Behavioural Interactions between Humans and Monkeys
Dr Sarah Papworth, Royal Holloway
A Talk to the Berkshire Mammal Group 7 December 2017
Sarah, a senior lecturer in Conservation Biology at Royal Holloway, was introduced as interested in the effects of human decisions and behaviour in complex ecosystems, and particularly having studied hunting in the tropics for her PhD. Indeed, she had been undertaking fieldwork in the Amazon basin when originally approached to give this talk! She explained that she would look at contact between the many species of monkey found in Amazonia, and humans – hunters, researchers and eco-tourists. She would focus on changes in behaviour and note their implications for conservation.
Turning to the map of South America to set her work in geographical context, Sarah explained that despite the great swathe of bright green, there was considerable diversity of habitat in Amazonia; it wasn’t just lowland moist forest as the colouring indicated. In Ecuador, the locus of much of her research, the forest is ‘terra ferme’ – dry underfoot despite year-round rainfall – while where she works in neighbouring Peru the forest is seasonally flooded. In these flooded forests, there is heavy rainfall for four months of the year, the level of which varies with El Nino and other climatic determinants. It is sufficiently pronounced that the high-water mark remains visible on the trees throughout the year – conspicuously above head-height. In both types of forests it remains dark beneath the canopy.
The human population of the forest was once more numerous, explorers originally entering Amazonia from over the Andes and finding elaborate communities based on cultivation. It was decimated in colonial times, by the effects of conquest and small pox, and is now smaller and more dispersed. Even the towns can be isolated. Sarah shared pictures of Iquitos in Peru, the largest town without access by road. To reach it one has to travel by boat or aeroplane.
But Sarah’s interest was in how humans and primates interact, and in the forest hunting is very much part of the indigenous people’s daily experience. They hunt deer, peccary and tapir, but monkeys – large bodied and apparently very tasty – are favoured. Monkeys are also kept as pets and even, on occasion, breast-fed. A favoured tactic is to kill a mother for food and retain her infant as a pet. Indeed, such pets can become almost surrogate babies. Traditionally monkeys feature in story-telling and animist culture, while more recently, they have become the object of eco-tourism and scientific research.
A PhD in Ethnobiology
“Ethnobiology is the scientific study of dynamic relationships between people, biota and environment”
To pursue her interest, Sarah had planned to undertake research for her PhD in West Africa, but civil war intervened and she was forced to find an alternative location. She simply googled ‘field sites with monkeys’! Ecuador was a clear option. Consulting the literature of the more specialised branch of knowledge, Ethnoprimatology, she was advised to start with indigenous societies for which monkeys are an important element of diet. Ecuador matched the criteria perfectly.
Her research was largely to be conducted in Yasuni National Park, where around 2000 Waorani live in a reservation the size of Wales. The Waorani’s first peaceful contact with the outside world was as late as the 1950s. Apparently, they had previously considered strangers to be ‘carnivorous ghosts’ and, feeling threatened, killed the occasional intruder in selfdefence. As a consequence, they acquired a fearsome reputation. However, when Sarah first went to Ecuador in 2009, many had settled in villages, maintaining neighbourly relations, though 500 or so still live in isolated groups in the forest.
The Waorani are notable as monkey hunters. Traditionally they hunted monkeys using toxins from the poison arrow frog to treat their blowpipe darts. These would be nicked so the tip would break off if the monkey tried to remove the dart from its body. A hunter would stand below a group of monkeys and blow the pipe. Once a monkey was hit, it would be paralysed by the poison and could be retrieved and killed.
Monkeys There are 11 species of monkey in Yasuni, including the Capuchin, Howler and Owl monkey, Saddleback tamarin, Saki, Squirrel, Spider, Titi and Woolly monkey. The locals identify three types of ‘night monkey’, rather to Sarah’s initial confusion, but two (the arboreal Olingo and Kinkajou) are not actually primates, despite having grasping hands. None-the-less, these and the Owl monkey form a coherent ethno-taxonomic group, however defined by science.
Early on, Sarah surveyed the culturally salient species, those that were repeatedly named as important. First, and conspicuously the most important, was the Woolly monkey, followed by deer and peccaries, then the Spider monkey, several other creatures and the Howler monkey. It would seem that monkeys were not, per se, more significant than other types of animal, but their value varied according to species.
Ref: Papworth et al (2013) ‘The natural place to begin’
The reaction of primates to predation
There is scholarly debate on the long-term impact of hunting. While it clearly is disastrous for the individual animals concerned, hunting does result in habitat protection. (Richard Bodmer et al (2008), chapt 8: ’Wildlife and Society’). However, Zuberbuhler argues that human activity is too recent to be evolutionarily relevant.
Nonetheless, humans are highly effective hunters, especially with (silent) blow pipes, with which entire groups of monkeys can be killed on one expedition, rather than (noisy and disruptive) guns, which, after the first death, alarm the other monkeys and drive them away.
How do primates reactions to predation? Sarah turned to the example of monkeys in Africa. In the case of an approach by an ambush predator, such as a leopard, the male descends to attack and draw attention while the females and infants climb to safety. In the case of an eagle, threatening them from above, the monkeys descend from the canopy to seek protection below. Likewise, monkeys need to react quickly to predators. Sarah referred to the example of Howler monkeys in Panama whose experience of the Harpy eagle was minimal. When the eagles returned to the locality after an absence of 20 years, the unwary monkeys were tempted to approach them and thus became vulnerable to ambush. It took a period of only six months to adapt and learn to keep their distance.
Woolly monkeys’ response to hunting
The Woolley monkey: Lagothrix Lagothricha
Sarah’s research into defensive behaviour was based on Woolly monkeys. The Woolly monkey, she explained, lives in large groups, eats fruit, seeks and leaves, is about 7kg and has a prehensile tail. In gauging the likely response of Woolly monkeys to predators in Yasuni, Sarah anticipated they would resort to silence, low visibility and collective group behaviour, avoiding the attention drawn by individual responses.
Her investigation involved researchers dressing and behaving respectively as three categories of human, each representing what was assumed to be a decreasing level of threat: hunters, gatherers and researchers. It was expected that the monkeys would respond to hunters, and ignore the unthreatening behaviour of gatherers and researchers. The results supported the prediction, in that the appearance of hunters prompted the biggest reaction, but the monkeys also reacted to the presence of gatherers and researchers. It was thought that perhaps the intensity of observation by researchers might be interpreted by the monkeys as threatening, or perhaps their positioning below the monkeys emulated that of the hunters?
Ref: Papworth (2013) ‘Hunted Woolly monkeys’
To explore the possible impact of monkey caution toward researchers on the accuracy of population studies, Sarah’s research student Camila Blasi-Foglietti is currently undertaking research in West Africa, investigating how behaviour might lead to under-estimation of monkey populations in known hunting areas.
The impact of human presence
The work of Geffroy et al (2015) suggests that human presence and their feeding of animals leads to the habituation and emboldening of other species, and affects their reaction to predators. This might manifest itself in a couple of ways:
• Through selection prey species become bolder, therefore less fearful of, and more vulnerable to, the predator.
• The ‘human shield’ effect is whereby the predator becomes more wary of man, and so the prey becomes bolder as the threat to it diminishes
The evidence to support either hypothesis is inconclusive, so Sarah undertook research into the impact of (non-predatory) behaviour by both eco-tourists and researchers, based this time in Peru. In contrast to Ecuador, the sites in Peru were flooded forest. Moreover, the monkeys in the new research area were different from those in Ecuador: the Saki is different; there are two species of Spider monkey, not one; and the Owl monkey might be a different species.
Proximity – Capuchin monkeys’ response to researchers
The test species was the Large-headed Brown Capuchin, a placid species, unlike the more aggressive White-fronted Capuchin. Taxonomical designation is fluid, but the latest Latin designation (checked, we were assured, that very morning) is Sapajus macrocephalus. The Capuchin is cat-sized and frugivorous / insectivorous – though some have been known to eat infant tamarins. They live in mixed groups of 15 to 20 individuals and associate with the Squirrel monkey (which lives in groups of up to 100), though the basis of their symbiosis is unclear.
This past summer’s research (2017) suggests that proximity to humans is not correlated with vigilance, and graphs were displayed to illustrate the point. Are humans acting as a shield? It is not yet clear, but Sarah did relay an anecdote in which a Harpy eagle was present, indeed very close to the researchers, but did not attack the monkeys. However, at present, the results of this research are merely preliminary.
Noise – Pygmy marmosets’ reaction to eco-tourists
Pygmy marmoset, Yasuni National Park 2010
The Pygmy marmoset is the world’s smallest monkey. They live in family groups and, unusually, pairs have twins twice a year. The parents are aided by their sub-adult offspring, who thereby gain parenting experience in anticipation of having families of their own. Pygmy marmosets are gum specialists, boring holes in clusters of three or so trees that constitute their home area, and rarely straying far. Because of this constraint they are easily observed and can be counted with reasonable reliability.
How do they respond to eco-tourists, whose presence is brief and irregular, unlike researchers who tend to stay in the locality for a period of several months?
The continuing presence of marmosets is good for tourism, and reflects well on the marmoset’s life experience. But what about the noise tourists are apt to make? Surprisingly there is no evidence in the literature. Sarah’s research relied on playing recordings of human speech to the marmosets, varying in volume from whispering and talking to shouting, and for both short and long durations. In a rather picturesque detail, Sarah explained that because the forest was flooded, the recording equipment and speaker were mounted in a canoe!
The results indicated, perhaps unsurprisingly, that the Marmosets ignored quiet or conversational voices, but ran away if they heard shouting. The median time elapsing before return was five minutes. Results were plotted at 30 dB, 60 dB ad 78 dB – the monkeys’ reaction doubling in intensity between the latter two levels. It was clearly the volume, rather than the presence of humans that was disturbing them. Sarah’s conclusion: don’t shout at monkeys! This, though seemingly obvious (on her own admission), will be used to reinforce the advice given at the education centres associated with eco-tourism.
A lively discussion followed, both in the form of questions from the floor and informal discussion after Sarah had been thanked for an engaging talk on a very interesting topic.
What is the size of monkey population and has it declined over the years? The population is not quantified in absolute terms, but from modelling it doesn’t appear to have declined in recent years, and with such a small human population, hunting is maintained at a sustainable level.
Is hunting practiced by both the sedentary and forest-dwelling Waoroni? Yes, as far as is known. Certainly, the sedentary Waoroni continue to hunt.
What proportion of Waoroni diet is accounted for by hunting? Actually, around 50% of protein is from fish. Fishing is popular because it is a sociable rather than silent activity. There is also some traditional shifting agriculture within the forest.
Are monkeys alarmed just by the volume of speech, or does the difference between languages play a part? This is very much of interest, but yet to be tested. (The Waoroni, incidentally, mostly speak Spanish, or are bilingual; Sarah has learned Spanish though not Waoroni)
Is it the props (the blowpipes) or behaviour of hunters that the monkeys react to? Not clear, but more probably the latter. This would explain why the positioning and intense observation by researchers – which mirrors that of hunters – also causes alarm.
Edwin A.R. Trout Berkshire Mammal Group