Sarah Papworth woolly monkey 2
Lagothrix poeppigii, Yasuní National Park. Reproduced with permission from Sarah Papworth

In the soft jungle sun, a thick-limbed primate—with heavy fur and a strong grasping tail—is poised for flight.  This is Lagothrix poeppigii, or Poeppigi’s woolly monkey, and it is the largest arboreal primate in this forest.  A sudden movement below it has just caught its eye.  Softly, a Waorani hunter emerges from the undergrowth, his blow-pipe in hand.  The monkey freezes, as the forest goes silent.  Over the next thirty minutes, it remains unnaturally quiet.

In another part of the forest later that day, a group of four woolly monkeys have gathered to socialise.  They are relaxed, uttering a range of graded vocalisations to each other as they groom.  Beneath them, the bushes part and a research scientist steps forward, binoculars and notebook in hand.  They glance down at him, curious.  In a few moments, they move on to the next feeding tree.

In the brush nearby, Sarah Papworth, a research fellow at the National University of Singapore, has acute pins and needles in her legs.  She is an undercover observer of the woolly monkeys today, and has been squatting in hiding for nearly an hour now.  Both the “Waorani hunter” and the “researcher” are the same person—one of Sarah’s two field assistants—dressed and acting the part.  During both encounters, Sarah has braved ants, insect bites and chronic inertia to record the reactions of the woolly monkeys to three characters – a hunter, a gatherer, and a field researcher.

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Sarah is interested in a number of questions: Will the monkeys treat the human as a potential predator? Will they respond by fleeing? Or does it benefit them more to mob the predator, drawing every other animal’s attention to its presence? Most importantly, do they modulate their reactions based on the type of human they see?

To find answers to these questions, Sarah has spent ten months with unhabituated woolly monkeys in the steamy Ecuadorian rainforests of Yasuní National Park. She conducted her experiments on woolly monkey reactions to perceived human threats at two sites—Yasuní Research Station, with high hunting pressure (the HP site), and Tiputini Biodiversity Station, with lower hunting pressure (the LP site). Her results were published recently in the journal PlosOne.

Oxbow lake, Yasuní National Park. Photo credit: Geoff Gallice on Wikimedia Commons
Figure 1. Locations of experiments at the LP and HP sites. show more One experiment of each type (hunter, gatherer and researcher) was conducted in each of the experimental areas used at the two sites (HP site = high hunting pressure, Yasuní Research Centre; LP site = low hunting pressure, Tiptutini Biodiversity Station).
Figure 1. (Papworth et al. 2013) Locations of experiments at the LP and HP sites.
One experiment of each type (hunter, gatherer and researcher) was conducted in each of the experimental areas used at the two sites (HP site = high hunting pressure, Yasuní Research Centre; LP site = low hunting pressure, Tiptutini Biodiversity Station).

 

She chose to work with the woolly monkeys because they are hunted fairly heavily—over 200 animals are extracted from an area of 800 km² of forest at the HP site per year.  They gather in large social groups that fission into smaller foraging groups of ca 9 individuals.  Each animal weighs ~ 6.1 kg (or 13.4 lbs), making it a sizeable catch for a hunter.  While the Waorani traditionally hunted with spears and blowpipes—all males over 18 typically go hunting—they are transitioning to guns and dogs today.  They have a subsistence economy, supplementing hunted food items with small-scale farming and gathering.  The monkeys in the area are no strangers to researchers either—several long term projects have been conducted at both sites, including some of the most comprehensive research studies on woolly monkey ecology today (by Dr. Tony DiFiore and colleagues).

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Sarah then set up three experimental conditions – the hunter, gatherer and researcher (see table below).  Each individual exhibited behaviours typical of their character, and also carried equipment to substantiate their roles.  For example, while the hunter carried a blowpipe or dart quiver, the researcher carried a small notebook, bag, binoculars or a video camera.

Table 1. Human behaviour associated with each experimental condition.
Table 1.  (Papworth et al. 2013) Human behaviour associated with each experimental condition.

Previous research has revealed that the degree of the perceived threat has an effect on prey responses.  For instance, elephants react aggressively to an individual in red clothing, and to the smell of clothing worn by a Maasai hunter, when compared to evidence presented to them of an ethnic group that does not hunt elephants.

Primates typically have two options when faced with a predator: alarm calling (usually accompanied by movement away from the predator), or a cryptic response (an attempt to be quiet and inconspicuous) that draws less attention to themselves.  Scientists reason that since excessive hunting by humans is a recent development, primates likely have not had a chance to evolve an adaptation to predation that has been selected over time.  Instead, Sarah believes, they are likely to adopt “socially learned threat-sensitive predator responses.”

Anti-predator responses can be costly—fleeing, alarm calling, and desisting from feeding are high-energy and disruptive behaviours.  Therefore, if a human’s intentions are NOT to predate upon them, it would benefit the monkeys to be able to detect it and avoid a costly display.  If the woolly monkeys can detect different “types” of humans, and thus discern their intentions, they can modulate their anti-predator responses to remain energetically efficient overall.

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Sarah first spent three months on a pilot study before she was able to conduct her first “real” experiment.

“I was learning about the woolly monkeys, where to find them, what their calls sounded like …conducting the experiments took a long time, particularly in the hunted area where groups were much harder to find,” she says.

“There were times when we went 2 weeks without seeing a single woolly monkey.”

The monkeys’ general inquisitiveness also made it hard for her to collect data.  No sooner had her team hidden themselves in the brush than a monkey would appear right above them, and observe both the “character” and the “observer”—in effect, the monkeys spotted them before they spotted the monkeys!

“This led to a lot of aborted experiments, and is part of the reason we had so few experiments after 10 months,” she says. “The worst would be when we hadn’t seen monkeys for weeks (literally—on one occasion I remember we went out every day and didn’t see any woolly monkeys for 2 weeks).  You start to wonder why you’re doing it—trying to calculate how long it will take to do the minimum number of experiments.”

Nevertheless, her team persevered.  She successfully conducted 9 experiments (3 sets) at the LP site, and 12 at the HP site (4 sets), across 10 months of study.

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Lagothrix poeppigii vocalising, photo credit: Sarah Papworth

Results

The first thing Sarah and her colleagues discovered during her preliminary work at the site was that the monkeys took at a least 20 minutes to return to baseline behaviour after encountering a human.

During the main study period, she learned that when presented with hunters, woolly monkeys vocalised less in the 5 minutes immediately after the experiment began at both sites—this suggests a cryptic anti-predator response to hunters. On the other hand, there was no change in vocalisation upon observing a researcher at either site.  Their reactions to gatherers were mixed—their vocalisations increased at the LP site, but decreased at the HP site. This indicates that they were treating gatherers as possible predators only at the site with higher hunting pressure.

Sarah also noted long-term effects of the experiment on the monkeys, by recording their vocalisations 30 mins after the monkeys observed the first human subject.  These results are more complex to interpret.  The monkeys were quieter than baseline values after having seen a hunter in the forest, which is consistent with the idea that they can recognise human hunters as potential threats.  At the LP site, where researchers have sometimes used dart guns to anaesthetise woolly monkeys for the placement of radio collars on them, the monkeys were quieter than normal in response to researchers as well.  Even though they do not treat researchers as suspicious right after encountering them, their presence eventually does appear to make the animals wary.  Gatherers did not have any long-lasting effects on the monkeys at the LP site, where they are less likely to have been threatened by them; however, the monkeys did become wary of gatherers at the HP site.

Sarah also recorded changes in the distance traveled by the group after encountering humans in all three conditions.  As you can now imagine, the primates minimised their travel at both sites upon observing hunters; at the HP site, they also had this reaction to gatherers.  This is more evidence of a cryptic anti-predator response, since the movement of primates in the canopy is the easiest way for humans to track them.  Although fleeing the scene might seem like a good strategy, it generally succeeds in alerting humans below to the presence of a primate, rendering them more vulnerable to attack.

They did not alter the distance traveled after encountering a researcher at either the low or high hunting pressure sites.

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Woolly monkeys appear to modulate their vocalisations and movements upon encountering humans, which is a response one would expect given our knowledge of prey behaviour in response to any predator.  More remarkable is this team’s discovery that woolly monkeys have learned to distinguish between different behaviours exhibited by the same predator species—they are more wary of hunters and gatherers in general, than they are of researchers.  The monkeys have learned that the most effective response to a pursuit hunter is to appear cryptic.  This is particularly appropriate as such hunters are not likely to be deterred by other anti-predator strategies, such as mobbing.

At the HP site, the theory that the woolly monkeys are exhibiting threat sensitive predator responses is strongly supported—they display “a strong change in behaviour in response to more threatening humans.”  However, at the LP site, while they exhibited the predicted response toward hunters, they did not exhibit a noticeably weaker response to human researchers than human gatherers.  The authors suggest that this might be merely due to the fact that the monkeys at the LP site are not as experienced in dealing with intruders as are the monkeys at the HP site—this lack of experience again lends credence to the idea that woolly monkeys are learning anti-predator strategies as their habitats change around them.

“I definitely think that a cryptic response in primates is something that has been overlooked by previous research on primate anti-predator behaviour,” says Sarah. “This is partly due to the research focus of papers on investigating [primate] psychology and communication, rather than anti-predator behaviour per se.”

To her, beginning to regard humans as “legitimate parts of primate ecology and behaviour” is paramount.  As humans expand their habitat and increasingly encroach on that of other species, we are less likely to observe “natural” populations of primates.  Sarah suggests that we begin to “consider humans as part of animal systems, even in areas traditionally considered remote, like Yasuni National Park.”

Perhaps there is a lesson here for behavioural research in general—animals could be reading more into our behaviour than we think.

Sources:

Papworth S., Milner-Gulland E.J., Slocombe K. & Noë R. (2013). Hunted Woolly Monkeys (Lagothrix poeppigii) Show Threat-Sensitive Responses to Human Presence, PLoS ONE, 8 (4) e62000. DOI:

More on woolly monkey predation:

Yasuní National Park is sitting on a giant bed of oil, its future uncertain.

The ecology and behaviour of woolly monkeys is the focus of long-term research at the Yasuní research station, as are a variety of other projects on primates at this site.

For more information (and some stunning visuals) head to Arkive.

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