Download Arboreal and Terrestrial Foraging Preferences in New World and

Arboreal and Terrestrial Foraging Preferences in
New World and Old World monkeys:
An Experimental Investigation
Samantha Elias
Natan Gervais
Stephen Lu
Mara Mathieu
James Wang
Anika Wikramanayake
Research in Ecology
University of Miami
Abstract
We examined the foraging and sentinel behavior between a group of New World and Old World
semi-free ranging monkeys in a naturalistic environment. The group of Old World monkeys
were Long-tailed Macaques (Macaca fascicularis), and the group of New World monkeys was
comprised of Peruvian Squirrel Monkeys (Saimiri boliviensis peruviensis) and Black-capped
Capuchins (Cebus apella). We created an experimental foraging site for each of the groups of
monkeys, each with an arboreal and terrestrial component, and recorded the frequencies of
foraging behavior and sentinel behavior at each area for both groups of monkeys. We found that
the Old World monkeys fed significantly more frequently at the terrestrial area than the New
World monkeys. New World monkeys fed more at the arboreal area in the beginning of our
foraging trials, but once preferred food items were depleted, they descended to the terrestrial
foraging area. Old World monkeys performed more sentinel behavior than New World
monkeys, and we interpreted this as a result of subordinate monkeys monitoring the whereabouts
of dominant group members in a competitive feeding situation. When terrestrial feeding
increased in New World monkeys, terrestrial sentinel behavior also increased, possibly related to
increased vulnerability to potential predators. Our results confirmed that new and Old World
monkeys preferred to feed at sites that matched their habitat preferences in nature.
Introduction
Many species of nonhuman primates have generalized diets and feed on fruits, leafs, and
insects and are therefore described as omnivores. Foraging, searching for food and feeding, is an
important and time-consuming behavior and frequently accounts for over 50 percent of
nonhuman primates waking activities (Strier 2007). Our experiment studies the foraging
behavior of monkeys.
There are two types of monkeys, Old World monkeys and New World monkeys. Old
World monkeys come from Africa and Asia. New World monkeys come from Central and South
America. New World monkeys have nostrils that are farther apart and point outwards and Old
World monkeys have nostrils that are closer together and point downward. Old World monkeys
have more pronounced sexual dimorphism and the males are frequently larger than the females
and have bigger canines. All New World monkeys are arboreal whereas Old World monkeys
can be terrestrial or arboreal.
The subjects of our investigation were two species of New World monkeys (Peruvian
Squirrel Monkeys [Saimiri boliviensis peruviensis] and Black-capped Capuchins [Cebus apella])
and one species of Old World monkey (Long-tailed Macaques [Macaca fascicularis]). The
Long-tailed Macaques were the largest monkeys and the squirrel monkeys were the smallest
(Rowe 1996). In nature, squirrel monkeys and balck-capped capuchins are almost exclusively
arboreal and rarely descend onto the forest floor (Boinksi 1987, Mitchell et. al 1991, Rowe 1996)
whereas the Long-tailed Macaques are found in both the canopy and the ground and are often
described as semi-terrestrial and spend time both in the trees and on the ground (DeRuiter 1994).
All three species are quadrupeds with good climbing abilities; Black-capped Capuchins have
prehensile tails (Youlatos 1999). All three species live in reasonably large mixed male and
female groups along with juveniles and infants.
Depending on the habitat and the height in the canopy where the monkeys live, monkeys
may either spend most of their time foraging in the trees (arboreally) or on the ground
(terrestrially). Factors that may be important in determining where a species of monkey forages
include their natural habitat, size of the monkey, and presence of predators.
Our problem statement was “what are the foraging location preferences between New
World monkeys and Old World monkeys?” The null hypothesis for this problem statement was
there is no difference between the foraging location preferences between New World monkeys
and Old World monkeys. The alternative hypothesis was there is a difference between the
foraging location preferences between New World monkeys and Old World monkeys. Based on
their natural history, we predicted that there would be a difference in the foraging location
preferences between New World monkeys and Old World monkeys. Specifically, since all New
World monkeys are arboreal and the Old World monkeys we studied, the Long-tailed Macaques,
spend time in the canopy and on the ground, we predicted that New World monkeys would show
less ground foraging than the Old World monkeys.
The risk of predation strongly influences the behavior of primates (Gursky and Nekaris
2007). Since we were examining foraging behavior in two different groups of monkeys that live
in two different habitats, we were interested in studying if one habitat seemed more risky to the
monkeys. Consequently we recorded sentinel behavior at both foraging locations with our null
hypothesis being that there would be no differences in the amount of sentinel behavior performed
at either foraging location.
Methods
Location of the experiments
Monkey Jungle is located in southwest Miami Dade, Florida. Of particular interest are
two enclosures containing semi-free troops of monkeys in semi-natural habitats. The larger
enclosure, the macaque enclosure is 2.46 hectares and the smaller rainforest enclosure is 1.45
hectares. Both enclosures contain forests known as hammocks, which consist of neotropical
hardwood trees of Caribbean origin. The hammock in the rainforest enclosure has been
supplemented with exotic plantings including fruit trees, palms, and shrubs transplanted from
Iquitos, Peru. The two enclosures are very naturalistic with complex supports including lianas
and resemble the habitats the monkeys occupy in nature. The enclosures are both surrounded by
a two-meter high electrified fence and there is a cleared area of approximately four meters
between the fence and the edge of the forest. In the rainforest enclosure, there are a series of
trails that allow visitors to hand feed the New World monkeys. Native wildlife (for example
raccoons and snakes) lives in both enclosures, and aerial predators (most likely hawks) have
been observed carrying juvenile squirrel monkeys out of the rainforest enclosure (Evans,
personal communication).
Subjects
Approximately 75 squirrel monkeys and five Black-capped Capuchins live in the
rainforest enclosure, and about 125 Long-tailed Macaques live in the macaque enclosure. All of
these monkeys were born and raised in captivity and are habituated to humans. The macaques
and the squirrel monkeys live in reasonably large male/female groups together with juveniles and
infants. The capuchin group contains only adult females. The Long-tailed Macaques are the
largest species (adult male weight 2.5-6.7 kg and adult female weight 4.7-8.3 kg), the squirrel
monkeys the smallest (adult male weight 0.9-1.9 kg and adult female weight 0.7-0.9 kg) with
male capuchins weighing between 3.3-4.8 kg and female capuchins weighing between 1.3-3.4 kg
(Rowe 1996). The monkeys can range freely in their enclosures. They are provisioned three
times a day to accompany educational presentations for park visitors and first thing in the
morning in the rainforest enclosure and at special feeding sites (hoppers) in the macaque
enclosure.
Location of Experimental Feeding Sites
There were a number of factors that we took into account when we selected the locations
for the experimental foraging sites. The sites had to be easily accessible to the experimental
observers; the arboreal sites had to have branches sufficiently strong to support the containers
and the weight of the adult monkeys; the terrestrial sites had to have enough exposed roots
and/or trunks to which to attach the foraging containers; and finally there had to be enough space
and with good visibility to accommodate the team of 10 observers. The experimental foraging
site in the macaque enclosure was easily accessible from the perimeter pathway. We searched
for a place that the monkeys would visit frequently and chose a site near the west hopper (a
feeding dispenser from which they feed every day). In the rainforest enclosure, we selected a
site adjacent to a trail and located in an area park visitors regularly feed the monkeys. For an
aerial view of the enclosure and experimental site locations, see Figure 1.
Scheduling of the Experiments
The experiments were performed twice each day; the first was performed in the early
morning (between 0900h and 1100h) and the second in the late morning/early afternoon
(between 1100h and 1300h). These times were selected to avoid any conflict with the visitor
feeding presentations that occur at Monkey Jungle throughout the day. Experiments were
conducted three times a week over a three-week period in June/July 2010.
Experimental Procedure
To create each experimental foraging site, we attached 10 hard plastic containers to the
natural vegetation at each site to simulate a high quality food patch. Five containers were
attached to roots or the base of trees on the ground (terrestrial foraging area) and the other five
were placed in the canopy on trunks or limbs of trees (arboreal foraging area). Holes were bored
into the sides of the containers so that they could be secured to the trees and roots. We made
sure the foraing containers were stable and secure enough so that curious monkeys would not tip
them over or pull them off the trees. In the macaque enclosure, the arboreal foraging containers
were attached to the trees at a mean height of 146 cm with a mean distance of 177 cm between
them. In the rainforest enclosure the foraging containers were attached at a mean height of 170m
and a mean distance of 174 cm between them. The containers were filled with approximately
750 cm3 of assorted foods from the monkeys’ normal diet at Monkey Jungle, which included
mixed fruits and vegetables and commercial monkey chow. The food for each container was
carried into the enclosures in a plastic bag so that the containers could be filled quickly at the
start of each experimental trial (it took approximately 40 seconds to fill all of the containers).
For each experimental trial, we recorded the frequency of three foraging aspects (monkeys
approaching the containers within one meter from any direction, monkeys touching the
containers, and monkeys feeding from the container) and sentinel behavior onto time-ruled (30
second interval) check sheets for an observation period of 20 minutes. Because we were not able
to identify individual monkeys in either enclosure, the frequency of each behavior was recorded,
not the number of monkeys performing each behavior. Sentinel behavior was defined as
scanning the area and emitting alarm calls. Two people were responsible for collecting
frequencies of each behavior; one collected the behavior for the arboreal foraging area and the
other at the terrestrial area. Running notes were made of any unusual behavior. We did not
conduct inter-observer reliability tests (Martin and Bateson 1993).
After each experimental trial, containers were removed to prevent monkeys from tearing
them off. We tied zip ties around branches (or trunks or roots) to mark a site of attachment of
the containers (for the duration of our experiments) and placed zip ties through the holes in the
containers and tied these to or near the zip ties on the branches and roots. The location of the
foraging containers was therefore the same throughout the trials.
If monkeys were not present by the time we had completed our experimental set up, an
attempt was made to lure them to the site. If after 10 minutes no monkeys appeared, the trial was
abandoned. The 20-minute trials were terminated early if there was a complete absence of any
monkeys at both the terrestrial and arboreal areas for three consecutive minutes or if all the food
was consumed from the foraging container at either the arboreal or terrestrial foraging areas.
Data analysis
When data collection was completed, we tallied the total frequency for each of the four
behaviors (approaching a container within one meter, touching a container, feeding from a
container, and sentinel behavior) in each area (arboreal and terrestrial) for the first and second
half of each experimental trial separately. We combined these total frequencies for an overall
total for that particular experimental trial. We then calculated the proportion of terrestrial
foraging for each of the four behaviors.
Data were analyzed using the Mann-Whitney U test. All data were analyzed using
SYSTAT 12.
Results
We conducted 10 trials for the New World monkeys, and 12 trials for the Old World
monkeys, two of which were abandoned because no monkeys were present within 10 minutes of
the experimental set-up. We therefore had data from 10 trials for each experimental site. One
New World monkey trial was cut short because there was no more food in the arboreal foraging
containers, and one Old World monkey trial was cut short because there was a 3-minute absence
of monkeys.
Foraging Behavior
When we compared the proportion of ground foraging behaviors between the New World
and Old World monkeys we found a difference between the feeding frequencies (Mann Whitney
U test, p=0.004), but no differences for approaching within one meter or touching (MWU,
p=0.821 and p=0.345, respectively; Figure 2). The Old World monkeys fed more frequently on
the ground than the New World monkeys did; however, New World and Old World monkeys
approached within one meter of and touched the food containers on the ground with
proportionally the same frequency as did the Old World monkeys. Therefore, we rejected the
null hypothesis for feeding behavior, but failed to reject the null hypothesis for the other two
foraging behaviors. We noted that New World monkeys were more hesitant to feed on the
ground in the first half than in the second half of the trial, so to determine when the greatest
difference between New World and Old World ground feeding was, we compared feeding
between Old World and New World monkeys for the first half and for the second half of the
trials. There was a significant difference in ground feeding between old and New World
monkeys for the first half of trials, but not for the second half (MWU, p=0.000 and p=0.07,
respectively; Figure 3).
Although significantly less than Old World monkeys, the proportion of New World
monkeys foraging on the ground was higher than we expected. As a result, we examined
whether the feeding preferences changed over time and consequently, we compared the
proportion of foraging behaviors between the first half and the second half of the foraging trials.
We found that the New World monkeys fed proportionally more on the ground in the second half
than in the first half of the trial (MWU, p=0.002; Figure 4a). There was no difference in
proportion of ground feeding in the Old World monkeys between the first and second half of the
trial (MWU, p=0.821; Figure 4b). There were no other differences detected for any other
foraging behavior in either the new or Old World monkeys.
When we reviewed our notes, it was very striking that intraspecific aggression was
observed only in the Old World monkeys. We observed intraspecific aggression in 70 percent of
the Old World monkey foraging trials. In the New World monkeys, there was no aggression
between conspecifics, but we often noted interspecific displacement, and the squirrel monkeys
would leave the foraging container if a capuchin approached (60 per cent of trials).
Sentinel Behavior
There was a significant difference in terrestrial sentinel behavior between New World
and Old World monkeys (MWU, p=0.003; Figure 5). A more detailed analysis of the sentinel
behavior revealed one other difference – a comparisons between the first half and second half of
the trails for New World monkeys revealed that there was a difference in sentinel behavior (U=5,
p=0.001, df=1; Figure 6), with New World monkeys performing more sentinel behavior while
feeding on the ground. A similar comparison between the first half and the second half of the
trails for the Old World monkeys revealed no difference.
Discussion
This is the first experimental investigation comparing foraging preferences between
terrestrial and arboreal foraging sites between new and Old World monkeys. The semi-natural
enclosures at Monkey Jungle together with the well-habituated monkey groups made this an
ideal location for this type of investigation. A field experiment investigation of predator
sensitive foraging in squirrel monkeys in covered and open areas in Eastern Amazonia found that
squirrel monkeys visited their experimental foraging sites on only seven out of a potential 39
trials (Stone 2007) whereas monkeys visited our experimental sites on 22 out of 24 of the trials.
Foraging Behavior
Both Old World and New World monkeys approached, touched, and fed from the
containers. Therefore, our foraging sites were easily located and exploited by the monkeys. Of
all the measures of foraging behavior, we detected a significant difference in the feeding
behavior only between the New World and the Old World monkeys. There was more terrestrial
feeding behavior in the Old World monkeys compared to the New World monkeys. This can be
explained because New World monkeys are exclusively arboreal and the Old World monkeys we
studied are semi-terrestrial.
However, the amount of New World monkey terrestrial feeding was more than we
expected since New World monkeys are exclusively arboreal and the two species we studied are
reasonably small-bodied. We considered that the New World monkeys would be less likely to
descend to the ground because of their potential increased vulnerability to predators. Largebodied cats can climb trees but are too heavy to reach outermost branches and will in general
have restricted mobility (Ferrari 2008), leaving these small-bodied species safer in the trees when
in their natural environment. One explanation for the increased amount of terrestrial feeding is
that these individuals are habituated to the rainforest enclosure, which is void of terrestrial
predators that they face in the wild (i.e., large felids and snakes that prey on monkeys).
The lack of difference in the proportion of terrestrial foraging between the first and
second half of the experimental trials with Old World monkeys demonstrates that there was no
habituation in Old World monkeys. That is, the Long-tailed Macaques were just as comfortable
foraging on the ground in the second half, as they were in the first half. While there was no
increase in the proportion of terrestrial foraging for approaching within a meter and touching in
the New World monkeys from the first half to the second, there was a difference in actually
consuming the food. One explanation for this is that the New World monkeys were wearier of
predators in the first half, and so more hesitant to feed in the ground containers. After some
time, they realized that there was no real danger of foraging on the ground. An alternate, more
realistic explanation is that New World monkeys preferred feeding at the arboreal foraging area,
but moved to the terrestrial foraging area once the preferred food items in the arboreal containers
were depleted. We consider this explanation likely because we terminated one of our New
World monkey foraging trials when all of the food in the arboreal containers was consumed after
12 minutes.
Sentinel Behavior
The sentinel behaviors we recorded were warning calls and scanning. There was a
significant difference in Old World (Long-tailed Macaques) and New World monkeys (squirrel
monkeys and capuchins) for sentinel behavior. Due to the size variation between old and New
World monkeys, we did not expect to find that Old World monkeys would have more sentinel
behavior than New World monkeys since New World monkeys are not adapted for ground
foraging, while Old World monkeys are. One explanation for the unexpected results is that Old
World monkeys are competitive feeders. Competitive feeding occurs in Long-tailed Macaque
society because of their marked dominance hierarchy. The dominant male and female in a troop
have first choice of food. During our trials, there was no competitive food aggression observed
among the New World monkeys, however this was observed in 70 percent of the foraging trials
for the Old World monkeys. Certain Old World monkeys, including macaques, possess cheek
pouches (to store food) as an adaptation and these are used by subordinate monkeys in
competitive feeding situations. We interpret this result as suggesting that intraspecific feeding
competition in the Long-tailed Macaques was responsible for the unexpectedly high frequency of
sentinel behavior. The subordinate macaques (most likely juveniles) were monitoring more
dominant members of their own social group and not necessarily predators.
Interestingly, when we looked at the second half of the foraging trials for the New World
monkeys, the increase in feeding on the ground was accompanied by an increase in sentinel
behavior. This corresponding increase suggests that the New World monkeys were more wary
on the ground and demonstrates support for arboreal monkeys showing more surveillance for
predators when foraging on the ground. However, as we did not record the number of monkeys
present at each site we cannot eliminate the possibility that there were more New World
monkeys feeding on the ground in the second half and the increase in the number of monkeys
was the reason for the corresponding increase in the sentinel behavior. No comparable
difference was detected for the Old World monkeys.
We succeeded in designing and creating experimental foraging sites that were visited
regularly by our subjects and allowed us to address our problem statement. The foraging site in
the rainforest enclosure was very successful, in particular, the arboreal foraging area. Monkeys
visited this area on all trials, and the squirrel monkeys in particular were observed in small
subgroups foraging harmoniously. One of the educational presentations at Monkey Jungle
involves feeding the rainforest monkeys while visitors watch; consequently, we made a
recommendation to Monkey Jungle that they consider setting up multiple feeding sites
resembling our set up as the overall effect we created was very naturalistic foraging in the trees.
Literature Cited
Boinski S. 1987. Habitat use by squirrel monkeys (Saimiri oerstedi) in Costa Rica. Folia
Primatol 49(3-4): 151-67
De Reiter, J. 1994. Behavior and genes in natural populations of Long-tailed Macaques (Macaca
fascicularis). Ph.D. thesis Utrecht University, Netherlands
Ferrari, S. 2009. Predation risk and anti-predator strategies in South American primates. Edited
by Garber, P A, Estrada, A, Bica Marques, J C, Heyman, E W, and Strier, K B. Springer, New
York, NY, pp. 251-271.
Gursky, S. L. and Nekaris K. A. R. 2007. Primate anti-predator strategies. Springer, New York,
NY.
Martin P and Bateson P. 1994. Measuring Behavior University of Cambridge Press, Cambridge,
UK.
Mitchell C. L., Boinski S., van Schaik C. P. 1991. Competitive regimes and female bonding in
two species of squirrel monkeys (Saimiri oerstedi and S. sciureus). Behav Ecol Sociobiol 28(1):
55-60.
Rowe N. 1996. The pictorial guide to the living primates. East Hampton (NY): Pogonias Press.
Strier, K. B. 2007. Primate Behavioral Ecology. Allyn and Bacon, Boston.
Stone, A L. 2007. Age and seasonal effects on predator sensitive foraging in squirrel monkeys
(Saimiri sciureus). American Journal of Primatology, 69, pp 127-141.
Youlatos D. 1999. Tail-use in capuchin monkeys. Neotropical Primates 7(1): 16-20.
Figures
Rainforest enclosure Macaque enclosure Figure 4. Proportion of foraging behaviors on ground in a) New World and Old World monkeys in first and second half of the trials (mean ± SEM). *p < 0.05