Biol. Rev. (2018), pp. 000–000.

1
doi: 10.1111/brv.12462

What, where and when: spatial foraging

decisions in primates
Cinzia Trapanese1,2,3,4∗ , Hélène Meunier2,3† and Shelly Masi4†
1
École Doctorale Frontières du Vivant (FdV) – Programme Bettencourt, Centre de Recherches Interdisciplinaires, Tour Maine Montparnasse,
Paris 75015, France
2 Centre de Primatologie de l’Université de Strasbourg, Fort Foch, Niederhausbergen 67207, France
3
Faculté de psychologie Laboratoire de Neurosciences Cognitives et Adaptatives, UMR 7364, CNRS et Université de Strasbourg, Strasbourg
67000, France
4
Département Hommes et Environnements Centre National de la Recherche Scientifique/Muséum National d’Histoire Naturelle, University Paris
Diderot, Sorbonne Paris Cité, Musée de l’Homme, UMR 7206-CNRS/MNHN, Paris 75116, France

ABSTRACT

When exploiting the environment, animals have to discriminate, track, and integrate salient spatial cues to navigate
and identify goal sites. Actually, they have to know what can be found (e.g. what fruit), where (e.g. on which tree) and
when (in what season or moment of the year). This is very relevant for primate species as they often live in seasonal and
relatively unpredictable environments such as tropical forests. Here, we review and compare different approaches used
to investigate primate spatial foraging strategies: from direct observations of wild primates to predictions from statistical
simulations, including experimental approaches on both captive and wild primates, and experiments in captivity using
virtual reality technology. Within this framework, most of these studies converge to show that many primate species can
(i) remember the location of most of food resources well, and (ii) often seem to have a goal-oriented path towards spatially
permanent resources. Overall, primates likely use mental maps to plan different foraging strategies to enhance their
fitness. The majority of studies suggest that they may organise spatial information on food resources into topological
maps: they use landmarks to navigate and encode local spatial information with regard to direction and distance. Even
though these studies were able to show that primates can remember food quality (what) and its location (where), still very
little is known on how they incorporate the temporal knowledge of available food (when). Future studies should attempt
to increase our understanding of the potential of primates to learn temporal patterns and how both socio-ecological
differences among species and their cognitive abilities influence such behavioural strategies.

Key words: spatial foraging strategies, cognitive map, primates, decision rules, spatial memory.

CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
II. Into the primate mind . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
(1) Random walks models: Lévy walks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(2) The strategy of re-using the same routes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(3) Path integration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
(4) Landmark navigation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
(5) Cognitive maps: acquisition, storage and organisation of information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
III. How to infer the mental processes underlying primate movements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(1) Experiments in captivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(2) Manipulating or observing the natural environment: wild primates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(a) Field experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
(b) Direct observations of wild primates: indicators of intentionality and the change-point test (CPT) 9
(c) An alternative method: the Circuity Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
(d) Quantitative statistical models based on direct observations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

* Address for correspondence (Tel: +33 7 52 59 25 74; E-mail: cinzia.trapanese@cri-paris.org).

† Authors contributed equally to this work.

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2 C. Trapanese and others

(e) Botanical or ecological knowledge: a complementary or an additional strategy? . . . . . . . . . . . . . . . . . . 13

(f ) Planning ahead: integrating ecological variables to assess behaviour goals . . . . . . . . . . . . . . . . . . . . . . . . 14
(3) Primate navigation in virtual reality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
IV. General discussion and perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
V. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
VI. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
VII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

I. INTRODUCTION travel routes of similar length to the optimal path (Cramer

Finding and locating food resources in wild habitats
can be cognitively demanding. For instance, animals
living in tropical forests have to cope with complex
environments often characterised by relatively unpredictable
food availability. Indeed, since all rainforest trees do not
always fruit each year, and because fruiting periods are
often short (Chapman et al., 1999), frugivorous animals
have to know what tree produces fruits and when. What,
where and when an individual eats are likely to affect its
fitness, and, ultimately, species-level adaptations (Lambert
& Rothman, 2015; Janmaat et al., 2016). When exploiting
the environment, animals have to discriminate, track and
integrate salient spatial cues to navigate and identify feeding
sites. Animals receive also a barrage of sensory inputs,
which help them to take efficient feeding decisions in
relation to the spatio-temporal distribution of food (Dominy
et al., 2001). While foraging, individuals generally face
three major challenges: (i) locating ephemeral, scattered
goal sites characterised by fluctuating annual and seasonal
patterns, (ii) competing with co-feeders (intra-group and
extra-group competition; Garber, Bicca-Marques & de O
Azevedo-Lopes, 2009) and (iii) avoiding predators.
For animals, an efficient way to maximise energy intake is
by planning foraging decisions. In this context, planning is
defined as the ability to search in advance for the best strategy
to forage efficiently (e.g. where to go to find a given resource
and when). We can argue that planning implies intentionality,
or the ability to formulate goals to proceed towards them with
direct intent (Dooris, Kelley & Trainer, 2004; e.g. maximise
energy intake while minimising costs). On the other hand,
we can also assume intentionality without planning, for
example the intentionality in the use of a behavioural tactic.
Optimisation of foraging strategies has been shown in many
animal taxa such as birds (Davies & Houston, 1981; Gill,
1988), bats (Lemke, 1984; Racey & Swift, 1985), rodents
(Reid & Reid, 2005), primates (e.g. Di Fiore & Suarez, 2007;
Noser & Byrne, 2013) and even pollinating insects (Janzen,
1971; Heinrich, 1976; Lihoreau, Chittka & Raine, 2011).
In traplining bumblebees (Bombus terrestris), for example, it
has been suggested that they are able to trade off between
the distance travelled and the prioritisation of high-reward
sites when foraging (Lihoreau et al., 2011). So what are the
strategies that animals – and primates in particular – use to
optimise their energy balance? Some studies have shown that
using a simple planning rule of travelling step-by-step from
one destination to the next nearest can produce complex
& Gallistel, 1997; Janson & Byrne, 2007). But is the strategy
of visiting all available food locations always the most
convenient? As the environment can be unpredictable and
unstable, a variety of reasons could lead primates to miss
out a feeding patch: to avoid environmental and physical
impediments, to avoid predators or competitors, to feed on
another food that is abundant in a given season (e.g. better
maturation state), or to use a more valuable food available in
the habitat. Cunningham & Janson (2007a) showed that wild
saki monkeys (Pithecia pithecia) increased the overall distance
travelled in order to visit preferred resources such as highly
productive fruit trees and tree-water holes. This strategy
allowed them to encounter the majority of the available fruit
trees even if they did not feed on them. This behaviour likely
allows them to minimise intra-group feeding competition and
to monitor continuously the state of resources throughout
their home range (Cunningham & Janson, 2007a). Primates
usually visit more than one destination when foraging: they
thus use multi-destination routes (Gallistel & Cramer, 1996).
When individuals leave a patch, they are expected to move
to their next goal (e.g. sleeping site, feeding site, refuge area)
in a direct manner, minimising unnecessary travel in order
to maximise their energy balance (Chapman & Chapman,
2000). If the potential choices between food locations are
already included in a known foraging sequence by the
individual, route optimisation becomes analogous to the
classical optimal foraging problem, the Traveling Salesman
Problem (TSP). This is an experimental algorithmic problem
that has many applications: an individual has to choose
an optimal route to visit many different locations before
returning to the starting point. Since this represents a
combinatorial optimisation problem, it has been intensively
studied from a computational standpoint as part of a
class of mathematical problems termed non-deterministic
polynomial-time hardness (NPhard; Lawler et al., 1985).
Solutions to TSPs become increasingly complex and
intractable as the number of destinations increases
(MacGregor & Chu, 2011). Cramer & Gallistel (1997) tested
the capacity to solve TSP-like problems in a group of captive
vervet monkeys (Cercopithecus aethiops). To visit four feeding
stations, they optimised their route to return to the starting
point in 20 out of 26 trials. In a second experiment, four
baited locations were provided on one side of the enclosure,
and two more on the other side, with the nearest location in
each group being equidistant from the starting point. Vervet
monkeys chose the side with the greater number of foraging
sites in all trials, showing the ability to plan their movements

Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society

Spatial foraging decisions in primates
at least three steps ahead (two further destinations beyond the
nearest site; Cramer & Gallistel, 1997). The computational
complexity required for such planned foraging raises the
question of whether in the wild primates can calculate
the shortest path among multiple destinations (Lawler et al.,
1985; Gallistel & Cramer, 1996). Wild individuals (and most
primate species) are confronted more often with open-TSP
or the so-called optimal Hamiltonian path problem (Garey
& Johnson, 1979). In the mathematical field of graph theory,
a Hamiltonian path visits each vertex of the graph exactly
once. Applying this to foraging routes, individuals visit each
destination only once and they do not need to return to the
starting point (Janson, 2014).
How does species socio-ecology shape the level of
cognitive sophistication in foraging strategies? Primates, and
particularly anthropoids, have relatively large brains com-
pared to other mammals (Clutton-Brock & Harvey, 1980).
The Social Brain Hypothesis identifies social complexity as
the main driver for primate cognitive complexity (Dunbar,
1998) whereas many comparative studies have linked a
larger brain size to a frugivorous diet (Clutton-Brock &
Harvey, 1980; Milton, 1981; DeCasien, Williams & Higham,
2017). Various other hypotheses about the evolution of
a large brain in the primate lineage have been proposed
[e.g. the cognitive-buffer hypothesis (Allman, McLaughlin
& Hakeem, 1993), the Machiavellian intelligence hypothesis
(Byrne & Whiten, 1988), the cultural intelligence hypothesis
(Whiten & Van Schaik, 2007), the ecological intelligence
hypothesis (Milton, 1981)]. The debate between a social or
ecological basis for cognitive complexity is now linked with
a growing body of evidence showing that brain organisation
may also relate to divergent ecological adaptations [Rosati,
2017; the ecological intelligence hypothesis (Milton, 1981)].
This seems to be the case for gorillas where differences
in life history and brain structure between the two species
correspond to their divergent ecological habits (Stoinski et al.,
2013; Barks et al., 2015): one species (Gorilla gorilla gorilla) is
more frugivorous while the other (Gorilla beringei beringei) is
more folivorous as a consequence of lower fruit availability in
their mountain habitat (Masi, Cipolletta & Robbins, 2009).
Recently, comparisons across several primate species found
evidence suggesting a greater influence of ecological rather
than social variables on brain size (DeCasien et al., 2017).
After controlling for body size and phylogeny, brain size was
better predicted by the diet than by multiple measures of
sociality (DeCasien et al., 2017): frugivores had larger brains
than folivores. Investigating the spatial foraging strategies
of primates may thus help to shed light on the origin of the
complex cognitive abilities of primates and on the roots of
the most complex planning capacities of humans.
Investigating spatial foraging decisions in primates
raises a number of challenges, including the methodological
approach used. For a better understanding of the approaches
used to investigate primate spatial foraging strategies and
the underlying cognitive mechanisms, we here review (i)
the existing literature to highlight the current foundations
on which the theoretical framework is based, and (ii) the
3
principal methods used to investigate the cognitive mech-
anisms underpinning decision making, memorisation, and
planning. We discuss those methods in order of increasing
experimental complexity, from behavioural observations in
the wild, through testing of theoretical expectations in exper-
imental settings both in the wild and captivity, and finally to
a new approach based on virtual reality. In order to provide
useful insights and perspectives for future investigations, the
limitations of each method are also discussed.
II. INTO THE PRIMATE MIND
Studies on spatial foraging decisions in primates aim to
investigate how primates encode, internally represent and
integrate spatial, temporal and quantity information to plan
their feeding choices efficiently. The simplest strategy for
foraging would be to move randomly until a feeding resource
is located. This would be particularly efficient for species with
a generalist diet living in a highly productive environment
containing abundant and readily available food (e.g.
herbaceous vegetation; Garber, 1987). However, this strategy
is unlikely to be effective for primates, given that many are
frugivorous and territorial, and live in large home ranges
with scattered and ephemeral fruit trees (Strier, 2007). In
tropical forests, where the majority of primates live, fruits are
available only at certain times of the year, and fruiting trees
are visited by many animals competing for this energy-rich
resource (Marriott, Robinson & Karikari, 1981; Diaz-Perez,
Bautista & Villanueva, 2000; Houle, Chapman & Vickery,
2007). According to Optimal Foraging Theory (Schoener,
1971; Stephens & Krebs, 1986), therefore, primates should
optimise their travelling patterns. Their complex cognitive
abilities allow them to minimise energy expenditure and
hence approach maximum foraging efficiency (Dall et al.,
2005; Robbins & Hohmann, 2006). Detours would increase
costs in terms of risk of starvation, predation, and increased
energy expenditure. However, the relative costs will vary
according to the feeding ecology of the species (Garber,
1987). For example, folivorous primates’ resources are more
homogeneously distributed and are present throughout the
year (and are therefore easily accessible) than are resources of
fruit specialists (e.g. Chapman, White & Wrangham, 1994;
Chapman, Wrangham & Chapman, 1995; Sayers, 2013;
Masi et al., 2015; Masi & Breuer, 2018).
According to the concept of rule-based decision-making
(Bugnyar & Heinrich, 2006), animals can use a ‘trial
and error’ strategy and/or different forms of social
learning to create expectations (hypotheses) and tactics
(rules) to find solutions (Laland, 2004). These capacities
require behavioural flexibility to generalise cause-and-effect
relationships from one context to another by recognising
critical elements common to past and present situations
(Watanabe & Huber, 2006). This would imply the ability
to recall which behavioural tactic was most successful
in the past and the capacity to apply that tactic to the
current problem (Watanabe & Huber, 2006). If a given
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4 C. Trapanese and others
tactic fails, the individual is expected to incorporate this
information and try other tactics or decision rules to solve
the problem (Garber, 2000). Primates seem to be able to
develop foraging strategies that integrate both social and
ecological information (Bicca-Marques & Garber, 2005).
Garber et al. (2009) suggested a set of ‘decision rules’ for
primates: information is organised hierarchically with the
most important information for that decision considered
first. For example, species with a more-specialist diet will
first evaluate ‘food type information’ (e.g. a given fruit
type such as leaves or flowers), whereas species living in
large social groups will first prioritise ‘quantity information’
(e.g. a clumped food distribution would be preferred to a
more scattered one). Secondly, ‘social information’ such
as the presence/absence/identity of other group members
(or other groups or predators) and finally ‘spatial and
temporal information’ (when the food is present/ripe and
where it is located) are considered. Based on previous
experience the forager will use this information to develop
particular decision rules (Garber et al., 2009). Some sets of
rules are likely to be relatively simple, integrating limited
amounts of social and ecological information, and represent
so-called ‘rules of thumb’ (e.g. for subordinate individuals:
the avoidance of any feeding site that is currently occupied
by more-dominant individuals; Bugnyar & Heinrich, 2006).
Other rules are likely to be more complex since they integrate
several types of context-specific information and thus require
greater computational abilities. For example, if after a given
period of time the quantity of food in a given patch has not
fallen below a critical level, a satiated individual will tolerate
additional foragers (Garber et al., 2009).
We now aim to reviewing the spatial and temporal
foraging strategies described in primate species according to
their different socio-ecology. For each strategy, we underline
advantages and disadvantages in terms of optimising their
energy balance.
(1) Random walks models: Lévy walks
The activity budget of an animal will be affected by
resource availability and distribution (Jager et al., 2011).
To be able to exploit food resources that are scattered
in space, an efficient strategy is to perform a random walk
(Codling, Plank & Benhamou, 2008). Prominent examples
of random walk strategies are Brownian walks and Lévy
walks that are conceptual tools for modelling animal search
paths (Codling et al., 2008). In these strategies both the
direction and step length of the constituent moves are drawn
from a probability distribution (Codling et al., 2008). The
movement patterns differ in the distribution of step lengths.
In Brownian walks, step lengths l j are derived from an
exponential distribution and have a characteristic scale,
usually defined by the first and second moment (the mean
and the variance, respectively) of the step length density
distribution P(l j ). In Lévy walks, step lengths are derived
from a power-law distribution (where many short steps are
occasionally alternated with a long one) and they have no
characteristic scale (Viswanathan et al., 1999). Lévy walks
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
provide faster dispersal, encounter a higher number of novel
sites (Bartumeus et al., 2005) and have a reduced likelihood
of intra-specific competition than Brownian walks. In Lévy
walks the variance (i.e. second-order moment) diverges and
adds a super-diffusive feature, increasing their efficiency
compared to purely diffusive movements. Moreover, Lévy
walks accurately describe the pattern but not the underlying
process, as they represent an efficient search strategy for
resources that are distributed in self-similar ways across
various environmental scales [i.e. both searches at a reduced
scale (which might be purely random) and searches at a high
scale with goal-oriented movements (Benhamou, 2007)].
Many animals adopt Lévy walk search strategies when
food (or prey) is rare and unpredictable (Humphries et al.,
2010), e.g. amoebas (Acanthamoeba castellanii) (Levandowsky,
White & Schuster, 1997), fruitflies (Drosophila melanogaster)
(Reynolds & Frye, 2007), wandering albatrosses (Diomedea
exulans) (Viswanathan et al., 1996, 1999), jackals (Canis adustus)
(Atkinson et al., 2002), reindeer (Rangifer tarandus tarandus)
(Mårell, Ball & Hofgaard, 2002) and also hunter–gatherer
humans (Ju/’hoansi hunters and foragers; Brown, Liebovitch
& Glendon, 2007; Raichlen et al., 2014).
In non-human primates, Lévy walk patterns have been
observed in spider monkeys (Ateles geoffroyi; Boyer et al., 2006):
their walks, consisting of a sum of independent and infrequent
steps, seem to represent an optimal searching strategy to find
scarce resources. In bearded saki monkeys (Chiropotes spp.),
waiting times were consistent with a Lévy pattern (i.e. many
low-quality patches and a few high-quality patches) while
their step lengths during foraging were more consistent
with a Brownian pattern (as resources had a more random
distribution) (Shaffer, 2014). Moreover, the distribution of
their turning angles indicated a high degree of directional
persistence between patches. Thus, the results suggest that
they encode the locations of high-quality food patches
and minimise travel time between them. They also feed
opportunistically from abundant and randomly distributed
lower quality patches en route (Shaffer, 2014).
(2) The strategy of re-using the same routes
An alternative strategy to the random-walk is to re-use the
same routes. A clear definition of what really constitutes a
‘route’ has not yet been formulated since its length or use
is species dependent and thus generalisations are difficult
(Noser & Byrne, 2013). The term ‘route’ has been used in
literature referring to humans (e.g. Brunyé & Taylor, 2008),
large mammals (e.g. Call et al., 2008) and insects (e.g. Lent,
Graham & Collett, 2009), but less frequently to non-human
primates. We can assimilate the concept of ‘route’ to that
of ‘pathway’: it represents an established animal path or
movement, i.e. it represents the ‘fossilised’ traces of a
movement path (Benhamou, 2010). Since it is essential that
the traces are fossilised, a path cannot be travelled only once
to become a route. It is also very difficult to define the length
of a route precisely: for example, Di Fiore & Suarez (2007)
found that 95% of the locations visited by white-bellied spider
monkeys (Ateles belzebuth) over several months fell within
Spatial foraging decisions in primates
50 m of a repeatedly travelled route, whereas Sigg & Stolba
(1981) felt that a ‘buffer zone’ of 500 m was appropriate
to define a repeatedly travelled ‘street segment’ in a group
of hamadryas baboons (Papio hamadryas). Moreover, routes
are not necessarily used exclusively by one species, since
they are paths that facilitate transfer (e.g. avoiding obstacles
such as dense vegetation, rivers, difficult terrain, etc.) and
are not necessarily the shortest path to a destination, but
are convenient. Routes can be a clearly visible path through
the vegetation or they may be less well defined or hidden.
Milton (2000) hypothesised that route travelling is a common
trait among primates; indeed re-use of the same paths by
wild primates occurs in distantly related species, such as
proboscis monkeys (Nasalis larvatus) in Borneo (Boonratana,
2000), howler monkeys (Alouatta spp.) in Nicaragua (Garber &
Jelinek, 2006) and in Barro Colorado Island Panama (Milton,
2000), and eastern chimpanzees (Pan troglodytes schweifurthii) in
Uganda, that re-use parts of their routes at least twice a year
(Bertolani, 2013). The travelling paths of Borneo orangutans
(Pongo pygmaeus) were described as arboreal ‘highways’ re-used
by several individuals (MacKinnon, 1974). Data collected
over 8 years on sympatric groups of spider monkeys (Ateles
belzebuth) and woolly monkeys (Lagothrix poeppigii) (Di Fiore &
Suarez, 2007) revealed that the animals consistently re-used
the same routes and that most feeding trees were within
25 m of a network of routes that ran mostly along ridges,
following the topography of the study site (Di Fiore & Suarez,
2007). Using habitual paths that cross commonly used food
patches and landmarks facilitates foraging and reduces the
cognitive effort necessary for spatial navigation (Bertolani,
2013), but will have a cost in terms of the reduced likelihood
of discovery of potential new food resources.
(3) Path integration
According to Gallistel (1990) animals may navigate by
combining two sorts of position vectors: egocentric vectors,
which specify the locations of terrain features (landmarks) in
a body-centred coordinate system, and geocentric vectors,
which specify the position of the animal in an earth-centred
coordinate system. The geocentric coordinate system is
created by dead reckoning, or path integration, and has
been studied in many animal taxa such as insects [bees
and ants (Collett, 1996; Dyer, 1996; Wehner, Michel &
Antonsen, 1996)], rats (Benhamou, 1997; Maaswinkel &
Whishaw, 1999) and other mammals (Séguinot, Cattet &
Benhamou, 1998; Etienne & Jeffery, 2004). Path integration
is the process of continuously updating one’s own position in
space, by keeping track of, and integrating, all distances and
changes of direction. Path integration has been particularly
well studied in insects, such as bees, ants, and spiders
(Wehner & Srinivasan, 2003). The mechanism is not precise,
however, because errors accumulate, both randomly and
systematically, and hence adjustments need to be made
regularly (Muller & Wehner, 1988). For this reason, path
integration is unlikely to be the only orientation system used.
In both invertebrates and mammals, it is likely integrated
with other mechanisms such as navigation based on visual
5
cues (Rodrigo, 2002). In fact, the Aka hunter–gatherer
populations of the Central African Republic seem to use
path integration together with the positions of landmarks
(presence of honey bee nests on trees, or positions of logs or
particularly large old trees such as those of the species Lophira
alata, Omphalocarpum elatum, Dialium polyanthum, Pachyelasma
tessmanii, etc.; S. Masi, unpublished observations).
(4) Landmark navigation
If visual cues are distant from the goal, and not directly
associated with it, it is necessary to remember the distance
and direction from the landmark to the goal, to calculate
one’s position relative to the landmark, and to infer one’s
position relative to the goal (Rodrigo, 2002). Similarly to
path integration, such landmark navigation has been shown
in bees (Cartwright & Collett, 1982), other insects (Collett,
1992), and also in mammals (Collett, Cartwright & Smith,
1986). A study in captive capuchin monkeys (Cebus apella)
showed that they can only learn simple associations between
a goal and a local landmark; they were not able to consider
distances from all possible goals in order to choose the shortest
one (Potì, 2000). However, captive cotton-top tamarins
(Saguinus oedipus oedipus) rely on the spatial relationship or
positions of multiple landmarks to locate hidden food items
in their environment (Dolins, 2009).
Studies on spatial orientation in humans have shown that
the use of landmarks is dependent on the ecological context
in which they live (Byrne, 1979; Thorndyke & Hayes-Roth,
1982). It seems that Western men travelling in a city
follow landmarks and are unable to provide clear directions
when mapping their pathways (Byrne, 1979; Thorndyke &
Hayes-Roth, 1982); on the other hand, aboriginal people,
who inhabit more open environments, are more accurate in
determining the direction of places that can be over 300 km
away (Lewis, 1976). Hunter–gatherer populations show also
sex-specific navigational strategies: while men prefer to use
an orientation strategy based on cardinal directions, women
prefer a landmark strategy to orientate themselves (e.g. Choi
& Silverman, 1996, 2003; Dabbs et al., 1998; Lawton &
Kallai, 2002). De Lillo, Kirby & James (2014) studied the
ability of Western humans to keep track of a set of spatial
locations while travelling. This ability depended on whether
the order in which the locations were explored was consistent
with certain organisation principles: short movements were
associated with better memory recall and required less time
to perform (De Lillo et al., 2014). These results indicate that,
at least in Western populations, organisational factors (i.e.
spatial configuration, e.g. in clusters, in a matrix etc.) may
play a large role in their spatial orientation ability.
(5) Cognitive maps: acquisition, storage and
organisation of information
Linear travel paths to distant (out-of-sight) food resources
have traditionally been used as evidence that animals had a
goal when initiating travel (Garber, 1989; Janson & Di Bitetti,
1997; Janson, 1998; Janmaat, Byrne & Zuberbulher, 2006a;
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
6 C. Trapanese and others
Valero & Byrne, 2007; Noser & Byrne, 2007a,b; Cunningham
& Janson, 2007b; Luhrs et al., 2009; Normand & Boesch,
2009). However, in response to a degree of unpredictability
in food availability, animals, including primates, will have
a dynamic relationship with their habitat. They can use
straight-line routes but may deviate from them according
to the situation, either because of anthropogenic [e.g.
construction of a road, deforestation (Tutin, 1999; Hockings,
2007; Hockings, Anderson & Matzusawa, 2012); availability
of human crops (e.g. Krief et al., 2014)] or natural causes
[e.g. seasonality (Brockman & van Schaik, 2005); landscape
features (e.g. rivers); predation pressure; decision to exploit
a different resource along the route (Cunningham & Janson,
2007a)]. The different strategies used by primates thus involve
adjustments to the changing environment and depend on the
species and their ecological niche.
At the highest level of complexity, primates may use
abstract mental representations to acquire, store and decode
spatial, temporal and ecological information, thus relying
on what Gallistel & Cramer (1996) called a ‘global cognitive
map’. The concept of a cognitive map is not used consistently
in the existing literature; for example, Tolman (1948, p. 189)
defined it as ‘an internal representation (or image) of external
environmental feature or landmark’, while O’Keefe & Nadel
(1978, p. 86) defined it as ‘the representation of a group of
places, some related to others by means of a set of rules
of spatial transformation’. Modern researchers refer mainly
to two different types of cognitive maps (Garber, 2000):
a route-based map, also called a network or topological
map, and a Euclidean map, which is coordinate-based or
geometric. The term ‘mental map’ is often used to refer to
cognitive maps in general, however sometimes this term has
been erroneously restricted to Euclidean maps (e.g. Tolman,
1948; O’Keefe & Nadel, 1978).We suggest that the term
‘route-based map’ (Poucet, 1993) is widely adopted for the
first type of map: a topological map in which animals use
landmarks to navigate and to approximate local information
about direction and distance (Asensio et al., 2011). They
can use qualitative information about connections and
destinations to memorise a finite number of routes, a network,
which is then used repeatedly to reach the resources in
relation to their position. In this graph-structured network,
vertices (also called nodes) represent locations (landmarks)
that are well defined and well known (Schkolkopf & Mallot,
1995). The second type of cognitive map, we propose to refer
to as a Euclidean map (O’Keefe & Nadel, 1978) as this is used
most frequently in the literature, although ‘coordinate-based
map’ (Garber & Dolins, 2014) would perhaps be more
intuitive. A Euclidean map is a detailed geometrical map
in which the individual has a quantitative representation
of the entire environment including the metric angles and
distances. The nervous system contains such information
as position vectors and can perform basic computations
with these vectors, such as rotating them and adding them
(Gallistel & Cramer, 1996). Other simpler strategies (e.g. a
topological map) do not require such precise organisation
but they benefit from the additional visual and qualitative
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
information provided by landmarks, thus distances are more
approximate. In the case of the Euclidean map, animals do
not tend to re-use pathways, but reach the same point from
different directions (Normand & Boesch, 2009). They use
short-cuts that connect two resources which correspond to
changes in direction. A Euclidean mental map is considered
to be the most flexible and therefore the most efficient
way to navigate; it is also more efficient in less well-known
areas (Gallistel & Cramer, 1996). There is no clear evidence
regarding the use of such maps in any non-human species.
In human children, some sort of Euclidian notion emerges
at around 6 or 7 years of age, allowing more complex
and flexible spatial operations (Piaget & Inhelder, 1956).
However, its development has been shown to be a function
of socioecological conditions (Parker, 1993; Wassmann &
Dasen, 1998; Boesch, 2007), thus experiments in other
human societies may provide different results. Given that
some cognitive abilities of chimpanzees are comparable to
those of 3-year-old children (Woodruf & Premack, 1979),
evidence for the use of Euclidean maps in chimpanzees in
Taï, Ivory Coast (Pan troglodytes verus; Normand & Boesch,
2009) was surprising and follow-up studies are needed to
confirm this ability. The use of such sophisticated mental
organisation in non-human primates is therefore still under
debate. However, it has been suggested that a possible
advantage to chimpanzees of using Euclidean maps is to
increase their travel efficiency in the context of tool use
(Normand & Boesch, 2009). Tool use in these chimpanzees
requires a precise knowledge of different stone hammer
locations (Boesch & Boesch, 1984) and an accurate tool
selection (in terms of size and shape) that together imply
an ability to anticipate future events (Sirianni, Mundry &
Boesch, 2015). Normand & Boesch (2009) analysed the
travel speed, directions, route used and the linearity index
(the direct distance between feeding sites divided by the
distance travelled) as a measure of goal-reaching efficiency
of chimpanzees moving through a forest habitat (Valero &
Byrne, 2007; Noser & Byrne, 2007a,b). Their results were
more consistent with the use of a detailed Euclidean map
than a topological map. However, it remains possible that
chimpanzees could combine a Euclidean map with other
navigation systems (e.g. landmark use, route-based map, etc.).
Recently, the presence of a Euclidean map in rats has been
supported by the discovery of neurons in the hippocampus
that fire when the animal is in a particular place, regardless of
its field of view, and even in complete darkness (Eichenbaum,
2014; Eichenbaum & Cohen, 2014). This neuronal activity
could reveal the capacity to store specific spatial information
in the brain independently from visual cues. Moreover,
Killian, Jutras & Buffalo (2012) and Killian, Potter & Buffalo
(2015) showed that grid cells in the primate entorhinal
cortex represent and encode positions in visual space. This
observation suggests that primates might be able to encode
a representation of their environment in order to memorise
valuable resources.
Although efficient travel between out-of-sight resources
can be achieved by both a route-based map and Euclidean
Spatial foraging decisions in primates
map, the two types of map result in different predicted
travelling patterns: in a Euclidean model, routes are not
consistently re-used because each travelling event results from
a novel calculation aimed at finding the best path (Byrne,
1979). In addition, under a Euclidean model changes in
direction occur at the start and end points of each travelling
event, while under a route-based map hypothesis a significant
proportion of changes in direction are expected to occur as
a result of a reorientation process (Bertolani, 2013).
III. HOW TO INFER THE MENTAL PROCESSES
UNDERLYING PRIMATE MOVEMENTS
(1) Experiments in captivity
In comparison to studies in wild habitats, experiments on
captive primates enable the control and manipulation of
external variables and the spatio-temporal availability of
resources, thus allowing detailed investigations of primate
spatial navigation and spatial memory. An extensive
summary of spatial foraging studies on captive primates
is provided in Table 1.
The food choice behaviour of titi monkeys (Callicebus
moloch) and squirrel monkeys (Saimiri sciureus) was examined in
captivity using an eight-arm maze under various conditions
of spatial and temporal food availability (Andrews, 1988).
Both species avoided revisiting the same feeding sites.
Moreover, under conditions in which the goals differed
in food abundance, both species tended to select goals
that maximised energy intake, even though this behavioural
adjustment involved a certain delay. Captive yellow-nosed
monkeys (Cercopithecus ascanius whitesidei) showed a similar
ability to remember feeding locations and also applied
the least-distance strategy (minimising the total distance
travelled) (MacDonald & Wilkie, 1990).
Capuchin monkeys (Cebus apella) showed higher search
efficiency in a cluster organisation of food than in a
matrix, using a strategy to reduce memory requirements
for solving the task (De Lillo et al., 1997); a similar strategy
was used by tree shrews (Tupaia belangeri) when tested with
the same experimental protocol (Bartolomucci, de Biurrun
& Eberhard, 2001). In a follow-up experiment, capuchin
monkeys (Cebus apella) showed a higher search efficiency
when the search space featured either a linear (in which
case they used methodical search trajectories from one end
to the other of the linear array) or circular arrangement of
containers, as opposed to a matrix or cross arrangement (De
Lillo et al., 1998). These results suggest that capuchins use
either the travel distance or the associated cognitive costs to
organise their searching behaviour (De Lillo et al., 1998).
Considering the three variables what, where and when,
Hampton et al. (2005) showed that the working memory
of rhesus macaques (Macaca mulatta) was restricted to the
what and where components but did not include when. The
macaques could not differentiate between short and long
delays: they seemed unable to learn that a preferred food
7
was available after a short interval, but not after a long
one. Recently, spatial memory skills have been studied
in four captive strepsirrhine primates that vary in level
of frugivory (Rosati et al., 2014). The results showed that
species with the greatest ecological disparity exhibited the
most variation in spatial memory skills: recall after a long
delay, learning mechanisms supporting memory, and recall
of multiple locations in a complex environment (Rosati et al.,
2014). The most frugivorous species, ruffed lemur (Varecia
sp.), consistently showed a more robust spatial memory than
the other species (ring-tailed lemur Lemur catta, mongoose
lemur Eulemur mongoz, sifaka Propithecus coquereli) across tasks,
particularly in comparison with sifakas, the most folivorous
species.
Other studies addressed only the when component, testing
memory for food locations. Capuchin monkeys (Sapajus cay;
Tujague et al., 2015) showed long-term spatial memory
revealing a capacity to remember the positions of three
accessible and non-accessible baited sites for periods up to
4 months. Chimpanzees (Pan troglodytes) were also able to
remember food locations well after limited exposure, 24 h
and 3 months (Mendes & Call, 2014). In an earlier study,
Menzel (1973) established the ability of chimpanzees to
remember the positions of 18 different feeding sites. Their
searching pattern approximated an optimum route and they
rarely re-checked a site they had already visited. Other
captive apes, such as western gorillas (Gorilla gorilla) and
Borneo orangutans (Pongo pygmaeus abelii) similarly remember
food location while avoiding revisitation of depleted sites
[even those visited by other individuals (MacDonald, Pang
& Gibeault, 1994; MacDonald & Agnes, 1999; Gibeault &
MacDonald, 2000)]. Although in general the use of captive
animals allows tighter control of environmental and social
variables, it may not always be possible to relate the results to
natural animal behaviour, and different studies use different
experimental designs. Moreover, captive-reared primates
might not have acquired appropriate experience to develop
their navigation abilities compared to their free-living
counterparts (Menzel & Beck, 2000), since environments in
captivity lack the complexity and unpredictability of natural
contexts. Therefore, studies investigating spatial strategies
using captive animals have often limited ecological validity
and generalisation to the behaviour of wild animals is
problematic (Dolins et al., 2014).
(2) Manipulating or observing the natural
environment: wild primates
(a) Field experiments
During last two decades, researchers have increasingly
investigated spatial foraging navigation directly in the
field using methods developed in captive settings. This
approach is of particular interest because while retaining the
possibility of controlling and manipulating some variables,
it allows measurements to be made in wild animals in their
natural environment. However, only a limited number of
variables can be controlled. Table 2 provides a summary
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society

Table 1. Spatial foraging studies based on experiments on captive primates. Landmarks and/or other cues: type of landmarks, cues or beacons used in the study; – indicates
that they were not present or not specified in the study
Reference Species
Menzel (1973) Chimpanzee
(Pan troglodytes)
Andrews (1988) Titi monkey (Callicebus moloch),
squirrel monkey (Saimiri
sciureus)
MacDonald & Wilkie (1990) Yellow-nosed monkeys
(Cercopithecus ascanius whitesidei)
MacDonald (1994) Gorilla (Gorilla gorilla gorilla)
Cramer & Gallistel (1997) Vervet monkey (Cercopithecus
aetiops)
De Lillo, Visalberghi & Capuchin monkey (Cebus apella)
Aversano (1997)
De Lillo et al. (1998) Capuchin monkey (Cebus apella)
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
MacDonald & Agnes (1999) Orangutan (Pongo pygmaeus abelii)
Gibeault & MacDonald Gorilla (Gorilla gorilla gorilla)
(2000)
Hampton, Hampstaed & Rhesus macaque (Macaca mulatta)
Murray (2005)
Dolins (2009) Cotton-top tamarin (Saguinus
oedipus oedipus)
Mendes & Call (2014) Chimpanzee (Pan troglodytes)
Rosati, Rodriguez & Hare Ruffed lemur (Varecia sp.),
(2014) ring-tailed lemur (Lemur catta),
mongoose lemur (Eulemur
mongoz), Coquerel’s sifaka
(Propithecus coque reli)
Tujague, Janson & Lahitte Capuchin monkey (Sapajus cay)
(2015)
8
Number of Number of feeding Landmarks and/
tested subjects stations used or other cues Conclusions
6 18 – Optimised route (‘least-distance’ strategy)
and avoided revisiting the same feeding
stations
8 C. moloch and 8 S. 8 Potential landmarks: plastic Visited the most rewarding sites; revisiting of
sciureus barriers, buildings, vacant the same sites was not observed
field cages, trees and
agricultural fields
2 1st experiment: 4 – Minimised the total distance travelled
2nd experiment: 8 (‘least-distance’ strategy)
2 8 – To minimise foraging effort, used a counting
strategy during the food-search phase
4 1st experiment: 4 – Chose the optimal route and planned their
2nd experiment: 6 movements three steps ahead
4 9 in clusters and 9 in – Minimised distances more when searching in
matrix a cluster configuration than in a matrix
4 9 in circle, 9 in matrix, 9 – Search efficiency higher when searching
in cross and 9 in line either in a linear or a circular
configurations arrangement of food containers
3 8 – Minimised expended energy by reducing
travelled distance
6 16 – Able to remember not only the sites they
depleted but also those depleted by
foraging partners
10 3 – Remembered food locations for up to 25 h;
failed to learn that preferred food was
available only after a short delay and not
after a long one
17 1st experiment: 3 Geometric shapes at each To locate hidden food they relied on spatial
2nd experiment: 4 feeding station relationships among multiple landmarks
rather than on an associative strategy
12 4 – Remembered food locations after limited
exposure (1–2 trials), after 24 h and after
a 3-month retention interval
1st experiment: 44 1st experiment: 2 Objects of different shapes The most frugivorous species (ruffed lemur),
2nd experiment: 48 2nd experiment: 2 and 8 and colours at each feeding consistently showed more robust spatial
3rd experiment: 47 station, only in experiment memory than the other species, especially
3 in comparison with the most folivorous
species, the sifaka
16 6 Visual and olfactory cues Showed a long-term memory (4 months) of
used as guides or beacons sites with accessible and non-accessible
food
C. Trapanese and others
Spatial foraging decisions in primates
of experimental field studies on spatial foraging in wild
primates.
To investigate spatial memory and route planning in
wild primates, researchers carry out foraging experiments
by placing a number of baited feeding sites in strategic
positions in a small- or large-scale array. Field experiments
in sanguinus monkeys (Aotus nigriceps), tamarins (Saguinus
imperator imperator and S. fuscicollis weddelli) and titi monkeys
(Callicebus cupreus) showed that these species relocate food
rewards based solely on spatial information (site predictabil-
ity) and on visual cues (Bicca-Marques & Garber, 2004).
Similarly, white-faced capuchin monkeys (Cebus capucinus)
could remember the spatial positions of 13 feeding platforms
using mainly spatial information (local landmarks; Garber
& Paciulli, 1997). Janson (1998, 2007) found that a group of
brown capuchin monkeys (Cebus apella) moved significantly
more often towards closer platforms, and in straighter lines
than expected by any random search model, integrating
information on spatial location, reward, and perhaps poten-
tial competition in their choice of multi-site foraging routes.
The food rewards of taking a particular foraging route
will depend on the number of individuals sharing the food
along the way together with the individual dominance rank
(Janson, 1985): subordinates generally run ahead to reach
unused resources first (Janson, 2007). In a recent follow-up
field experiment, Janson (2016) presented an array of eight
feeding stations with a progressive increase in the abundance
of food rewards in proportion to the time lapsed since the pre-
vious visit. Comparison of their observations with simulated
movements derived from statistical models showed that the
monkeys could remember and integrate three characteristics
of the feeding site: distance to the site (where), the elapsed time
since the previous visit (when), the rate of food renewal of the
site (what). Another study on a group of wild vervet monkeys
(Chlorocebus pygerythrus; Teichroeb, 2015) revealed that when
alone, individuals take the shortest possible path to visit all
of the feeding sites (consistent with the convex hull strategy,
i.e. the smallest convex set containing the points). However,
in a competitive situation, their strategy varied according
to their dominance rank: a cluster strategy was adopted by
dominants (i.e. moving towards clumped close resources) and
the nearest-neighbour rule by subordinates (i.e. choice of the
closest site not yet visited). In another similar task (Teichroeb
& Aguado, 2016), vervet monkeys prioritised high-reward
food sites over low-reward sites, accessing food sites in order
of proximity (nearest-neighbour rule) when alone, while in
the presence of competitors they prioritised high-reward
sites, sometimes by-passing low-reward sites. Vervet mon-
keys therefore can integrate distance/reward information
over multiple feeding stations, show spatial discounting and
can optimise their path in different ways according to social
context.
In general, studies on wild primates allow the maintenance
of a degree of complexity similar to that of natural conditions,
thus providing insights into the selection pressures involved
in determining species navigation abilities. When possible,
a combination of captive and wild experiments is ideal to
9
investigate the mechanisms involved in foraging (Janson &
Byrne, 2007).
(b) Direct observations of wild primates: indicators of intentionality
and the change-point test (CPT)
To investigate the cognitive processes underlying travel paths
in wild animals and the spatial planning of their foraging
behaviour, indicators of intentionality are used to understand
whether primates have a goal in mind (Janson & Byrne,
2007). The degree of directedness in relation to a feeding
site is one such indicator: movements should be straighter
towards larger and more-productive sites, e.g. a fruit tree
(Milton, 1981) or water hole (Altmann, 1974). Changes
in travel speed could also signify that animals know in
advance the position of a goal site [e.g. in yellow baboons
Papio hamadryas cynocephalus (Pochron, 2001, 2005), sooty
mangabeys Cercocebus atys atys and grey-cheeked mangabeys
Lophocebus albigena johnstoni (Janmaat et al., 2006a)]. Changes
in travel direction may also be important: foraging routes
are more likely to deviate at meaningful, preferred or
productive sites (Pochron, 2005; Valero & Byrne, 2007)
and at significant landmarks (e.g. nodes of a trail system,
rivers, etc.; Dolins & Mitchell, 2010; Noser & Byrne, 2010)
rather than between such locations (Dolins & Mitchell, 2010;
Noser & Byrne, 2010). Table 3 provides a summary of
studies on spatial foraging in wild primates using analytical
approaches.
Byrne et al. (2009) proposed a statistical procedure for
determining intentionality: the change-point test (CPT). This
procedure, based on permutation, calculates retrospectively
if a change in direction from a recorded step n to n + 1
was significantly more abrupt than expected on average
when permutating points. Change-points are considered as
points where the animals re-orient themselves. A study on a
community of wild chimpanzees revealed that the majority
of direction changes occurred clearly in relation to the
network of trails in order to re-use routes (Bertolani, 2013).
Moreover, application of the CPT showed that chimpanzees
use long-term spatial memory to monitor large fruit trees
by remembering the location of abundantly fruiting trees
across different fruiting seasons (Janmaat et al., 2013a). In
addition, chimpanzees use their memory to anticipate and
revisit high-value fruit trees from long distances (Ban, Boesch
& Janmaat, 2014). The nutrient content and the abundance
of fruit indeed exerted a significant impact on female
travel paths of western chimpanzees (Pan troglodytes verus;
Ban et al., 2016); females were more likely to change their
travel direction to reach rarer trees providing fruit with a
higher fat content (Ban et al., 2016). The arboreal brachiating
gibbons (Hylobates lar) show goal-oriented travel compared
to a heuristic travel model based on straight travel paths
in random directions, and change direction primarily at
preferred fruit sources (Asensio et al., 2011). Applying the
CPT to the travel route of a group of wild baboons (Papio
ursinus) revealed that their directional changes represented (i)
locations where they decided to return to their sleeping site,
and (ii) locations close to important landmarks (e.g. change
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society

Table 2. Field experiment studies on spatial foraging in wild primates. Landmarks and/or other cues: type of landmarks used in the study; – indicates not present or not
specified
Reference Species
Garber & Paciulli Capuchin monkey (Cebus
(1997) capuchinus)
Janson (1998) Capuchin monkey (Cebus
apella)
Bicca-Marques & Night monkey (Aotus
Garber (2004) nigriceps), tamarin,
(Saguinus imperator
imperator, S. fuscicollis
weddelli), titi monkeys
(Callicebus cupreus)
Bicca-Marques & Tamarin (Saguinus imperator
Garber (2005) and S. fuscicollis)
Janson (2007) Capuchin monkey (Cebus
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
apella nigritus)
Luhrs et al. (2009) Grey mouse lemur
(Microcebus murinus)
Teichroeb & Vervet monkey
Chapman (2014) (Chlorocebus pygerythrus)
Teichroeb (2015) Vervet monkey
(Chlorocebus pygerythrus)
Janson (2016) Capuchin monkey (Cebus
apella nigritus)
Teichroeb & Aguado Vervet monkey
(2016) (Chlorocebus pygerythrus)
∗
Exact number of individuals not specified.
10
Number of
Number of feeding Landmarks and/
tested subjects stations used or other cues Conclusions
10–12 13 Yellow blocks at each Used spatial information (local landmarks) to
feeding station remember feeding sites
15 15 – Moved significantly more often towards the
closest platforms in straighter lines than
expected by any random search model
3–4 A. nigriceps, 4–6 S. i. 8 Red light at each feeding All species relocated food rewards solely based
imperator, 4–5 S. f. station on spatial information; used visual cues to
weddelli distinguish real food from sham food
4–6 C. cupreus
16 4 Coloured blocks, In group-foraging context, integrated social
red-and-yellow striped and ecological information in
posts at each feeding decision-making mechanisms
station
41 3 – Preferred the closest site even if providing less
food; to balance the energetic costs, they
chose a detour more often when the reward
was larger
8 7 – Using spatial cues, rapidly learnt a new spatial
arrangement of feeding stations; showed
high travel efficiency in directed movements
24 7 Objects, beacons at each Located food above chance levels in the
feeding station presence of goal-object cues and associative
cues; dominance of sight over smell when
foraging was found
21 6 – Individually: chose the shortest possible path in
fewer than half of the trials (convex hull)
In social group: dominants used a cluster strategy
while subordinates used the
nearest-neighbour rule to reduce
competition
around 30∗ 8 – Feeding choices were consistent with dynamic
memory for elapsed time specific to each site
21 5 – Individually: accessed food sites in order of
proximity (nearest-neighbour rule or a
convex hull)
In social group: prioritised high-reward sites
sometimes bypassing low-reward sites
C. Trapanese and others
 Table 3. Field studies on spatial foraging in wild primates according to the analytical approach used: (A) the Change Point Test, (B) the Circuity Index, (C) other statistical
models and/or comparison to computerised simulations, and (D) botanical or ecological knowledge. Evidenced mechanisms/knowledge: for A–C this column provides the
navigation mechanisms used by primates as suggested by the results of the study, for D this column indicates the ecological knowledge used by primates that was investigated
by the study
Reference
(A) The Change Point Test
Asensio et al. (2011)
Noser & Byrne (2013)
Janmaat, Ban & Boesch (2013a)
Ban et al. (2016)
Joly & Zimmermann (2011)
(B) The Circuity Index
Garber & Hannon (1993)
Porter & Garber (2013)
Garber & Porter (2013)
Suarez et al. (2014)
(C) Other quantitative statistical models and/or comparison to computerised simulations
Boyer et al. (2006)
Di Fiore & Suarez (2007)
Noser & Byrne (2007a)
Noser & Byrne (2007b)
Valero & Byrne (2007)
Erhart & Overdoff (2008)
Normand & Boesch (2009)
Noser & Byrne (2010)
Janmaat & Chancellor (2010)
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
Species
Gibbon (Hylobates lar)
Baboon (Papio ursinus)
Chimpanzee (Pan troglodytes)
Chimpanzee (Pan troglodytes verus)
Mouse lemur (Microcebus murinus)
Moustached tamarin (Saguinus
mystax), saddleback tamarin
(Sanguinus fuscicollis)
Weddell’s saddleback tamarin
(Sanguinus fuscicollis weddelli)
Weddell’s saddleback tamarin
(Sanguinus fuscicollis weddelli)
Spider monkey (Ateles belzebuth)
Spider monkey (Ateles geoffroyi)
Spider monkey (Ateles belzebuth).
woolly monkey (Lagothrix poeppigii) 18–25 L. poeppigii
Baboon (Papio ursinus)
Baboon (Papio ursinus)
Spider monkey (Ateles geoffroyi
yucatanensis)
Lemurs (Propithecus edwardsi, Eulemur
fulvus rufus)
Chimpanzee (Pan troglodytes)
Baboon (Papio ursinus)
Grey-cheeked mangabey (Lophocebus
albigena johnstoni)
Mechanisms/
Number of knowledge evidenced
study subjects by the study Conclusions
11 groups, 3–6 Route-based map In a large-scale space their travel was goal oriented towards
individuals each most of the preferred resources
25 Route-based map Directional changes corresponded to locations where the
decision to return to their sleeping site was taken or near
important landmarks
Spatial foraging decisions in primates
5 Long-term spatial Used long-term spatial memory to monitor large fruit trees,
memory remembering this information also across fruiting seasons
5 Spatial memory Changed travel direction at rare and fat-rich fruit trees
7 Spatial memory or Change-points coincided with out-of-sight keystone food
olfactory cues resources; travel paths were goal oriented; insufficient
evidence for a presence of a route-based map
1 mixed group∗ Spatial memory and Although likely to rely also on olfactory cues, used a detailed
olfactory navigation spatial map to minimise distance between scattered feeding
sites
5 Route-based map Navigated at large scales using a route-based spatial
representation
5 Route-based map Used route-based travel near to goal landmarks to relocate and
monitor food in small-scale space
19 Route-based map Foraging and ranging behaviour was goal-oriented
1 group∗ Lévy walk Probably use Lévy walks to find randomly distributed resources
16–23 A. belzebuth, Route-based map Both species use landmarks to navigate and likely memorise a
series of route segments to forage efficiently
25 Route-based map Considering time and energy costs, lacked the ability to
compute Euclidean relations among locations; instead using
landmarks to navigate
25 Route-based map Planned journey choosing among several out-of-sight resources;
approached food sites in an efficient, goal-directed way
20 Spatial memory Travelled in straight lines when moving between resources and
likely planned their movements in advance
10 P. edwardsi and 7 Route-based map Both species preferred nearest-neighbour food patches and P.
E. f. rufus edwardsi travelled in relatively straight lines
15 Euclidean map (possibly) Travelled in a straight line to reach food resources from many
different directions; reduction in the distance travelled at the
periphery of the home range
25 Route-based map Cognitive maps either contained information on relatively few
trees or on a single route along which several trees were
situated
20–28 Long-term spatial Foraging efficiency was influenced by spatial memory and
memory knowledge acquired via long-term exposure
11

Table 3. Continued
Reference
Janmaat et al. (2014)
Shaffer (2014)
Schreier & Grove (2014)
Hopkins (2016)
(D) Botanical or ecological knowledge
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
Olupot, Waser, & Chapman (1997)
Janmaat et al. (2006a)
Janmaat, Byrne & Zuberbulher
(2006b)
Janmaat et al. (2012)
Janmaat, Ban & Boesch (2013b)
Janmaat et al. (2016)
∗
Exact number of individuals not specified.
12
Mechanisms/
Number of knowledge evidenced
Species study subjects by the study Conclusions
Chimpanzee (Pan troglodytes) 5 Future-oriented cognitive Left sleeping nests earlier when breakfasting on highly
mechanisms ephemeral fruits, especially when they were located at a
distance
Bearded saki (Chiropotes sagulatus) 40–50 Lévy walk Step length consistent with a Brownian walk pattern; waiting
times consistent with a Lévy walk
Baboon (Papio hamadryas) 110 Route-based map ‘Tipping points’ (landmarks) used as transition between
movements in small-versus large-scale space
Manteld howler monkey (Alouatta 18 Spatial and temporal Maximised food gain while minimising distance travelled
palliata) knowledge
Grey-cheeked mangabey (Lophocebus 15 Frugivorous bird calls Possibly use the calls of hornbills to locate fruiting trees
albigena)
Sooty mangabey (Cercocebus atys atys), 95–100 C. a. atys and Spatial memory and tree Fruiting trees were approached significantly faster than trees
grey-cheeked mangabey 20–25 L. a. johnstoni phenology without fruit
(Lophocebus albigena johnstoni)
Grey-cheeked mangabey (Lophocebus 18–24 Weather conditions Took into account past weather conditions when searching for
albigena johnstoni) food
Grey-cheeked mangabey (Lophocebus 20–27 Tree phenology Probably used fruiting synchrony to find available fruit
albigena)
Chimpanzee (Pan troglodytes) 5 Tree phenology Used fruiting synchrony and based their expectations of finding
fruit on a combination of different botanical knowledge (e.g.
categorisation of fruit species, rates of fruit discovery)
Chimpanzee (Pan troglodytes) 3 groups∗ Botanical and ecological Remembered the quantity and frequency of fruit production
knowledge across years; flexibly planned revisiting time to feeding trees
via efficient travel
C. Trapanese and others
Spatial foraging decisions in primates
of slope, roads) where they adjusted their direction (Noser &
Byrne, 2013). The travel to out-of-sight resources of solitary
and nocturnal mouse lemurs (Microcebus murinus) appeared to
be planned ahead since their strategy was more efficient at
detecting resources than a heuristic random travel model. In
this case too, change-points coincided with food resources
(Joly & Zimmermann, 2011). However, the authors were
unable to exclude fully the use of olfactory cues to locate
resources despite the large distances at which the change of
direction occurred.
(c) An alternative method: the Circuity Index
Garber & Hannon (1993) used another method for
determining intentionality, the Circuity Index, or the actual
distance travelled divided by the straight-line distance
between sites. They studied the foraging patterns of
moustached tamarins (Saguinus mystax) and saddleback
tamarins (Saguinus fuscicollis): the tamarins’ foraging routes
were relatively direct despite discontinuities in the canopy,
detours due to physical impediments and the risk of meeting
predators. Later, Porter & Garber (2013) and Garber
& Porter (2013) used the Circuity Index to investigate
movements between out-of-sight goals in saddleback
tamarins (Sanguinus fuscicollis weddelli): they tended to travel
in both small and large-scale space using a route-based
map, and certain areas of the forest appeared to serve
as switch points. Both spider and woolly monkeys (Ateles
belzebuth and Lagothrix poeppigii; Di Fiore & Suarez, 2007)
use preferred routes that seem to be associated with
distinct topographic features (i.e. ridge-tops). In both
species, these environmental features may constitute easily
recognised landmarks useful for spatial navigation via a
route-based map.
(d) Quantitative statistical models based on direct observations
The newest approach to the study of wild primate foraging
strategies relies on comparisons between observational
data from wild primates and predictions from quantitative
statistical models. These predictions are often derived from
null models of random searches, including factors such
as the distribution of distances moved, the distribution of
the angles turned between movements (and possibly the
interdependence between them), and the ‘tortuosity’, i.e.
the convolutedness of the path, which is inversely related
to the efficiency of the orientation mechanism involved
(see Sections II.3 and II.4) (Benhamou, 2004; Janson &
Byrne, 2007). This approach has revealed that several wild
primate species are likely to know where they are going,
remember where their resources are, and can generally
optimise their travel (e.g. Janson, 1998; Pochron, 2001;
Janmaat et al., 2006a,b; Cunningham & Janson, 2007a;
Noser & Byrne, 2013). These studies show that a topological
route-based model best explains how primates find a suitable
route and orientate in their landscape. Grey mouse lemurs
(Microcebus murinus) regularly revisit the same feeding sites,
and when leaving their nest, their departure directions are
13
not randomly distributed (Joly & Zimmermann, 2007). This
study provides, to our knowledge, the first evidence for
the relocation of stationary food resources in nature and
thereby, for spatial memory in a strepsirrhine primate. A
follow-up study on the same species revealed that, primarily
using spatial cues, mouse lemurs rapidly learn the spatial
arrangement of new feeding sites (Luhrs et al., 2009). They
showed high travel efficiency in directed movements and
the presence of a detailed mental representation of their
surroundings. Route-based goal-oriented travel was also
observed in wild lemurs (Propithecus edwardsi and Eulemur fulvus
rufus; Erhart & Overdoff, 2008) and in wild tamarins (Saguinus
mystax and Sanguinus fuscicollis weddelli; Garber & Hannon,
1993; Garber & Porter, 2013). The tamarins seem to pay
attention to near-to-goal landmarks to relocate and monitor
food availability in small-scale space and to minimise the
travelling distance between scattered feeding sites. However,
to locate resources in small-scale space primates may also rely
on olfactory cues. By comparing the animals’ movements
with different possible orientation mechanisms, it has been
shown that baboons (Papio ursinus) plan their journeys among
several out-of-sight resources in an efficient, goal-directed
way (Noser & Byrne, 2007a,b). These findings suggest that
baboons have a spatial mental representation of important
locations, i.e. possess a mental representation of several
alternative resources situated beyond their perceptual field,
thus allowing them to reach each of them. However, they
appear to be strongly tied to a network of learned sequences
of landmarks and lack the ability to compute Euclidean
relations among sites (Noser & Byrne, 2007a,b), rather using
a route-based map to find out-of-sight locations. Comparison
between foraging movements of spider monkey (Ateles geoffroyi
yucatanensis) in the wild and computer-generated simulations
revealed that they also can plan to reach more than one
resource site (Valero & Byrne, 2007; Suarez et al., 2014).
By testing several heuristic models of decision making
as possible alternative strategies (i.e. movement to core
home-range areas instead of individual trees; travel along
a sensory gradient; movement along arboreal pathway
networks without a pre-determined destination; straight-line
travel in a randomly chosen direction; random walks),
Hopkins (2016) showed that mantled howler monkeys
(Alouatta palliata) maximise resource gain while minimising
distance travelled via the integration of spatial and temporal
knowledge of food availability. For all these species, the
authors rejected the null hypothesis of random foraging
walks but all seem to lack the capacity for vector operations
characteristic of Euclidean maps. Instead they rather orien-
tate themselves using a limited number of well-established
routes.
(e) Botanical or ecological knowledge: a complementary or an
additional strategy?
In tropical forests, primates could complement their use of
sensory cues with other foraging strategies to facilitate the
discovery of newly emerged fruits (Janmaat et al., 2013b).
Primates may know where a food source is located, but use
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
14
other sensory cues to define more narrowly what is and is
not edible (Dominy et al., 2001). Sensory acuity declines with
distance; thus, primates have developed a keen spatial and
temporal memory for food location and edibility (Garber,
2000). Thus, some primates know where the resources are
(Garber, 1989; Garber & Paciulli, 1997; Janson, 2007),
when to look for them (Janmaat et al., 2006a,b) and what or
how much is likely to be available (Cunningham & Janson,
2007a,b). For example, studies on grey-cheeked mangabeys
(Lophocebus albigena) suggested that they (i) may use the calls
of hornbills to locate fruit (Olupot et al., 1997), (ii) seem to
take into account past weather conditions when searching
for food, and are more likely to approach trees with fruit at
various stages of development than empty trees of the same
species (Janmaat et al., 2006b), and (iii) seem to use cues
related to synchronous fruiting during foraging (Janmaat
et al., 2012). The latter strategy allows prediction of the
fruiting state of a large number of trees of the same species
without having to check specific trees (Janmaat et al., 2012).
In a follow-up study, Janmaat et al. (2013b) found that
chimpanzees may use botanical skills to plan and search for
food resources. Western chimpanzees (Pan troglodytes verus)
seem to combine knowledge of the synchronous emergence
of rainforest fruits with sensory cues, such as sight and smell.
They base their expectations of finding fruit on a combina-
tion of knowledge that includes prior success rates of fruit
discovery and categorisation of fruit species (Janmaat et al.,
2013b). The study suggested that chimpanzees possess some
ability to classify food trees, remembering their quantity
and frequency of fruit production across the year (Janmaat
et al., 2013a,b). They might also have a sophisticated ability
to plan revisiting of fruit trees flexibly, maximising travel
efficiency (Janmaat et al., 2014). Similarly, interviews with
hunter–gatherer Aka people suggested that they rely on
botanical information to infer seasonal variables, including
the availability of fruit on other forest plant species (e.g. the
presence of new leaves on certain tree species, for example
the young red leaves of Lophira alata, appear just before
the beginning of the fruiting season; S. Masi, unpublished
observations).
(f ) Planning ahead: integrating ecological variables to assess behaviour
goals
Janmaat et al. (2014) found that chimpanzees (Pan troglodytes
verus) leave their sleeping nests earlier when breakfasting
on highly ephemeral fruits, especially when they are
located at a distance. In addition, females positioned their
sleeping nests in the direction of the breakfast sites of the
next day more often for ephemeral fruit than for widely
available (predictable) fruit. Evidence of planning ability
beyond immediate needs was also found in male Sumatran
orangutans (Pongo abelii; van Schaik, Damerius & Isler, 2013).
The direction in which a male emits ‘long calls’ in the
morning predicts his subsequent travel direction for many
hours, and a new call indicates a change in his travel
direction. The authors argue that the ability to plan in
this way is likely to be adaptive for great apes, as well as
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
C. Trapanese and others
other taxa. Taken together these studies reveal a cognitive
mechanism, behavioural planning, by which large-brained
primates could buffer the effects of seasonal variability in food
availability and inter-specific competition while foraging.
(3) Primate navigation in virtual reality
New technologies can now be used to investigate comparative
spatial cognitive abilities in non-human primates and
humans. A virtual reality software program simulates an
experimental situation that can vary in features, scale,
and complexity concurrently allowing precise control over
variables such as landmarks (e.g. De Lillo & James, 2012;
Dolins et al., 2014). Changes to geometry of space could
allow more precise assessment of the subject’s attention to
various topographical features (De Lillo & James, 2012). The
use of virtual reality also allows researchers to obtain data
with large sample sizes relatively rapidly. Table 4 provides
a summary of studies that used virtual reality to investigate
navigation abilities in primates.
Mushiake et al. (2000) carried out one of the first studies
of this kind. In a maze ‘path-finding’ computerised task, two
Japanese macaques (Macaca fuscata) chose the shortest path
rather than approaching the target randomly. Moreover,
when some paths in the maze were blocked, they chose a new
shortest path, bypassing the obstacles. More recently, a study
comparing chimpanzee (Pan troglodytes) and human attention
to visual–spatial features during navigation revealed that
both species discriminated efficiently between positive and
negative landmarks, and used relatively efficient navigation
to successfully localise goal sites (Dolins et al., 2014). In the
most complex maze, human performance was less accurate
compared to that of one female chimpanzee. This result could
arise from a loss of capacity in humans due to our modern
lifestyle, or may simply have arisen due to the very small size
of the sample (4 chimpanzees, 16 humans). However, the
results suggest that chimpanzees and humans do learn and
respond to virtual environments similarly. Interestingly, age
differences were found in the human subjects (Dolins et al.,
2014). An increasing data set from capuchin monkeys (Cebus
apella), baboons (Papio papio), and humans now indicates clear
species differences in the perception of the global spatial
organisation of a collection of local elements in foraging tasks
(e.g. Deruelle & Fagot, 1997, 1998; Fagot & Deruelle, 1997;
De Lillo et al., 2005, 2011).
In a computerised virtual task, capuchin monkeys (Cebus
apella), but not rhesus macaques (Macaca mulatta), showed a
significant preference for a densely arranged array over a
sparsely arranged one (Parrish et al., 2017). The difference in
terms of sensitivity to density was linked to a difference in the
perceptual processing of multi-element arrays: capuchins
perceive individual items (i.e. local features) prior to
and sometimes more accurately than global configuration
(Spinozzi, De Lillo & Truppa, 2003; De Lillo et al., 2005).
By allowing us to obtain a large data set rapidly, virtual
reality could lead to a better understanding of the cognitive
mechanisms underlying spatial foraging cognition in apes,
monkeys and other animals.
Spatial foraging decisions in primates
Table 4. Studies on virtual reality navigation in primates. Number of stimuli: number of virtual goals or cues for navigation
Number of
Reference Species tested subjects
Mushiake et al. (2000) Japanese macaque 2 12 dots (goals)
(Macaca fuscata)
Dolins et al. (2014) Chimpanzee (Pan 4 P. troglodytes,
troglodytes) and 16 H. sapiens
human (Homo sapiens)
Parrish, James & Capuchin monkey 15 S. apella and
Beran (2017) (Sapajus apella), 7 M. mulatta
rhesus macaque
(Macaca mulatta)
IV. GENERAL DISCUSSION AND PERSPECTIVES
The available results from al the studies discussed above
suggest that primates can remember the locations of food
resources (e.g. Menzel, 1973; Janson, 1998, 2016; Pochron,
2001; Janmaat et al., 2006a). Studies also agree in showing
that primate travel across spatially fixed resources is often
goal-oriented: routes taken between known resources often
approximate straight lines (e.g. Janson, 1998; Pochron,
2001; Di Fiore & Suarez, 2007; Valero & Byrne, 2007;
Cunningham & Janson, 2007a,b; Noser & Byrne, 2007a,b).
Researchers often interpret primate foraging strategies in
terms of enhancing fitness (Janson & Byrne, 2007): either
by minimising the distance travelled by visiting the closest
available resources (e.g. Garber, 1989; Janson, 1998), or
by minimising the energy expenditure in multi-destination
routes, opportunistically skipping some nearby resources
(Gallistel & Cramer, 1996; Cramer & Gallistel, 1997).
Primates can choose to minimise the energy expenditure
[e.g. avoiding hills, slopes, long-distance travel (Suarez, 2003;
Di Fiore & Suarez, 2007)] or to reduce the computational
demands by using habitual travel routes (Di Fiore & Suarez,
2007; Noser & Byrne, 2007a,b). Monitoring food resources
(Janmaat et al., 2006a,b) allows some primates to return
to a patch only when it is fully recovered (Janson, 1990,
1996), thus reducing the daily overlap in foraging areas
(Di Bitetti, 2001). They can also minimise intra-group
feeding competition by visiting food patches with the highest
availability of resources (Cunningham & Janson, 2007a).
While it is now accepted that primates possess a
‘mental map’ of their foraging areas, the type of mental
representations primates use while foraging and how
information about resources (i.e. what, where and when) is
organised remain subject to debate. The Euclidean map
model is not supported conclusively in any animal (even
in chimpanzees, despite claims by Normand & Boesch,
2009). We await further investigation or the development
15
Number of stimuli Conclusions
Chose the shortest route to the
targets
8 variable goal locations, Both species able to discriminate
directional cues between positive and negative
provided by positive Landmarks; in contrast to
and negative landmarks chimpanzees and adult humans,
performance in human children
decreased as maze complexity
and size increased
2 patches with equal Capuchins showed a density bias in
number of dots (N = 12 discrimination of dense versus
or 5) and 2 patches with sparse stimuli but macaques did
unequal number of dots not
(N = 5 versus 6 and
N = 10 versus 12)
of more parsimonious and testable explanations (Bertolani,
2013). Neither is there convincing evidence of complex rules
used to plan multi-step travel routes (Poucet, 1993; Gallistel
& Cramer, 1996; Janson, 2014). The most parsimonious
hypothesis is the use of a less cognitively demanding
route-based map by primates (e.g. Byrne, 2000; Di Fiore
& Suarez, 2007; Noser & Byrne, 2007a) which relies on
landmarks and a network of established routes.
The use of statistical models to analyse field data on
animal movements has greatly increased our understanding
of primates’ spatial movement strategies. However, by
allowing investigation of only one behaviour at time, even
this approach sometimes fails to identify the mechanisms
involved precisely (Janson, 1998).
Finally, spatial movement decisions may not necessitate
the complex planning required by optimal solutions (such as
in the Travelling Salesman Problem), but will always require
processing of multiple sources of information to locate food.
Wild primates face challenges involving seasonally variable
environments, and thus learn through exploration, encoding,
recalling travel routes, orienting themselves, monitoring food
availability and finding the best strategy to minimise energy
expenditure and maximise efficiency. Movements observed
in frugivorous primates have been explained in terms of
the ‘gravity rule’ which assumes that every goal has an
attraction to the animal user proportional to the goal’s
value at a given moment and that is inversely proportional
to the distance of the goal from the user (Sen & Smith,
1995). The goal’s value can differ over time. In other words,
this is a combination of the different costs and benefits
for accessing the goal: they may depend on the forager’s
state (e.g. physiological state or predation risk; Janson, 2014)
or the relative availability of other preferred food (Sen &
Smith, 1995). We can hypothesise that long-lived species that
inhabit relatively unpredictable environments will require a
higher capacity for learning, and thus that they will possess
more developed planning capacities (van Woerden et al.,
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
16
2011). Similarly, more-terrestrial species are likely to require
more-sophisticated abilities for locating food than arboreal
species, who may be able to assess ripe fruit availability and
abundance more easily from the top of the canopy.
There is a growing body of evidence that primates
remember food locations (where) and food quality (what) but
there is still little information available concerning temporal
knowledge (when): are primates able to integrate spatial and
temporal decisions? The ability to recall specific events in
the past, termed ‘episodic memory’, has been postulated to
be uniquely human (Tulving, 2005). However, some animals
in captivity (e.g. birds, rats, chimpanzees; Allen & Fortin,
2013) behave as if they possess integrated memories of past
events, remembering what happened, where and when (Crystal,
2010), although others e.g. rhesus macaques (Macaca mulatta)
failed to perform these tasks (Hampton et al., 2005). To date,
evidence for episodic memory in wild animals is scarce. In
wild capuchin monkeys (Cebus apella nigritus), there is some
evidence for integrated memories of prior food patch use,
including where the patch is, how productive it is and
when was last visited (Janson, 2016). Wild chimpanzees
(Pan troglodytes verus) have been shown to use sophisticated
botanical and ecological knowledge to locate and relocate
food (Janmaat et al., 2013a,b, 2014, 2016).
Developing an integrative research framework of cognitive
foraging in primates would enable us to relate the cognitive
abilities of individuals directly to their foraging behaviour.
Future studies should integrate experiments on captive
animals (to control and analyse different variables) with
experiments on wild animals in which the complexity of
the natural environment is maintained. Such integration
of studies on one species should allow us to unravel the
cognitive mechanisms associated with when: knowing when
is the right time to revisit a resource and how they can
infer that. Step-by-step controlled manipulation of what,
where and when – i.e. food quality, location and distribution,
and temporal availability – is a crucial step to assess the
relative importance of those variables in primate foraging
decisions. Moreover, to clarify goal-directed foraging abilities
a deeper investigation of the effects of socio-ecological and
cognitive factors in different primate species is also crucial.
In the same framework, across-species comparisons will
allow us to investigate not only the influence of ecological
and evolutionary conditions on diet and foraging habits in
primates, but also how the ecological framework has led
to specific solutions at the level of behavioural strategies
and related cognitive capacities (Rosati, 2017). Rosati (2017)
underlined how both social and ecological factors can explain
variation in cognition, with each being relevant in distinct
cognitive domains. For example, lemurs with more complex
diets, e.g. more frugivorous species, show more sophisticated
memory and inhibitory control capacities in comparison
to more folivorous species (MacLean et al., 2013; Rosati
et al., 2014). Patterns of variation across species are very
different in terms of social cognitive capacity: ring-tailed
lemurs (Lemur catta) live in large groups with complex
dominance hierarchies (Sauther, Sussman, & Gould, 1999)
Biological Reviews (2018) 000–000 © 2018 Cambridge Philosophical Society
C. Trapanese and others
and although they exhibit intermediate performance on
several foraging cognitive tasks, they possess exceptional
socio-cognitive skills such as following gaze direction (Sandel,
MacLean & Hare, 2011) or making transitive inferences
(MacLean, Merritt & Brannon, 2008). Thus, for lemurs
foraging cognition varies with ecology, while social cognition
varies with social complexity (Rosati, 2017). However, a
similar conclusion may not be applicable to other primate
species and concerning all social cognitive skills [e.g. Theory
of Mind capacities (Call & Tomasello, 2008)]. Cognitive
social skills can also be driven by ecological correlates rather
than by social group size (e.g. Devaine et al., 2017). Indeed,
cognition likely evolved in mosaic patterns, with different
evolutionary processes shaping different cognitive domains
(Rosati, 2017).
Many views on human uniqueness focus on the special
nature of human sociality, but it has been emphasised that
humans also stand out among primates in terms of ecological
niche (Hardesty, 1972). Large-brained foragers that need a
high-energy diet to maintain their large and costly brains
(Milton, 1981; Byrne, 1997) could gain a clear evolutionary
advantage by using flexible planning to reduce unnecessary
energetic expenditure (Janmaat et al., 2014). This attribute
may have been particularly important for hominoids living
in highly seasonal habitats, probably experiencing similar
environmental challenges to those of modern primates
(Milton, 1981; Chapman et al., 2005). This proposed benefit
of flexible planning skills encourages deeper investigation into
the temporal aspects of ecological complexity (Milton, 1981;
Byrne, 1997) and of its role in brain-size evolution in hominid
and non-human primates (Zuberbühler & Janmaat, 2010).
V. CONCLUSIONS
(1) The available evidence suggests that several primate
species can memorise the locations of food resources. During
foraging, their ranges and trajectories depict goal-oriented
behaviours and the use of straight-line paths to minimise
travelling distances between sites.
(2) Spatial foraging strategies of primates have been seen in
terms of fitness-maximisation strategies. Locating ephemeral
and scattered resources such as ripe fruit in tropical forests
may have triggered the evolution of the relatively large brain
size of primates.
(3) There is growing evidence that primates use
route-based maps when foraging. This map is a topological
representation in which animals use landmarks and routes
to navigate and approximate directions and distances. To
date, there is no clear evidence for the integration of more
sophisticated cognitive maps such as the Euclidean map in
primates or in humans.
(4) Despite the growing body of literature showing that
primates remember food location and quality, very little
information is available on the extent of primate temporal
knowledge of food availability and further investigations are
needed.
Spatial foraging decisions in primates
VI. ACKNOWLEDGEMENTS
The authors thank the Ethoikos foundation (Roberto
Cozzolino in particular), the Muséum National d’Histoire
Naturelle de Paris and the Centre de Primatologie de
l’Université de Strasbourg for financial and institutional
support. We also thank Benjamin Robira and Ornella
Ferrario for their feedback on this review. We are very
grateful for the thoughtful suggestions and comments of the
anonymous reviewers.
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