.x
Brock, S. E., Rothbart, M. K., & Derryberry, D. (1986). Heart-rate deceleration and smiling in 3-month-old infants. Infant Behavior and Development, 9, 403–414.
doi: 10.1016/0163-6383(86)90014-7
Brown, D. K., Barton, J. L., & Gladwell, V. F. (2013). Viewing nature scenes positively affects recovery of autonomic function following acute-mental stress. Environmental Science & Technology, 47, 5562–5569.
doi: 10.1021/es305019p
Cassinello, J., & Pieters, I. (2000). Multi-male captive groups of endangered dama gazelle: Social rank, aggression, and enclosure effects. Zoo Biology: Published in affiliation with the American Zoo and Aquarium Association, 19, 121–129.
doi: 10.1002/1098-2361(2000)19:2<121::AID-ZOO3>3.0.CO;2-1
Caza, N., Taha, R., Qi, Y., & Blaise, G. (2008). The effects of surgery and anesthesia on memory and cognition. Progress in Brain Research, 169, 409–422.
pubmed: 18394490
doi: 10.1016/S0079-6123(07)00026-X
Chang, T. R., Forthman, D. L., & Maple, T. L. (1999). Comparison of confined mandrill (Mandrillus sphinx) behavior in traditional and “ecologically representative” exhibits. Zoo Biology: Published in affiliation with the American Zoo and Aquarium Association, 18, 163–176.
doi: 10.1002/(SICI)1098-2361(1999)18:3<163::AID-ZOO1>3.0.CO;2-T
Chen, X., Zhao, M., White, P. F., Li, S., Tang, J., Wender, R. H., . . . others. (2001). The recovery of cognitive function after general anesthesia in elderly patients: A comparison of desflurane and sevoflurane. Anesthesia & Analgesia, 93, 1489–1494.
Chlan, L. (1998). Effectiveness of a music therapy intervention on relaxation and anxiety for patients receiving ventilatory assistance. Heart & Lung, 27, 169–176.
doi: 10.1016/S0147-9563(98)90004-8
Cloutier Barbour, C., Danforth, M. D., Murphy, H., Sleeper, M. M., & Kutinsky, I. (2020). Monitoring great ape heart health through innovative electrocardiogram technology: Training methodologies and welfare implications. Zoo Biology, 39, 443–447.
pubmed: 32909258
doi: 10.1002/zoo.21567
Clubb, R., & Mason, G. (2003). Captivity effects on wide-ranging carnivores. Nature, 425, 473–474.
pubmed: 14523435
doi: 10.1038/425473a
Clubb, R., & Mason, G. J. (2007). Natural behavioural biology as a risk factor in carnivore welfare: How analysing species differences could help zoos improve enclosures. Applied Animal Behaviour Science, 102, 303–328.
doi: 10.1016/j.applanim.2006.05.033
Colombo, J. R. (2001). Heart rate defined phases of attention, look duration, and infant performance in the paired-comparison paradigm. Child Development, 72(6), 1605–1616.
pubmed: 11768135
doi: 10.1111/1467-8624.00368
Colominas, M. A., Schlotthauer, G., & Torres, M. E. (2014). Improved complete ensemble EMD: A suitable tool for biomedical signal processing. Biomedical Signal Processing and Control, 14, 19–29.
Darrow, C. W. (1929). Differences in the physiological reactions to sensory and ideational stimuli. Psychological Bulletin, 26, 185.
doi: 10.1037/h0074053
Davey, G. (2006). Relationships between exhibit naturalism, animal visibility and visitor interest in a Chinese zoo. Applied Animal Behaviour Science, 96, 93–102.
doi: 10.1016/j.applanim.2005.04.018
Davis, C., Crowell, D., & Chun, B. (1965). Monophasic heart rate accelerations in human infants to peripheral stimulation., 478.
Delaney, J. P. A., & Brodie, D. A. (2000). Effects of short-term psychological stress on the time and frequency domains of heart-rate variability. Perceptual and Motor Skills, 2000(91), 515–524.
Derakhchan, K., Chui, R. W., Stevens, D., Gu, W., & Vargas, H. M. (2014). Detection of QTc interval prolongation using jacket telemetry in conscious non-human primates: Comparison with implanted telemetry. British Journal of Pharmacology, 171, 509–522.
pubmed: 24372552
doi: 10.1111/bph.12484
Dezecache, G., Zuberbühler, K., Davila-Ross, M., & Dahl, C. D. (2017). Skin temperature changes in wild chimpanzees upon hearing vocalizations of conspecifics. Royal Society Open Science, 4, 160816.
pubmed: 28280584
pmcid: 5319350
doi: 10.1098/rsos.160816
Dobson, A. J., & Barnett, A. G. (2008). An introduction to generalized linear models. CRC Press.
doi: 10.1201/9780367807849
Elsner, B., Pauen, S., & Jeschonek, S. (2006). Physiological and behavioral parameters of infants’ categorization: Changes in heart rate and duration of examining across trials. Developmental Science, 9, 551–556.
pubmed: 17059451
doi: 10.1111/j.1467-7687.2006.00532.x
Erickson, H. H., & Olsen, S. C. (1985). Electrocardiogram, heart rate, and blood pressure in the chimpanzee. The Journal of Zoo Animal Medicine, 16, 89–97.
doi: 10.2307/20094753
Fàbregas, M. C., Guillén-Salazar, F., & Garcés-Narro, C. (2012). Do naturalistic enclosures provide suitable environments for zoo animals? Zoo Biology, 31, 362–373.
pubmed: 21688309
doi: 10.1002/zoo.20404
Forstmeier, W., & Schielzeth, H. (2011). Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner's curse. Behavioral Ecology and Sociobiology, 65, 47–55.
pubmed: 21297852
doi: 10.1007/s00265-010-1038-5
Froesel, M. G. (2020). Automated video-based heart rate tracking for the anesthetized and behaving monkey. Scientific Reports, 1–11.
Graham, F. K., & Clifton, R. K. (1966). Heart-rate change as a component of the orienting response. Psychological Bulletin, 65, 305.
pubmed: 5325894
doi: 10.1037/h0023258
Graham, F. K., & Jackson, J. C. (1970). Arousal systems and infant heart rate responses. Advances in Child Development and Behavior, 5, 59–117.
pubmed: 4950022
doi: 10.1016/S0065-2407(08)60465-6
Graham, F., Anthony, B., & Zeigler, B. (1983). The orienting response and developmental processes. 371–430.
Hajar, R. (2018). The pulse from ancient to modern medicine: Part 3. Heart Views: The Official Journal of the Gulf Heart Association, 19(3), 117.
pubmed: 31007864
doi: 10.4103/HEARTVIEWS.HEARTVIEWS_16_19
Hall, M., Vasko, R., Buysse, D., Ombao, H., Chen, Q., Cashmere, J. D., Kupfer, D., & Thayer, J. F. (2004). Acute stress affects heart rate variability during sleep. Psychosomatic Medicine, 66, 56–62.
pubmed: 14747638
doi: 10.1097/01.PSY.0000106884.58744.09
Hilz, M. J., Stadler, P., Gryc, T., Nath, J., Habib-Romstoeck, L., Stemper, B., & Koehn, J. (2014). Music induces different cardiac autonomic arousal effects in young and older persons. Autonomic Neuroscience, 183, 83–93.
pubmed: 24636674
doi: 10.1016/j.autneu.2014.02.004
Horschler, D. J., Santos, L. R., & MacLean, E. L. (2019). Do non-human primates really represent others’ ignorance? A test of the awareness relations hypothesis. Cognition, 190, 72–80.
pubmed: 31026672
pmcid: 6570545
doi: 10.1016/j.cognition.2019.04.012
Hyeroba, D. A. (2011). Managing a speared alpha male chimpanzee (pan troglodytes) in Kibale National Park, Uganda. The Veterinary Record, 169(25), 658.
pubmed: 21984563
doi: 10.1136/vr.d4680
Ing, C., DiMaggio, C., Whitehouse, A., Hegarty, M. K., Brady, J., von Ungern-Sternberg, B. S., & Sun, L. S. (2012). Long-term differences in language and cognitive function after childhood exposure to anesthesia. Pediatrics, 130, e476–e485.
pubmed: 22908104
doi: 10.1542/peds.2011-3822
Jensen, M. T. (2019). Resting heart rate and relation to disease and longevity: Past, present and future. Scandinavian Journal of Clinical and Laboratory Investigation, 79(1–2), 108–116.
pubmed: 30761923
doi: 10.1080/00365513.2019.1566567
Kano, F., Hirata, S., Deschner, T., Behringer, V., & Call, J. (2016). Nasal temperature drop in response to a playback of conspecific fights in chimpanzees: A thermo-imaging study. Physiology & Behavior, 155, 83–94.
doi: 10.1016/j.physbeh.2015.11.029
Kearns, K. S., Swenson, B., & Ramsay, E. C. (2000). Oral induction of anesthesia with droperidol and transmucosal carfentonil citrate in chimpanzees (Pan troglodytes). J Zoo Wildlife Med, 31, 185–189.
doi: 10.1638/1042-7260(2000)031[0185:OIOAWD]2.0.CO;2
Kremer, J. J., Foley, C. M., Xiang, Z., Lemke, E., Sarazan, R. D., Osinski, M. A., & Beck, T. W. (2011). Comparison of ECG signals and arrhythmia detection using jacketed external telemetry and implanted telemetry in monkeys. Journal of Pharmacological and Toxicological Methods, 1, e47.
doi: 10.1016/j.vascn.2011.03.164
Krumhansl, C. L. (1997). An exploratory study of musical emotions and psychophysiology. Canadian Journal of Experimental Psychology/Revue canadienne de psychologie expérimentale, 51, 336.
pubmed: 9606949
doi: 10.1037/1196-1961.51.4.336
Kutska, D. (2009). Variation in visitor perceptions of a polar bear enclosure based on the presence of natural vs. un-natural enrichment items. Zoo Biology: Published in affiliation with the American Zoo and Aquarium Association, 28, 292–306.
doi: 10.1002/zoo.20226
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82, 1–26.
doi: 10.18637/jss.v082.i13
Lacey, J. I. (1959). Psychophysiological approaches to the evaluation of psychotherapeutic process and outcome. In E. A. Rubinstein & M. B. Parloff (Eds.), Research in psychotherapy (pp. 160–208). American Psychological Association. https://doi.org/10.1037/10036-010
Lansink, J. M. (1997). Heart rate and behavioral measures of attention in six-, nine-, and twelve-month-old infants during object exploration. Child Development, 68(4), 610–620.
pubmed: 9306641
doi: 10.2307/1132113
Lowenstine, L. J., McManamon, R., & Terio, K. A. (2016). Comparative pathology of aging great apes: Bonobos, chimpanzees, gorillas, and orangutans. Veterinary Pathology, 53, 250–276.
pubmed: 26721908
doi: 10.1177/0300985815612154
Maple, T. L., & Finlay, T. W. (1986). Evaluating the environments of captive nonhuman primates. In Primates (pp. 479–488). Springer.
doi: 10.1007/978-1-4612-4918-4_38
Maple, T. L., & Perdue, B. M. (2013). Zoo animal welfare (vol. 14). Berlin, Germany: Springer.
Maple, T. L., & Stine, W. W. (1982). Environmental variables and great ape husbandry. American Journal of Primatology, 3, 67–76.
doi: 10.1002/ajp.1350030513
McCraty, R. A. M. (1995). The effects of emotions on short-term power spectrum analysis of heart rate variability. The American Journal of Cardiology, 76, 1089–1093.
pubmed: 7484873
doi: 10.1016/S0002-9149(99)80309-9
Melfi, V. A., McCormick, W., & Gibbs, A. (2004). A preliminary assessment of how zoo visitors evaluate animal welfare according to enclosure style and the expression of behavior. Anthrozoös, 17, 98–108.
doi: 10.2752/089279304786991792
Ming-Zher Poh, D. J. (2010). Non-contact, automated cardiac pulse measurements using video imaging and blind source separation. Optics Express, 10762–10774.
Mireault, G. C., Crockenberg, S. C., Heilman, K., Sparrow, J. E., Cousineau, K., & Rainville, B. (2018). Social, cognitive, and physiological aspects of humour perception from 4 to 8 months: Two longitudinal studies. British Journal of Developmental Psychology, 36, 98–109.
pubmed: 28944500
doi: 10.1111/bjdp.12216
Murphy, H. W., Danforth, M. D., & Clyde, V. L. (2018). The great ape heart project. International Zoo Yearbook, 52, 103–112.
doi: 10.1111/izy.12180
Nomura, S., Yoshimura, K., & Kurosawa, Y. (2013). A pilot study on the effect of music-heart beat feedback system on human heart activity. Journal of Medical Informatics & Technologies, 22, 251–256.
Ogden, J. J., Lindburg, D. G., & MAPLE, T. L. (1993). The effects of ecologically-relevant sounds on zoo visitors. Curator: The Museum Journal, 36, 147–156.
doi: 10.1111/j.2151-6952.1993.tb00787.x
Park, B. J., Tsunetsugu, Y., Kasetani, T., Kagawa, T., & Miyazaki, Y. (2010). The physiological effects of Shinrin-yoku (taking in the forest atmosphere or forest bathing): Evidence from field experiments in 24 forests across Japan. Environmental Health and Preventive Medicine, 15, 18–26.
pubmed: 19568835
doi: 10.1007/s12199-009-0086-9
R Core Team. (2021). R: A language and environment for statistical computing. Retrieved from http://www.R-project.org/
Raper, J., Alvarado, M. C., Murphy, K. L., & Baxter, M. G. (2015). Multiple anesthetic exposure in infant monkeys alters emotional reactivity to an acute stressor. Anesthesiology, 123, 1084–1092.
pubmed: 26313293
doi: 10.1097/ALN.0000000000000851
Rasmussen, L. S. (2006). Postoperative cognitive dysfunction: Incidence and prevention. Best Practice & Research Clinical Anaesthesiology, 20, 315–330.
doi: 10.1016/j.bpa.2005.10.011
Reynolds, G. D., & Richards, J. E. (2008). Infant heart rate: A developmental psychophysiological perspective.
Richards, J. E. (1992). Development of sustained visual attention in the human infant. Attention and information processing in infants and adults: Perspectives from human and animal research, 30–60.
Sahlin, E., Lindegård, A., Hadzibajramovic, E., Grahn, P., Vega Matuszczyk, J., & Ahlborg, G., Jr. (2016). The influence of the environment on directed attention, blood pressure and heart rate—An experimental study using a relaxation intervention. Landscape Research, 41, 7–25.
doi: 10.1080/01426397.2014.982079
Santos, L. R., Barnes, J. L., & Mahajan, N. (2005). Expectations about numerical events in four lemur species (Eulemur fulvus, Eulemur mongoz, Lemur catta and Varecia rubra). Animal Cognition, 8, 253–262.
pubmed: 15729569
doi: 10.1007/s10071-005-0252-4
Schielzeth, H., & Forstmeier, W. (2009). Conclusions beyond support: Overconfident estimates in mixed models. Behavioral Ecology, 20, 416–420.
pubmed: 19461866
doi: 10.1093/beheco/arn145
Shepherdson, D. J. (1998). Tracing the path of environmental enrichment in zoos (pp. 1–12). Environmental enrichment for captive animals.
Shively, C. A. (2015). Social inequalities in health in nonhuman primates. Neurobiology of Stress, 1, 156–163.
pubmed: 27589665
doi: 10.1016/j.ynstr.2014.11.005
Sleigh, J. W., & Henderson, J. D. (1995). Heart-rate-variability and preoperative anxiety. Acta Anaesthesiologica Scandinavica, 39, 1059–1061.
pubmed: 8607309
doi: 10.1111/j.1399-6576.1995.tb04229.x
Snyder, D. S. (1984). Peer separation in infant chimpanzees, a pilot study. Primates, 25(1), 78–88.
doi: 10.1007/BF02382297
Sommerfeldt, S. L. (2019). Individual differences in the association between subjective stress and heart rate are related to psychological and physical well-being. Psychological Science, 30(7).
Stekelenburg, J. J. (2002). Pericranial muscular, respiratory, and heart rate components of the orienting response. Psychophysiology, 39(6), 707–722.
pubmed: 12462499
doi: 10.1111/1469-8986.3960707
Stroud, P. (2007). Defining issues of space in zoos. Journal of Veterinary Behavior, 2, 219–222.
doi: 10.1016/j.jveb.2007.10.003
Talpos, J. C., Chelonis, J. J., Li, M., Hanig, J. P., & Paule, M. G. (2019). Early life exposure to extended general anesthesia with isoflurane and nitrous oxide reduces responsivity on a cognitive test battery in the nonhuman primate. Neurotoxicology, 70, 80–90.
pubmed: 30445043
doi: 10.1016/j.neuro.2018.11.005
Uller, C., Carey, S., Hauser, M., & Xu, F. (1997). Is language needed for constructing sortal concepts? A study with nonhuman primates. Proceedings of the 21st annual Boston University conference on language development, 21, 665–677.
Unakafov, A. M., Möller, S., Kagan, I., Gail, A., Treue, S., & Wolf, F. (2018). Using imaging photoplethysmography for heart rate estimation in non-human primates. PLoS One, 13, e0202581.
pubmed: 30169537
pmcid: 6118383
doi: 10.1371/journal.pone.0202581
Von Borell, E. L.-F. (2007). Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals—A review. Physiology & Behavior, 92(3), 293–316.
doi: 10.1016/j.physbeh.2007.01.007
Walters, J. L., Zhang, X., Talpos, J. C., Fogle, C. M., Li, M., Chelonis, J. J., & Paule, M. G. (2019). Sevoflurane exposure has minimal effect on cognitive function and does not alter microglial activation in adult monkeys. Neurotoxicology, 71, 159–167.
pubmed: 30605762
doi: 10.1016/j.neuro.2018.12.008
Watts, D. P., & Mitani, J. C. (2001). Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour, 299–327.
Watts, D. P., Muller, M., Amsler, S. J., Mbabazi, G., & Mitani, J. C. (2006). Lethal intergroup aggression by chimpanzees in Kibale National Park, Uganda. American Journal of Primatology: Official Journal of the American Society of Primatologists, 68, 161–180.
doi: 10.1002/ajp.20214
Weissler, A. M., Fineg, J., & Warren, J. V. (1961). The electrocardiogram of the young chimpanzee. Texas Univ Galveston Medical Branch.
Wilson, M. L., & Wrangham, R. W. (2003). Intergroup relations in chimpanzees. Annual Review of Anthropology, 32, 363–392. https://doi.org/10.1146/annurev.anthro.32.061002.120046
doi: 10.1146/annurev.anthro.32.061002.120046
Wim Verkruysse, L. O. (2008). Remote plethysmographic imaging using ambient light. Optics Express, 21434–21445.
Winters, S., Dubuc, C., & Higham, J. P. (2015). Perspectives: The looking time experimental paradigm in studies of animal visual perception and cognition. Ethology, 121, 625–640.
doi: 10.1111/eth.12378
Wolf, R. L., & Tymitz, B. L. (1981). Studying visitor perceptions of zoo environments: A naturalistic view. International zoo yearbook, 21, 49–53.
doi: 10.1111/j.1748-1090.1981.tb01943.x