Research on primate behavior, especially chimpanzees, is used to develop theories about the evolution of human behavior. But we can only observe primates that tolerate us following them around. The process of tracking primates until they learn to accept their human paparazzi is known as habituation. But could observing primates cause them to act differently? When evolutionary theorists like Steven Pinker or Richard Wrangham argue that humans are innately violent based on evidence from chimpanzee hunting and aggression, how do we know the data they’ve drawn from wasn’t biased in the process of human observation? In particle physics, the mere act of looking at an electron changes its direction of movement (because it collides with a photon). In a similar way, could observing primates in the field also change the outcome of what is observed?

There has previously been some evidence to suggest this might be the case. At Gombe Stream National Park in Tanzania, where Jane Goodall studied chimpanzees, the chimps were given bananas in order to speed habituation. However, it had the unanticipated side effect of causing aggressive competition over the bananas they were provisioned with. Today, researchers typically avoid provisioning animals with food for this very reason. However, until recently, there was no way of knowing how habituation and observation affected behavior. With the advent of new technology to remotely observe animals, we can finally begin to figure out what primates do when there aren’t humans watching their every move.

The author conducting behavioral research on the island of Cayo Santiago.

One of the first indicators of how behavior may change in the presence of humans comes from studies of vervet monkeys. In 1993, Lynne Isbell and Truman Young reported long term data on predation rates of the species Chlorocebus aethiops. Vervets are small monkeys that make a tasty snack for leopards. However, the researchers noticed that vervets were more likely to disappear during periods when field researchers were away from the site. The data indicated that the monkeys’ disappearance rate was 3.6 times higher during periods when observers were away. Furthermore, leopards were seen most frequently in the two days after researchers returned to the site, and sightings also occurred later in the field season.

Isbell and Young’s research suggested that human presence was changing the predator’s behavior, and therefore the monkeys’ behavior indirectly. This isn’t too surprising since the vervets were habituated to human observers, but the leopards were not! Did the monkeys feel safer with humans around? Could they actively use their human entourage to protect themselves from predators? A follow-up study on samango monkeys (Cercopithecus mitis erythrarcus) suggested this was the case and that monkeys do realize that humans keep them safe. Katarzyna Nowak and colleagues studied samango monkeys in South Africa to test the “human shield effect.” Their experiment consisted of feeding groups of monkeys at two vertical feeding platforms of different heights and measured the amount of food eaten at each. What they found was that, when monkeys were accompanied by humans, they were more likely to forage at the ground level where they were at the greatest risk of predation. These results strongly suggested that the monkeys understood that researcher presence protected them from ground predators.

In a similar way, data from chimpanzees indicates that habituation impacts their hunting behavior. In a long-term study from 1982-1991, Craig Stanford observed that habituated chimpanzees at Gombe would exploit the fear of their unhabituated prey, red colobus monkeys. The unhabituated colobus fled from the scary humans that followed the habituated chimpanzees, and the wily chimpanzees took advantage of this behavior to flush the colobus out from hiding for an easy kill. Recently, in a study published in PLoS One, Catherine Hobaiter and colleagues reported on potentially altered hunting behavior in chimpanzees in the Budongo Forest of Uganda. The well-habituated Sonso chimpanzees primarily hunt black-and-white colobus monkeys, and high-ranking individuals monopolize prey carcasses. However, the recently-habituated Waibira chimpanzees hunt duiker, an ungulate prey that has never been observed in the Sonso chimpanzees’ diets. Furthermore, the Waibira communities’ hunting patterns resemble those observed shortly after the Sonso chimpanzees were habituated, and the low-ranking Waibira individuals are more likely to retain control over their prey. The authors suggest that the differences observed between the communities’ hunting behaviors may be a result of habituation. After all, the predation of colobus monkeys involves complex group coordination that may be disrupted by habituation.

If predator-prey dynamics are affected by habituation and observation, could other behaviors be disturbed too? So far the results are inconclusive. For example, Margaret Crofoot and colleagues directly compared observational data on capuchin monkeys on Barro Colorado Island, Panama to activity data collected via radio-telemetry. The radio-telemetry data provided information on location every 10 minutes. Calculating the distance moved over those time periods allowed Crofoot and colleagues to distinguish active time from static time. They found that the monkeys’ activity patterns did not differ between remote and direct methods.

However, this does not mean that monkeys behaved the same both with and without observers present. While the data on activity patterns may tell one story, there’s a lot more going on in the day-to-day behavior of most social primates. I don’t think we can fully explore this until we have more data from remote cameras to compare with direct observations. Ancedotal accounts of primate behavior, including my own, confirm that habituated primates recognize their familiar human followers and may adjust their behavior to them. The situation is comparable to the behavior exhibited by human participants when interacting with each other on reality TV shows. Most people report an initial heightened awareness, but say they get used to the cameras and begin to ignore them. However, as most of us can infer from the behavior we see on reality TV, that claim is unlikely to be reliable.

Spider monkey feeding in a tree. Photo by author.

In my own research with spider monkeys, I’ve recognized that I can only follow the fast-moving monkeys when they allow me to. I’ve watched them travel and then stop so they can wait for me to catch up. I’ve also watched subadult females play apparent “hide-and-seek” or “chase” games with me, where they will stay still until I find them, travel quickly, hide in the trees, and then move again once I’ve found them. I suspect that watched primates typically alter their behavior to accommodate their human observers, and thus behave differently than unwatched primates. However, these differences may be subtle, particularly for well-habituated primates. Hopefully, research incorporating new technologies can better explore these differences, and determine how watched primates differ. Until then, I think it’s best to infer watched primates do change their behavior in response to observation—and we need to keep this in mind when evaluating evolutionary hypotheses based on their behavior.

References

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(3), 475–480.

Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior. Cambridge: Bellknap Press.

Hobaiter, C., Samuni, L., Mullins, C., Akankwasa, W. J., & Zuberbühler, K. (2017). Variation in hunting behaviour in neighbouring chimpanzee communities in the Budongo forest, Uganda. PLoS ONE, 12(6), 1–17.

Isbell, LA, Young T. (1993). Human presence reduces predation in free-ranging vervet monkey population in Kenya. Animal Behavior, 45, 1233–1235.

Nowak, K., Le Roux, A., Richards, S. A., Scheijen, C. P. J., & Hill, R. A. (2014). Human observers impact habituated samango monkeys’ perceived landscape of fear. Behavioral Ecology, 25(5), 1199–1204.

Stanford, C.B. (2001). Chimpanzees and Red Colobus: The Ecology of Predator and Prey. Cambridge: Harvard University Press.

Published On: May 17, 2018

Michelle Rodrigues

Michelle Rodrigues

Michelle A. Rodrigues is a Postdoctoral Fellow with the Beckman Institute and the Department of Anthropology at University of Illinois.

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