1. PSY 433 Primate Cognition – Final Paper John Suloman
How is primate perception mediated by feeding ecology?
Literature Review
Introduction
Primates are an order of animals with many diverse taxa. Across the diversity of the
primate group, many species differ from each other in the types of foods composing their diets
and the different strategies used to successfully acquire these foods. The type of, quantity of
and the sensory cues made available by foods typical of the diet for a given primate species can
be considered to be that species’ feeding ecology. An interesting research question then
becomes are there any differences in perceptual cognition across primate species resulting
from variation in their feeding ecology? Apart from social problems such as locating and
securing mates, food acquisition is likely the other major adaptive problem faced by primates
that has driven selection for an array of specialized perceptual capabilities. Thus, it is plausible
for research to inquire about the differences in perception between primate species that have
enabled them to pick up on specific sensory cues projected by foods relevant to their unique
feeding ecologies.
Since the evolution of stereoscopic vision is considered a defining characteristic of the
primate order and later the evolution of trichromatic (color) vision in higher primates, the
majority of scientific literature has focused on vision as the perceptual modality most valuable
to primates for successfully acquiring food. While visual perception is certainly used in some
way by all primates in their foraging behaviors, the following literature review focuses on other

2. perceptual modalities that appear to become important for primates based on specific aspects
of their feeding ecologies. This paper will examine two major trends, the presence of fruit and
the unavailability of visual cues, in primate feeding ecologies, and discuss how each of these
has mediating effects on the perceptions of foraging primates.
Foraging for Fruits
Available empirical evidence reveals some interesting trends about how the presence of
fruits in primates feeding ecologies may have some effects on which perceptions these
primates rely more heavily on during fruit foraging, and possibly on certain neuroanatomical
perceptual adaptations that aid successful foraging in primates with fruit-rich diets. Foremost,
articles converge on the idea that the sense of olfaction plays a key role for primates when
foraging for fruits (Nevo & Heymann, 2015; Rushmore et al., 2012; Laska et al., 2006; Dominy,
2004; Bicca-Marques & Garber, 2004).
Olfaction [sense of smell]
To understand why olfaction might be important for primates foraging for fruit, consider
the adaptive challenge that is being faced: the selection of ripe as opposed to unripe fruits.
Olfaction may aid in the selection of ripe fruits because when a fruit ripens, volatile chemicals
are released that produce fruity aromas detectable by the nose (Rushmore et al., 2012). Natural
selection has favored primates that select fruits of optimal ripeness because these fruits
contain the highest sugar and calorie concentrations, thus provide the highest fitness benefits.
Similarly, natural selection has favored the avoidance of unripe fruits because these fruits are
potentially harmful to the consumer due to the presence of plant-produced secondary

3. compounds such as tannins and alkaloids (Dominy, 2004; Rushmore et al., 2012). In the form of
comparative behavioral studies and studies on chemical ecology, the following articles provide
evidence that olfactory perception is an important sense for primate species encountering
fruits in their foraging ecologies.
In a study involving chemical and physical measurements of tropical fruits, Dominy
(2004) calculated the reflectance spectra, hardness, and ethanol concentrations of 14 different
Southeast Asian fruits and then calculated correlations of these factors to the fruits’ sugar
concentrations, i.e. their ripeness. Ethanol is a volatile chemical that produces a distinct odor.
The author found that the reflectance spectra (color) of fruits was not a reliable indicator of the
fruits’ sugar concentrations when integrated into the simulated color space of primates with
trichromatic vision. In contrast, concentrations of ethanol in fruits were found to be positively
correlated with fruits’ sugar concentrations. This result suggests that olfactory cues involved in
the quality-assessment stage of foraging for fruits may be a more reliable predictor of high
sugar contents than visual cues for foraging primates, and that ethanol is a chemical that relays
this information.
Laska and colleagues (2007) provide behavioral evidence for the idea that feeding
ecologies characterized by fruit foraging may drive primates to rely on olfactory perception in
foraging situations by comparing the highly frugivorous [fruit-eating] spider monkey to the
more omnivorous squirrel monkey. The researchers presented captive monkeys of each species
with familiar, experimentally modified, or completely novel food items and observed their
behavioral responses to each food type in order to assess which sensory cues the animals were
honing in on. It was observed that the frugivorous spider monkeys sniffed novel food items

4. significantly more often than the more omnivorous squirrel monkeys, indicating that olfaction is
heavily relied on by spider monkeys in their evaluation of unfamiliar foods. Although this study
did not create a very ecologically valid situation, the sniffing behavior of the spider monkeys
may reflect their natural tendencies to evaluate the quality of individual fruits using olfactory
perception.
In another comparative behavioral study, Rushmore and colleagues (2012) provide
more evidence of fruit-eating primates relying on olfactory perception for successful foraging of
fruits. Experimenters selected three different lemur groups from the Duke Lemur Center (North
Carolina): the folivorous [leaf-eating] Coquerel’s sifaka, two closely related species of
frugivorous ruffed lemurs, and the generalist feeding ring-tailed lemur, and tested the
hypothesis that the different feeding ecologies of these species might have an effect on the
type of perceptions used by them to complete a foraging task. Individual lemurs were
habituated to a Plexiglas ‘feeding box’ partitioned into two equal compartments, each
compartment containing one ripe or unripe piece of food. In experimental trials, compartments
of the feeding box were either transparent or opaque to allow/eliminate visual cues, contained
several holes on top or were solid to allow/eliminate olfactory cues, or were mixed to allow
only one cue per compartment. The lemurs were tested on their abilities to obtain the higher
quality foods (immature red leaves for sifakas, mature ripe fruits for ruffed and ring-tailed
lemurs), and their accompanying behaviors were observed to determine if there were any
species differences in their reliance on either visual or olfactory perception. It was observed
that frugivorous ruffed lemurs were able to select ripe fruits successfully using only olfactory
cues while the sifakas could not. Additionally, when presented with a ripe fruit in each

5. compartment and having both visual and olfactory cues available to them, ruffed lemurs sniffed
the compartments to inform their decision almost as much as they used vision. Although not
significant, this result is worth mentioning because it may reflect the finding by Dominy (2004)
that the olfactory perception of ethanol in fruits is likely a more reliable indicator of fruit quality
to foraging primates than the visual perception of color. Also worth noting is the observation
that generalist ring-tailed lemurs used either visual or olfactory cues alone to select the higher
quality foods above chance level. This result represents a clear example of the mediating effects
of a generalist feeding ecology because the ring-tailed lemur is able to successfully forage for
both fruits and plants by having both fairly acute senses of smell and vision.
There is also evidence that the effectiveness of olfactory perception is not limited to
primate species that are highly frugivorous. In species whose feeding ecologies involve foraging
of both fruits and invertebrates among other items, behavioral studies indicate that olfactory
perception is more useful in detecting fruity odors than the odors of invertebrates. A study by
Siemers et al. (2007) found that grey mouse lemurs (Microcebus murinus) in temporary
captivity were able to choose from two opaque containers the container holding a piece of
banana with nearly 100% success, using only olfactory cues detected from small slits in the top
of containers. However, when researchers placed live insects in the same type of containers,
only two out of five lemurs selected the insect-filled container above chance level, and this was
likely due to the additional acoustic information generated by insects made available to the
lemurs. Similarly, Nevo & Heymann (2015) review studies finding that capuchin monkeys could
not locate arthropod prey items in close proximity using only olfactory cues but could easily

6. locate hidden fruits, and likewise that capuchins have a more sensitive olfactory discrimination
mechanism for fruity odors than they do for fishy odors.
Available evidence suggests that primate species whose feeding ecologies are
characterized by some degree of fruit foraging may also have adapted some more sensitive
capabilities in the form of taste perception. It is important to make the distinction, however,
between the detection of fruits and the selection of fruits when considering the role of
olfaction in primate foraging. Due to the fact that odors travel through the air in very narrow
plumes, it is unlikely that primates actually detect fruits from a distance using their sense of
smell, rather it is likely that vision plays more of a major role in fruit detection from a distance
while olfaction is used for quality assessment of fruits already detected (Nevo & Heymann,
2015). While olfactory perception aids foraging primates in selecting ripe fruits, acute senses of
taste may supply primates with an ability to discriminate and learn small differences in sugar
content between ripe fruits, and therefore help decide which fruits are worth the time and
energy to forage.
Gustation [sense of taste]
In a study done by Laska et al. (1999) captive born spider monkeys and hamadryas
baboons were tested in their abilities to discriminate small differences in the sucrose
concentrations of two adjacent bottles of liquid. The researchers worked on the assumption
that the primates would prefer the solution with a higher sucrose concentration (as all primates
have done in previous similar studies), and used the consumption of two-thirds or more of one
solution in at least 80% of trials as the criterion for preference. It was found that frugivorous

7. spider monkeys exhibited remarkably low taste thresholds for sucrose across six reference
concentrations with thresholds being lower as sucrose reference concentrations went up. In
other words, the spider monkeys exhibited a proportionately better taste sensitivity with
solutions high in sucrose than solutions low in sucrose. This pattern may be a reflection of the
spider monkey’s feeding ecology because as a species that is primarily foraging for fruits that
have high sugar concentrations, a perceptual ability to discriminate subtle differences in sugars
between fruits would provide a huge adaptive advantage in the form of facilitating the selection
of the most sugary, high-quality items (Laska et al., 1999, 158). In an earlier study done by this
author, Laska observed that omnivorous squirrel monkeys exhibited an average taste threshold
for sucrose that was 20% higher than, thus less sensitive, to that of the fruit-eating spider
monkey in the current study (1994). Somewhat surprisingly, the current study observed that
the hamadryas baboons, whose diets consist of a general variety of fruits, plants, roots,
invertebrates and small vertebrates, displayed a taste threshold for sucrose almost as low as
the spider monkeys. However, the baboons taste perceptions were most acute at the lowest
reference concentrations of sucrose. This pattern may also reflect a mediating role of the
baboons’ specific feeding ecology, which involves foraging for plants low in soluble sugars
(Laska et al., 1999, 158). As such, baboons are at an advantage being informed by their taste to
decipher which plant foods have the most sugars, and most nutrition, out of the bunch.
A study of similar design conducted by Remis (2006) provides evidence that primate
species with different degrees of fruit consumption in their diets may also have different
degrees of taste perception for the chemical class called tannins, which are plant secondary
compounds known to inhibit digestion. The author conducted bottle preference tests with

8. captive chimpanzees and assessed the animals’ sensitivities to the presence of tannins
dissolved in solutions of fructose. These observations with chimpanzees were then compared
to equivalent data previously collected from captive gorillas. It was found that chimpanzees
overall consumed more liquids than gorillas containing low to mid tannin concentrations, but
gorillas consumed more liquids than chimps that had higher tannin concentrations. In other
words, chimpanzees did not tolerate the sweet solutions as much as gorillas once tannin
concentrations reached a certain percentage, and thus can be said to have more taste
sensitivity to tannin compounds than gorillas. This result again may reflect a difference
between species’ fruit consumption having a mediating effect on perception. It is likely that
gorillas exhibited a less sensitive taste perception of tannins than chimpanzees because gorillas
feed avidly on herbaceous plants having low-tannin concentrations, and thus can forage more
successfully by not perceiving, to a certain degree, the tannins they are consuming.
While it seems that fruit mediated perceptual differences in primate foraging strategies
are largely geared toward food quality assessment, the next major trend in the literature
suggests that perceptual differences mediated by foraging ecologies are geared to solve a more
general problem of food location and assessment.
Unavailability of Visual Cues
The absence of visual cues that would otherwise allow primates to forage successfully
for their preferred foods is the other major factor of primate feeding ecologies that may have
effects on their perception. This review has not touched on the huge amount of evidence in the
literature describing various adaptations of the primate visual perception system, but

9. nonetheless vision may be the most important perception for primates in completing the
challenge of successful foraging. This being said, a plausible research question asks how might
primate perceptual capabilities and the sensory cues they use for successful foraging be
affected by a feeding ecology characterized by a lack of visual cues?
In the absence of visual cues, studies have shown that foraging primates may tend to
rely more on olfactory and auditory perception. Primate species whose feeding ecologies are
most characterized by an unavailability of visual cues are probably those species who forage at
nighttime, i.e. those who are nocturnal. Therefore, a potentially powerful research design may
be one that compares the foraging-related perceptions of nocturnal and diurnal [active in the
daytime] species.
Nocturnal Foragers
A study done by Bicca-Marques and Garber (2004) is one of the few works to date to
investigate how nocturnal and diurnal primates might differ in their relative reliance of certain
sensory modalities in foraging. The researchers designed an experimental field study at a
Zoobotanical Park in Brazil which set up feeding stations in areas known to be frequented by a
group of nocturnal owl monkeys (Aotus), two groups of diurnal emperor tamarins, two groups
of saddle-back tamarins and one group of titi monkeys. The tamarin groups were all captured
and marked for identification while the other species were not. Each feeding station was
composed of eight feeding platforms arranged in a circle, with two out of the eight platforms
always containing a real banana and the other six platforms containing plastic sham bananas.
Researchers manipulated the sensory cues available to the primates by allowing only spatial

10. memory cues via repeated location of real bananas, only visual cues by placing all banana items
on top of leaves but concealing real bananas under the platforms of sham bananas, and only
olfactory cues by concealing all banana items but leaving the sham platforms without real
bananas underneath. All groups of monkeys successfully foraged for real bananas using spatial
memory cues. Similarly, all groups except one tamarin group successfully foraged above chance
level using only visual cues, including the owl monkeys when their inexperience with plastic
sham bananas was controlled for. However, it was found that only owl monkeys and one group
of tamarins could successfully locate the real bananas above chance level. This result suggests
that the nocturnal owl monkeys may have more sensitive olfactory perception than some
diurnal species, enabling them to forage for fruits in periods where light and visual cues are
limited.
While owl monkeys who are largely frugivorous may have heightened olfactory
perception for fruit-foraging at night, other more insectivorous species may rely more on
auditory perception to accomplish their foraging goals. Siemers et al. (2007) observed that the
fairly insectivorous grey mouse lemur used auditory cues in the form of recorded insect rustling
sounds in order to accurately pinpoint artificial prey dummies. These temporarily captive
lemurs were observed to respond very rapidly to audio playbacks of moth fluttering and
exhibited frequent bouts of rapid ear movements, indicating an active sampling of auditory
information by the animals. A follow-up study by Goerlitz & Siemers (2007) attempted to
answer the question of exactly how grey mouse lemurs use the auditory cues emitted by
insects in order to complete successful foraging. The researchers began by recording the
rustling sounds of various insects of Madagascar, and found that the amplitude (loudness) of

11. the rustling sounds were positively correlated with the insects’ mass. In an audio choice
experiment, the authors then presented temporarily captive mouse lemurs with simultaneous
playbacks of insect rustling noises of two different amplitudes. It was observed that the lemurs
responded more often to the audio playbacks with higher amplitudes. This result provides
evidence to the idea that grey mouse lemurs have acute auditory capabilities that decipher
slight differences in amplitude of sounds generated by insects, allowing them to forage for
insects with the greatest mass, and thus the greatest nutritional reward.
While species differences in activity time may have effects on primate perception due to
an unavailability of sunlight, so to might species or intra-species differences in the possession of
trichromatic color vision.
Color Vision
To test whether or not individuals with trichromatic color vision have an advantage over
dichromatic individuals in foraging for food items, Bunce & colleagues composed a series of
observations on the foraging behaviors of wild titi monkeys in Peru (2011). The researchers
observed that both trichromatic and dichromatic females had more successful foraging
encounters with yellow, orange and red food patches than their dichromatic male counterparts,
but did not observe any difference in success rates between the trichromatic and dichromatic
females. These results were interpreted as meaning that trichromatic color vision provides
monkeys with a foraging advantage over dichromatic individuals only when their nutritional
requirements force them to search for completely novel food patches, or ones outside of their
spatial memory. Future studies will benefit by examining whether or not primates with

12. dichromatic color vision rely more on any nonvisual cues in order to complete successful
foraging. For example, dichromatic primates may rely more on their olfactory capabilities in
order to successfully forage for ripe fruits.
Conclusion
The reviewed literature identifies two major aspects of primate feeding ecologies that
influence primate perceptual space in relation to the adaptive challenge of successful foraging.
First, primates foraging for fruits or species whose diets are highly composed of fruits,
respectively, rely more on olfactory perception to select high quality fruits, and may have
specialized olfactory capabilities realized physically in the main olfactory system for fine-tuned
perception of high quality fruits. The presence of fruit in primate diets have also been shown to
be correlated with more sensitive gustatory capabilities in detecting sucrose and the chemical
class of tannins, as these perceptual differences may allow for optimal foraging. The second
major trend identified in the literature is that the unavailability of visual cues to foraging
primates is correlated with a greater reliance on olfactory and auditory perception for
successful food acquisition. Experimental field studies and behavioral studies have shown that
nocturnal primates foraging for fruits exhibit an extra sensitive sense of smell while nocturnal
primates foraging for invertebrates show an acute sense of auditory perception.
Proposed Study
If I were to conduct a study following the findings if this literature review, I would design
an experimental field study that compares the perceptual decisions used by owl monkeys and
spider monkeys when these animals forage for food. This study will contribute to the reviewed

13. literature by further examining how the major trends of fruit foraging and the unavailability of
visual cues in primate feeding ecologies might mediate the types of perception used by these
two species. The reviewed literature suggests that both fruit foraging and foraging in the
absence of daytime light are correlated with a reliance on olfactory perception by primates. In
my study I will be able to control for the reliance on olfaction due to feeding ecologies
characterized by a lot of fruit consumption, because both spider monkeys and owl monkeys are
regularly frugivorous. However, I will be able to isolate the possible effects that the
unavailability of visual cues might have on olfactory perception because owl monkeys are
nocturnal foragers while spider monkeys are diurnal foragers.
The design of this study will be similar to that of Bicca-Marques & Garber (2004) which
compared the foraging behaviors of nocturnal owl monkeys and diurnal tamarins and titi
monkeys. I will set up feeding stations in areas known to be frequented by the spider and owl
monkeys, each station consisting of multiple leaf piles where pieces of fruit will be
experimentally placed. Monkeys will be habituated to these stations with pre-experimental
fruit reward baitings. I will test the monkeys’ rates of successful fruit foraging by examining
their uses of both visual and olfactory sensory cues. In trials where only visual cues are available
I will place a citrus fruit randomly on top of one of the leaf piles and place fake citrus fruits on
top of the other leaf piles. To eliminate the olfactory cues given by the real citrus fruit, I will
hide real citrus fruits in the leaf piles with fake fruits on top. In trials where only olfactory cues
are available, I will place two citrus fruits randomly under the surface of one of the leaf piles so
that the fruits are not visible from outside. Spider monkeys, of course will be tested in the
daytime, and owl monkeys tested at night.

14. Two separate analyses will be done on the observed foraging behaviors of the monkeys:
rate at which the first visit to a leaf pile is the pile containing the real fruit, and the rate at which
the pile containing the real fruit was visited at all during any given trial. I hypothesize that
because owl monkeys are used to foraging at night in sparse amounts of light, they will
outperform the spider monkeys in the successful foraging of fruits using only olfactory cues.
If I observe that owl monkeys do in fact outperform spider monkeys in foraging for fruits
using only olfactory cues, I will have demonstrated an interaction between the two major
trends previously identified in the reviewed literature. I will have shown through a comparative
behavioral study that a primate species that is both naturally frugivorous and spends its
foraging time in the absence of most visual cues, the owl monkey, has greater olfactory
capabilities related to foraging than the spider monkey who is just naturally frugivorous but has
ample visual cues in its normal time of foraging.
If my hypothesis is not supported by this experiment, then perhaps more comparative
field experiments could shed some more light on how olfactory perception is utilized by
nocturnal and diurnal frugivores. Similarly, neuroanatomical comparative analyses of the
olfactory systems of both nocturnal and diurnal frugivores may provide information on how
fruit foraging is accomplished by specific neural mechanisms in these primate species.

15. References
Bicca-Marques, J. C., & Garber, P. A. (2004). Use of spatial, visual, and olfactory information
during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing
Aotus, Callicebus, and Saguinus. American Journal of Primatology, 62(3), 171-187.
Bunce, J., Isbell, L., Grote, M., & Jacobs, G. (2011). Color vision variation and foraging behavior
in wild neotropical titi Monkeys (Callicebus brunneus): possible mediating roles for
spatial memory and reproductive status. International Journal of Primatology, 32(5),
1058-1075.
Dominy, N. J. (2004). Fruits, fingers, and fermentation: the sensory cues available to foraging
primates. Integrative and Comparative Biology, (4), 295-303.
Goerlitz, H. R., & Siemers, B. M. (2007). Sensory ecology of prey rustling sounds: acoustical
features and their classification by wild grey mouse lemurs. Functional Ecology, 21(1),
143-153.
Laska, M., Freist, P., & Krause, S. (2007). Which senses play a role in nonhuman primate food
selection? A comparison between squirrel monkeys and spider monkeys. American
Journal of Primatology, 69(3), 282-294.
Laska, M., Scheuber, H., Sanchez, E. C., & Luna, E. R. (1999). Taste difference thresholds for
sucrose in two species of nonhuman primates. American Journal of Primatology, 48(2),
153-160.

16. Nevo, O., Heymann, E.W. (2015). Led by the nose: Olfaction in primate feeding ecology.
Evolutionary Anthropology, 24(4), 137-148.
Remis, M. J. (2006). The role of taste in food selection by African apes: implications for niche
separation and overlap in tropical forests. Primates, 47(1), 56-64.
Rushmore, J., Leonhardt, S. D., & Drea, C. M. (2012). Sight or scent: lemur sensory reliance in
detecting food quality varies with feeding ecology. Plos One, 7(8), 1-12.
Siemers, B. M., Goerlitz, H. R., Robsomanitrandrasana, E., Piep, M., Ramanamanjato, J.,
Rakotondravony, D., & Ganzhorn, J. U. (2007). Sensory basis of food detection in wild
Microcebus murinus. International Journal of Primatology, 28(2), 291-304.