.

.


  EXPLORATIONS: AN OPEN INVITATION TO BIOLOGICAL ANTHROPOLOGY


    Editors: Beth Shook, Katie Nelson, Kelsie Aguilera and Lara Braff


      American Anthropological Association Arlington, VA

2019


        CC BY-NC 4.0 International, except where otherwise noted

ISBN – 978-1-931303-63-7

www.explorations.americananthro.org


        Karin Enstam Jaffe, Ph.D., Sonoma State University


          Learning Objectives

  * Describe the behavioral variation that exists within the Primate
    Order and how primate behavior and morphology are influenced by
    diet, predation, and other ecological factors.
  * Explain why primates live in groups.
  * Distinguish primate social systems from mating systems.
  * Contrast male and female reproductive and parental investment
    strategies.
  * Describe the ways in which primates communicate.
  * Evaluate the evidence for primate cultural variation.

Nonhuman primates from now on simply referred to as “primates”) are our
closest living relatives, and their behavior is often strikingly similar
to our own. If you’ve ever seen a female monkey at your local zoo cooing
over her newborn baby Figure 6.1a) or watched a video of a tufted
capuchin monkey using rocks as a hammer and anvil to crack open a nut to
access the edible kernel inside Figure 6.1b), then you know how
interesting they can be.

Figure 6.1a

Figure 6.1b

I have been fascinated by primates since I was a young child. In the
summer of 1996, I went with my dissertation advisor, Dr. Lynne A.
Isbell, to her field site in Laikipia, Kenya Figure 6.2) with the
intention of studying the play behavior of juvenile patas monkeys. One
day we were following our patas study group when several females and
juveniles began giving high-pitched “nyow” alarm calls. I was awestruck
as I watched the entire group take off at breakneck speed. Patas monkeys
are, after all, the fastest primate, capable of running 20 miles per
hour for short distances. It did not even occur to me that they had
sounded an alarm and then run away from something—until my advisor
pointed to the lioness hidden in the grass at the base of a tree. We
slowly backed away and got in our car.) My research interests changed in
that moment: I wanted to study primate antipredator behavior, the
strategies primates use to escape from predators. I would spend two
years at that same field site collecting data on anti-predator behavior
of patas monkeys and vervets, two closely related species who occupy
different habitats. Patas monkeys Figure 6.3a) live far from rivers, in
habitats composed of short trees spaced far apart Figure 6.3b). These
trees have little to no overlapping canopy, so climbing one to escape a
lion in pursuit can result in a literal dead end. In contrast, vervets
Figure 6.4a) spend most of their time along rivers, with access to tall
trees with overlapping canopies

Figure 6.2

Figure 6.4b) that provide good escape routes from terrestrial predators.
But they also venture into patas habitats, the short trees with canopies
that do not overlap. I wanted to know: How would the structure of these
habitats affect the responses of vervets and patas monkeys to alarm
calls that signal the approach of a terrestrial predator like a lion?
Not surprisingly, when vervets are near the river, they climb the tall
trees to seek refuge from such predators. But not patas monkeys. These
“cheetahs of the primate world” are more likely to take off running as I
had seen them do that summer), even bypassing nearby trees. Their
physical adaptations for speed, like their long legs, combined with the
lack of arboreal escape routes, makes fleeing on the ground their best
option. But what do vervets do when they are away from the river and the
safety of their tall trees? Is their behavior “hard-wired” so that their
response to an alarm call is the same, regardless of the habitat? Or do
they assess key aspects of their habitat, like tree height and canopy
cover, and alter their behavior? Although they cannot run as fast, when
they hear an alarm call they run back toward the river, by-passing the
short trees, just like the patas do Enstam and Isbell 2002). The
implication is clear: these monkeys, our close relatives, with their
highly developed intelligence and ability to learn, do assess key
features of their habitat and use this information to alter their
behavior and maximize their chance of escape.

Figure 6.3a and 6.3b A female patas monkey with infant (left). A patas
habitat in Laikipia, Kenya (right).

Figure 6.4a and 6.4b A female vervet (left). A vervet habitat in
Laikipia, Kenya (right).

The branch of science that focuses on the study of primate behavior is
called primatology, and people, like myself, who study primates Figure
6.5) are called primatologists. Primatologists come from many different
disciplines and study primate behavior for different reasons. Biologists
study primates as examples of evolutionary theories like natural
selection or parental investment. Primate intelligence is of interest to
psychologists who want to learn more about the underlying cognitive
principles involved in deceptive or cooperative behavior and to
linguists interested in the principles of communication and language.
Ecologists studying conservation issues examine how primates are
affected by deforestation, poaching, or illegal animal trade. Biological
anthropologists, like myself, who study primates are interested in their
social complexity and ecological and behavioral variation. Because both
humans and most nonhuman primates live in groups, biological
anthropologists study primates to better understand the evolution of
social behavior and its costs and benefits. Because primates are our
closest living relatives, we study them to gain insights into how our
human ancestors may have behaved as well as to better understand our own
behavior.


  ECOLOGY

Figure 6.5

The more than 600 species and subspecies of living primates are highly
diverse in their dietary preferences and the habitats they occupy. These
aspects of primate ecology have significant impacts on every part of a
primate’s life, including their morphology, physiology, and body size as
well as their interactions with other individuals inside and outside
their social group. They even play a role in determining whether a
primate lives in a group or is solitary and lives alone. A primate’s
habitat determines the food to which they have access and the community
of other species with whom they interact, including predators.


    Primate Diets

Diet may be the most important variable influencing variation in primate
morphology, behavior, and ecology, and primate diets are highly varied.
Some primatologists separate foraging, the act of finding and handling
food, from feeding, the act of consuming food, while others combine
these into one category. Most primates are omnivores who ingest a
variety of foods in order to obtain appropriate levels of protein,
carbohydrates, fats, and fluids, but one type of food often makes up the
majority of each species’ diet. Because you learned about the dental and
digestive adaptations experienced by frugivores who feed primarily on
fruit), folivores whose diet consists mostly of leaves), and
insectivores who eat mainly insects) in Chapter 5, we will not discuss
them here. Instead, we will focus on the relationship between diet and
body size and the variation in food abundance how much is available in a
given area) and distribution how it is spread out).


      Body Size and Diet

As you learned in Chapter 5, insects are a high quality food. Full of
easily digestible protein and high in calories, insects are an excellent
source of nutrients, meeting most of a primate’s dietary needs. Although
all primates will eat insects if they come Figure 6.6b A mountain
gorilla eating leaves. upon them, those species that rely most heavily
on insects tend to be the smallest. If insects are such a high-quality
food, why aren’t all primates insectivores? The answer is that larger
primates simply cannot capture and consume enough insects every day to
survive. This is because the basal metabolic rate BMR), or the rate at
which energy is used to maintain the body while at rest, increases more
slowly than body size. The result? Heavier animals must consume
absolutely more food, but they have a slower metabolism so they need
fewer calories per unit of body weight. Because of their small size less
than 150 g), tarsiers do not need to consume large amounts of food each
day, but their high metabolic rate means they convert food into energy
very quickly. This is only possible by consuming food that is easily
digestible, like insects. It does not matter to a tarsier that a
grasshopper only weighs 300 mg, because the tarsier itself is so small
that one grasshopper is a good-size meal Figure 6.6a). However, an adult
male gorilla, who may weigh up to 200 kilograms, cannot possibly consume
enough insects to meet its caloric needs. And it does not need to.
Because of their large body size, gorillas have a much lower metabolic
rate than tarsiers, so they can consume low-quality food, like leaves,
and take their time digesting it, so long as they get enough Figure
6.6b). Fortunately for gorillas, leaves are plentiful, as we will see in
the next section. Most medium-size primates are highly frugivorous.
Whether they supplement their high-fruit diet with insects or leaves
also depends on their size. Smaller frugivores tend to supplement with
insects, while larger frugivores tend to supplement with leaves.

Figure 6.6a


      Food Abundance and Distribution

Figure 6.7a

Nutrients see Chapter 5) and food quality are not the only dietary
considerations primates must make. They must also ensure that they
consume more calories than they burn. The abundance and distribution of
food affect energy expenditure and calorie intake because they determine
how far animals must travel in search of food and how much they must
compete to obtain it. Abundance refers to how much food is available in
a given area while distribution refers to how food is spread out. Food

abundance is either plentiful Figure 6.7a) or scarce area.

Figure 6.7b). Food is distributed in one of three

Figure 6.7b

ways: uniformly Figure 6.8a), in clumps Figure 6.8b), or randomly Figure
6.8c). In general, higher-quality foods, like fruit and insects, are
less abundant and have patchier distributions than lower-quality foods,
like leaves. In a rainforest, like the Amazon, every tree has leaves, so
they are abundant and uniformly distributed Figure 6.9a). Folivores do
not have to travel very far to find food so they do not burn many
calories searching for food. In comparison to leaves, fruit is scarce
and clumped Figure 6.9b). Because not every tree contains fruit, it is
less plentiful than leaves. In addition, in a rainforest, a single tree
with fruit may be surrounded by many trees without fruit. To a
frugivore, this one fruit tree is a clump of fruit. Frugivores who do
not eat leaves must travel farther distances in search of food because
they can only feed in some trees i.e., those producing fruit).
Frugivores burn more calories searching for food than folivores, so it
is a good thing that fruit is such a high-quality food. Lastly, insects
are scarce, and due to their mobile nature, most are randomly
distributed Figure 6.9c). This combination makes it impossible for
larger primates to rely on insects for a significant part of their diet.

Figure 6.8a

Figure 6.9a

Figure 6.8b

Figure 6.9b

Figure 6.8c

uniform nor clumped distribution.

Figure 6.9c

It is important to remember that species preferences for specific types
of food may cause it to exist in abundance or distribution that is
different than the general patterns we’ve discussed here. For example,
for folivores who prefer young i.e., immature) leaves, their food supply
is patchier and less abundant than it appears to a researcher looking at
the lush green carpet of the Amazon forest because only some leaves are
immature at any point in time. During fruiting season, when many trees
are producing fruit, fruit may be temporarily abundant and less clumped.
Similarly, some insects, like termites in a termite mound Figure 6.10),
are found in clumps, similar to the way a single fruit tree is a “clump”
of fruit surrounded by trees with no fruit.


    Competition for Food

When a resource that is important for survival or reproduction is
scarce, individuals will compete to obtain that resource. This is a
central tenet of Charles Darwin’s theory of evolution by natural
selection see Chapter 2). Because female primates like all mammals)
devote a lot of energy to offspring production and care discussed in
detail in the “Parental Investment” section of this chapter), especially
while pregnant and nursing, they compete for access to food, so long as
the food is worth competing for. Competition between primates takes two
forms: Individuals engage in direct competition e.g., fighting) over
resources that are large and worth defending fruit is a good example of
a food resource over which primates will fight) or individuals engage in
indirect competition e.g., eating food before another individual gets to
it), which occurs when a resource is small or not worth defending.
Primates often engage in indirect competition for insects, like
grasshoppers, that are eaten quickly Figure 6.6a). Primates may engage
in direct and/or indirect competition with members of their own group or
with members of other groups.

Effects of Food Abundance and Distribution on Interactions Between and
Within Groups

Figure 6.10

notable exception are termite mounds, like this one in Tanzania, where,
inside the mound, insects are abundant and clumped.

The amount, or abundance, of food determines the nature of competition
between different groups Isbell 1991). Between-group competition is seen
in terms of changes to home range size and nature of interactions
between groups. A group’s home range is the area over which the group
moves in search of food. Groups that defend the boundary of their home
range are said to occupy a territory. Consider a patch of forest covered
in leaves e.g., Figure 6.9a). If you are a folivore, every tree is a
dinner table. When your group size increases, your home range does not
expand because there is more than enough food for everyone, and it is a
waste of energy to travel farther than you need to. And as long as your
group does not expand its home range, you will not encroach on the trees
of neighboring groups. This keeps competitive interactions between
groups of folivores to a minimum. Now imagine you are a frugivore.
Unlike leaves, not every tree has fruit on it. Maybe only two or three
trees are in fruit at any given time, so fruit is scarce Figure 6.9b).
Thus, if your group size increases, it is likely that the few fruit
trees available in your current home range will not be able to feed
everyone. If that’s the case, then your group will need to expand its
home range in search of additional fruit trees, which are in the home
ranges of neighboring groups. Home-range expansion is also often
accompanied by fighting between groups as members attempt to keep
intruders away from valuable, scarce food resources.

While food abundance determines interactions between groups, food
distribution determines the interactions between individuals within a
group Isbell 1991). Competition within a group is marked by changes in
day-range length and the presence of dominance hierarchies. Day-range
length measures the distance a group must travel in a single day in
search of food. A dominance hierarchy reflects the place of each
individual in the group in comparison to others. An individual’s place
in the hierarchy, or “rank,” determines their priority of access to
resources. If food is evenly distributed as with leaves; Figure 6.9a),
individuals can spread out while feeding so that their day-range length
does not increase when their group size increases. Likewise, because
leaves are “everywhere,” there is little benefit to females engaging in
interactions that determine “priority of access” to resources, so
dominance hierarchies are uncommon among folivores. However, if food is
clumped as with fruit; Figure 6.9b), individuals in groups must feed in
more cohesive units i.e., all in one fruit tree). When group size
increases, the group must travel farther each day in order to visit
enough fruit

trees to feed all group members. Likewise, when food is clumped,
individuals have the opportunity to monopolize it and keep others from
feeding. Under such circumstances, females benefit from competing with
one another for “priority of access” to the resource, and dominance
hierarchies result.

The fact that food abundance and food distribution vary independently
helps us understand the complex nature of between-group and within-group
interactions Isbell 1991). For example, both olive baboons and patas
monkeys feed on scarce resources, and both species engage in competition
with other groups and expand their home-range size when food is in short
supply. But olive baboons’ food is clumped while patas monkeys’ is
dispersed, so the interactions within groups are very different. Female
baboons have a strong dominance hierarchy, and the distance they travel
each day increases with group size. Patas monkeys have a weak dominance
hierarchy, and when group size increases, individuals spread out while
feeding and daily travel distance does not increase.


    Community Ecology

Figure 6.11a

In addition to interactions with other members of their own group and
other groups of conspecifics members of the same species), primates are
members of broader ecological communities composed of other species,
including other primates, predators, and even humans. When two species
or populations) occupy the same geographic area, they are sympatric. The
patas monkeys and vervets that I studied in Kenya, along

with olive baboons and Senegal bush babies, are sympatric and form a
primate Figure 6.11b A vervet. community Figure 6.11a–d). However,
vervets Figure 6.11b) and muriquis of Brazil Figure 6.12) are
allopatric, meaning their geographic ranges do not overlap. Some
habitats support highly diverse primate communities consisting of 10 or
more species Figure 6.13). How can so many species of primate occupy the
same area and avoid competition? Sympatric species do sometimes compete
with each other.

Figure 6.11c

Observations of one species displacing another at a food site is a sign
of competition between the two species. When this happens, usually it is
the large bodied species that supplants the small-bodied species. The
exception is when the small bodied species significantly outnumbers the
larger-bodied one. The competitive exclusion principle states that two
species that compete for the exact same resources cannot coexist. This
means that two species cannot occupy the same niche—cannot seek to meet
their needs for food and shelter in the exact same way. Because tropical
rainforests are highly variable, with many habitats and many Figure
6.11d A Senegal bush baby. sources of food and shelter, there are many
different niches for multiple species

Figure 6.12

to exploit, and large primate communities result Figure 6.13). In non
rainforest habitats, like Kenya’s open woodland, which is home to four
species Figure 6.11a–d), there are fewer niches for multiple species to
occupy. Regardless of habitat type, sympatric species avoid competition
through niche partitioning using the environment differently). Niche
partitioning includes differences in diet, ranging behavior, and habitat
use. In Laikipia, Kenya, bush babies reduce competition with vervets by
feeding more heavily on insects. They further reduce competition by
being nocturnal while vervets are diurnal. Even though bush babies
Figure 6.11d) and vervets Figure 6.11b) do sometimes eat the same food,
since they eat at different times of day they rarely, if ever, interact.

Site 	Primate Community
Krau Game Reserve, Malaysia 	white-handed gibbon, siamang, dusky leaf
monkey, mitered leaf monkey, long-tailed macaque, pigtail macaque, slow
loris
Manu National Park, Peru 	black spider monkey, red howler monkey, brown
capuchin, white-fronted capuchin, South American squirrel monkey, owl
monkey, dusky titi monkey, common woolly monkey, monk saki monkey,
Goeldi’s marmoset, emperor tamarin, saddleback tamarin, pygmy marmoset
Beza Mahafaly Reserve, Madagascar 	ring-tailed lemur, Verreaux’s sifaka,
white-footed sportive lemur, reddish-gray mouse lemur
Kibale National Park, Uganda 	Ugandan mangabey, L’Hoest’s monkey,
Ugandan red colobus monkey, vervet monkey, olive baboon, blue monkey,
grey-cheeked mangabey, potto, galago, black and white colobus monkey,
chimpanzee

Figure 6.13 Examples of primate communities.


    Predation

Figure 6.14a

An important aspect of primate communities is the predators that also
occupy them. As discussed in the “Primate Diets” section, all primates
incorporate some insects into their diet, and so they may be themselves
considered predators in this respect. In this section, we will limit our
discussion to predation of and by vertebrates animals with an internal
spinal column or backbone). Many primates incorporate some vertebrate
prey into their diet. Often, predation by primates is opportunistic,
occurring because the prey happen to be in the right place at the right
time. I’ve observed vervets opportunistically killing lizards by
smashing them against a rock

Figure 6.14b

or tree trunk and eating them much as this lion-tailed macaque has done;
Figure 6.14a). In some parts of their range including Gombe Stream
National Park and Mahale Mountain National Park, both in Tanzania),
chimpanzees are described as opportunistic hunters, with the vast
majority of hunts occurring after a chance encounter with prey Figure
6.14b; Boesch and Boesch 1989). Other primates are more deliberate
predators, and some even work together to increase their chances of
success. Cooperative hunting has been observed in white-faced capuchins
and some chimpanzee populations. White-faced capuchins hunt more often
during the dry season, when other food is scarce, and sometimes work
together to chase, surround, and capture small mammals like young
squirrels or coatis Fedigan 1990). The chimpanzees of Taï National Park
in Côte d’Ivoire take deliberate, cooperative hunting to the next level.
Unlike their Tanzanian counterparts, they form hunting parties to search
for red colobus monkeys and, once located, anticipate the prey’s
movement and coordinate with other hunters to drive, isolate, and
capture prey Boesch 2002). Since hunting-party size correlates with
hunting success, it is not surprising that sharing the spoils of a
successful hunt is more common in Taï chimpanzees who rely on others for
success Boesch and Boesch 1989).

All primates are susceptible to predation by mammalian carnivores
animals whose diet consists primarily of animal tissue) Figures 6.15a–
d), birds of prey Figures 6.15e-f), and/ or reptiles Figure 6.15g),
although the specific predators differ based on geography and primate
body size. Smaller primates fall prey to a wider range of predators than
larger primates, and some habitats contain a greater diversity of
predators. Primates use a variety of anti-predator tactics to avoid and/
or escape predation. Perhaps the best way to avoid predation is to avoid
being detected by predators in the first place, and some primates use
crypsis to great effect.

Nocturnal primates are often small and solitary or live in very small
groups. If you are already hard to see because you are active at night,
moving quietly in small groups is a good strategy to avoid detection by
predators. The slow loris of Southeast Asia exemplifies this strategy
Figure 6.16). Nocturnal and solitary, the slow loris moves slowly as its
name suggests) and quietly as its primary strategy to avoid predation
Wiens and Zitzmann 2003). If detected, however, the slow loris will
attempt to escape by releasing its grip and falling off the branch or
biting in defense.

Figure 6.15a

Figure 6.15c

Figure 6.15b

Interestingly, the slow loris is the only venomous primate. The venom is
formed when the slow loris combines oil from a gland on its arm with its
saliva Nekaris et al. 2013). It can either apply the venom to its head
for protection or store it in the mouth to deliver through a bite. Slow
loris bites are painful and take a long time to heal. In extreme cases,
individuals who are bitten may go into shock and die. It is not as easy
for diurnal primates to avoid

Figure 6.15d

detection by predators, and most but not all) diurnal primates, like
Hanuman langurs, have larger body sizes and live in groups Figure 6.17).
Indeed, anti-predator behavior, including vigilance, alarm calling, and
mobbing, may be one of the primary benefits primates get from living in
groups; we will discuss these behaviors in a later section, entitled
“Why do Primates Live in Groups?”

Figure 6.15e

Figure 6.15f

Figure 6.15g

Figure 6.16

Figure 6.17


  SPECIAL TOPIC: PRIMATE CONSERVATION

There are over 600 species and subspecies of primates on the planet
today, and almost half of them live under the threat of extinction.
While there are many threats to primates, habitat destruction and
hunting are the leading causes of population decline Figure 6.18a–b).
Primate populations have withstood small-scale forest clearing and low
levels of hunting by local human groups for hundreds of years. However,
the recent, intense pressure of expanding human populations on many
primate habitats is resulting in rapid population declines for many
species. The majority of primates live in tropical habitats, and the
loss of tropical forest, whether due to logging or farming, is the
single greatest factor contributing to the decline of primate
populations across the planet. Between 1973 and 2010, almost 100,000 km2
of orangutan habitat was cleared for palm oil plantations in Borneo
Figure 6.18a). During this same time, the orangutan population decreased
from almost 300,000 to 100,000, an average loss of more than 5,000
orangutans every year. As of 2017, that number may be as low as 60,000
Schwitzer et al. 2017). If this rate of loss is not curtailed, the
Bornean orangutan will go extinct in less than 15 years. Hunting,
whether for bushmeat Figure 6.18b), trophies, or the pet trade, has had
devastating effects on many primate populations. Even though Grauer’s
gorillas are legally protected, they are highly prized for bushmeat
because they are relatively easy to track and shoot, and their large
body size yields significant amounts of meat. Survey work has revealed
that the Grauer gorilla population has declined significantly since the
1990s, due almost entirely to illegal hunting. The gorilla population in
Kahuzi-Biega National Park, in Democratic Republic of Congo DRC), is
estimated to have declined 87% since 1994 Schwitzer et al. 2017). As
consumers and concerned citizens, all of us are learning how to use our
wallets to combat habitat and species loss. We do not buy palm oil or
products made with palm oil in an effort to save orangutans. We donate
to conservation organizations doing important on-the-ground work in
Democratic Republic of Congo and other conservation hot-spots. We
educate ourselves as well as our friends, families, and communities
about the plight of endangered primates. Primatologists, too, contribute
to conservation efforts. No longer is primatology research restricted to
the “ivory tower” of academia. Current and future primatologists have
the opportunity to affect real change in primate conservation Chapman
and Peres 2001). Whether understanding the mechanisms that determine
species abundance, predicting the effects of human activity on species
survival, documenting patterns of environmental change, understanding
the effects of species removal in broader contexts, or evaluating
different approaches to conservation, information gained from

Figure 6.18a

Figure 6.18b

primate studies offers some of the best hope we have for a future that
continues to include our closest living relatives. You can learn more
about primate conservation in Appendix B.


  SOCIALITY, RESIDENCY PATTERNS, AND DISPERSAL

The majority of mammal species are solitary, with individuals living
alone, except for mothers and dependent offspring. However, most primate
species live in groups. Primate groups vary in size, composition, and
cohesiveness. Gibbons and siamangs of Southeast Asia and titi monkeys of
South America form long-term pair bonds with groups consisting of an
adult male and female with their dependent young. Ukaris of South
America and ring-tailed lemurs of Madagascar both live in groups of up
to 35 individuals containing multiple adult males and females,
juveniles, and infants. Gorilla troops typically number between eight
and 10 individuals, consisting of multiple females, juveniles, and
infants but only one adult male, the silverback. Some primate groups
like gorillas, ukaris, and ring-tailed lemurs) are stable and cohesive
over long periods, except for the dispersal of some individuals who
leave the group. Others, like chimpanzees and spider monkeys, have more
fluid social systems, called fission-fusion, where groups break up and
reunite based on differences in food availability throughout the year.
In this section, we’ll examine why primates live in groups and who
stays, who goes, and why.


    Why Do Primates Live in Groups?

Because group living is relatively unusual among mammals but quite
common among primates, a central question for primatologists is: Why do
primates live in groups? The answer is that primates live in groups when
the benefits of feeding competition and/or predation avoidance exceed
the costs.


      Feeding Competition

As discussed in the previous section, when species feed on high-quality,
scarce food like fruit), larger groups mean there are more individuals
competing for access to the resource. The result of this competition
takes the form of dominance hierarchies and increased day-range length.
A dominance hierarchy is the result of aggressive and submissive
interactions, but once established, a dominance hierarchy functions to
reduce levels of aggression because all individuals “know their place.”
Female vervets illustrate the costs and benefits of different dominance
ranks Whitten 1983). Dominant high-ranking) females spend more time
feeding and eat more ripe fruit than subordinates low ranking), so they
consume more nutrients. This affects their health and fitness an
individual’s reproductive success relative to that of other individuals;
Whitten 1983). Dominants weigh more, start reproducing earlier, and
produce more offspring than subordinates do. So why do subordinate
females remain in the group? The answer is that larger groups are more
successful in competition with other groups. In a long-term study of
vervets in Kenya’s Amboseli National Park, larger vervet groups had
larger and better home ranges, which importantly included access to
permanent sources of water. The result? Females in larger groups had
shorter interbirth intervals the average length of time between one
birth and the next) and higher average infant and female survival rates
than the smallest group. In terms of competition for resources, the
benefits of being a member of a larger vervet group even a low-ranking
member) outweigh the costs

Cheney and Seyfarth 1987).


      Predator Avoidance

While D. L. Cheney and R. M. Seyfarth 1987) found that larger vervet
groups had higher average infant and female survival rates, causes of
mortality differed based on group size. Unlike the small group,
mortality in larger groups was almost entirely due to predation, and
this highlights another set of costs and benefits of group living.
Larger groups are more conspicuous than smaller groups. This is one of
the reasons that primates who rely on crypsis to avoid predation like
the slow loris; Figure 6.16) are often solitary. However, some anti-
predator behaviors, like shared vigilance duties, alarm calling, and
mobbing, are responses to predators that are only available to group-
living species like Hanuman langurs; Figure 6.17). Whether or not a
primate is group-living or solitary, it engages in some form of
vigilance, or watchful behavior to detect potential danger. Often,
researchers cannot determine whether vigilance is intended to detect
predators or potential competing conspecifics with predator detection as
a side benefit). However, because vigilance interferes with other
important behaviors like feeding, resting, or being social, primates who
live in groups benefit from sharing the cost of vigilance and reaping
the rewards of early predator detection. When a predator is detected, an
alarm call is given. We will discuss the information communicated
through alarm calls in greater detail in the “Communication” section,
but in short, they serve one of two functions: 1) to alert members of
the group to the presence of a predator or 2) to alert the predator that
it has been detected. In some species, mobbing the act of cooperatively
attacking or harassing a predator) accompanies alarm calls. Mobbing
involves two or more individuals making repeated advances on a predator,
often while vocalizing and/or displaying. The point of mobbing is to
drive off or distract the predator long enough for others to escape.
Primates have been observed mobbing several species of predators,
including chimpanzees, leopards, and eagles, but snakes are the most
common targets. Although mobbing often occurs as the predator is
approaching, in some cases, it occurs after a predator has attacked and
escalates to a counter-attack. A group of Coquerel’s sifaka mobbed a
Madagascar ground boa that had grabbed and was constricting an adult
female. The attack, which consisted of loud alarm calls, along with
multiple individuals biting and scratching the snake’s body and head,
resulted in the snake releasing the female sifaka, who survived Gardner
et al. 2015). Similar reports of mobbing resulting in the rescue of a
group member from the coils of a boa constrictor have also been reported
for white-faced capuchins and moustached tamarins. Such examples clearly
illustrate the benefits of group living.


      Polyspecifc Associations

In regions with a large number of sympatric primate species Figure
6.13), interactions between species are bound to occur. Often
interactions are competitive more on this in the “Competition for Food”
section). However, polyspecific associations are different. These are
associations between two or more different species in which at least one
species changes its behavior to maintain the association. Polyspecific
associations have been documented in many New World and Old World
primate communities. While some associations are short in duration,
others can be semi-permanent. In these cases, species are found more
often in association than not. As discussed above, decades of research
indicates that primates obtain benefits from living in groups with
conspecifics. So why do some primates form associations with other
species instead of increasing the size of their own group? Although the
specific costs and benefits of polyspecific associations differ in each
case, in general, species that form these associations gain foraging or
anti-predator benefits while avoiding within-group competition for food
that occurs in a larger group of conspecifics.

There are many possible foraging benefits of polyspecific associations.
In some cases, one species gains access to a food resource that is
otherwise inaccessible. In Manu National Park, in Peru, brown capuchins
chase smaller squirrel monkeys away from scarce resources. Despite this,
squirrel monkeys maintain the association because the capuchins can
crack open palm nuts that squirrel monkeys cannot. Squirrel monkeys then
feed on kernels dropped by the capuchins Terborgh 1984). In Brazil,
saddle-back tamarins obtain a slightly different foraging benefit by
associating with moustached tamarins. The larger in body and group size)
moustached tamarins flush insects from the upper canopy as they forage.
The fleeing insects are captured at high rates by saddle-back tamarins
foraging below them Peres 1992). In other cases, associated species
avoid competition for food. In Makokou, Gabon, associations form between
greater spot-nosed guenons, moustached guenons, and crowned guenons,
despite the fact that these closely related species have very similar
diets. Instead of competing for food, the species benefit from reduced
indirect competition. Because they encounter food sites together, they
avoid visiting a site that might have been depleted by one of the other
species if they were foraging separately Gautier-Hion et al. 1983).

In other cases, the benefit of polyspecific associations is predator
avoidance. Like foraging benefits discussed above, anti-predator
benefits are variable. In some cases, one species may be particularly
good at detecting a specific type of predator and may alert the other
species to its presence. In Makokou, Gabon, the guenon species discussed
above play different alarm call roles when associated Gautier-Hion et
al. 1983). Moustached guenons, who spend more time close to the ground,
are usually the first to alarm call at terrestrial predators. Crowned
guenons, who spend more time high in the forest canopy, are most likely
to detect aerial predators. Because both species give an alarm call
familiar to the other species in the association, everyone benefits from
increased predator detection. Sometimes associations result in proactive
defense against predators. In the Una Biological Reserve in Bahia,
Brazil, a mixed-species group of golden headed lion tamarins and black-
tufted ear marmosets was observed jointly mobbing an ocelot Raboy et al.
2008). In Taï National Park in Côte d’Ivoire, putty-nosed guenons join
Diana monkeys in coordinated mobbing of crowned eagles

Eckardt and Zuberbühler 2004).


    Dispersal: Who Goes, Who Stays, and Why?

Whether primates live in groups or are solitary, some individuals must
disperse, or leave the place or group of their birth. In the solitary
orangutan, females spend about seven years caring for each highly
dependent offspring. But once mature, offspring of both sexes leave
their mother’s home range. If this did not happen, orangutans would not
be solitary. In group-living species, one or both sexes must disperse at
sexual maturity. Which sex disperses depends on the relative costs and
benefits to each. In most primate species, males are the dispersing sex
because the benefits of dispersal, including increased access to mates
and reduced competition from other males, outweigh the costs. For most
female primates, the opposite is true: they usually benefit from
remaining philopatric, or in the group of their birth. This allows them
to maintain strong social alliances so that they can compete
successfully against other groups for food. In species where females are
typically philopatric, like vervets and macaques, female dispersal only
occurs under extreme circumstances, such as when group size falls to
precariously low levels. Despite the patterns discussed below, it is
important to remember that there is considerable variation in dispersal
and numerous exceptions to any rule. Although uncommon, female dispersal
has been observed in typically female philopatric species like capuchins
and baboons. Likewise, female philopatry has been recorded in species
like chimpanzees and muriquis, whose females typically disperse. These
exceptions underscore the high degree of behavioral variation and
flexibility displayed by primates.


      Costs of Dispersal

Transferring into a new group can be fraught with difficulties. Members
of both sexes may experience aggression from same-sex members of their
chosen group because they are viewed as potential competitors.
Aggression toward transferring individuals has been documented in
multiple species, and aggression directed toward transferring males is
almost universal and can be lethal Isbell and Van Vuren 1996). During my
fieldwork in Kenya, a subadult male patas monkey who had recently
dispersed attempted to return to the group into which he was born, which
happened to be our study group. The resident male attacked him and
severely wounded him. We did not see the subadult male again and assume
he died. Transferring females can also experience aggression. Female red
howler monkeys are often prevented from joining established groups and
can be injured by resident females when they attempt to do so Crockett
and Pope 1988). Even if new group mates are not aggressive, the
dispersing individual has lost all alliances with members of their old
group and must expend time and energy developing relationships with
members of the new group. New group members are often lower in the
dominance hierarchy and may produce fewer offspring and suffer from
greater mortality. Individuals who disperse into an unfamiliar home
range must contend with a lack of ecological knowledge. For species who
feed on clumped and seasonal resources like fruit, the lack of knowledge
about food sites in a new area can be a significant cost. Lack of
knowledge about predators can also put dispersing individuals at greater
risk, as appears to be the case for vervets. When their trees
deteriorated, vervets in Amboseli National Park, in Tanzania, began to
shift home ranges. Use of unfamiliar areas correlated with an increase
in vervet disappearances. Most were suspected to have died from leopard
predation, probably due to a lack of knowledge about escape routes and
refuges in unfamiliar areas Isbell et al. 1990). Individuals who lose
both social allies and knowledge of a specific area when they disperse
may suffer even higher costs Isbell and Van Vuren 1996).


      Benefts of Dispersal

If the costs are so high, why do individuals disperse at all? The answer
to this question depends on whether we look at the immediate cause of
dispersal or the reproductive consequences over the long term. In the
short term, the cause of dispersal is often eviction by same sex members
of the group, as occurs in gibbons, ring-tailed lemurs, red howler
monkeys, and other species. In Hanuman langurs, the resident male may be
kicked out by bachelor males who invade heterosexual groups during the
breeding season. In other cases, maturing individuals may choose to
leave their group because they are attracted to individuals in another
group. This explanation is supported by the observation that most
transfers by males between groups occur during the breeding season, when
females are sexually receptive, or ready to mate. Among hamadryas
baboons of Ethiopia, one cause of female dispersal is abduction of
juvenile females by adult males. The male incorporates the female into
his harem and mates with her when she reaches adulthood Swedell and
Schreier 2006). In chimpanzees, females disperse because males gain
significant benefits from remaining in their natal group the group into
which they are born). These benefits include hunting cooperatively and
patrolling the community boundary together Lutz et al. 2016; Stumpf et
al. 2009). Other explanations for dispersal are related to enhancing
reproductive success, or one’s genetic contribution to future
generations, often measured through number of offspring produced. A male
may disperse to enter a group with fewer same-sex individuals, so as to
avoid competition for mates. Likewise, dispersing into a group with more
members of the opposite sex can increase an individual’s mating
opportunities. Perhaps the most common explanation for dispersal of at
least one sex from the perspective of reproductive success is to avoid
inbreeding, or mating with close relatives. When close relatives mate,
the likelihood that the offspring will inherit two copies of a recessive
gene increases. If the trait that these recessive genes code for is
harmful, then such matings can result in inbreeding depression, or
reduced fitness of the population. Evidence for inbreeding avoidance as
an explanation for dispersal includes the fact that natal dispersal, or
dispersal out of the group of one’s birth, takes place at sexual
maturity and that at least one sex always disperses.


  REPRODUCTIVE STRATEGIES

It is important to recognize that primate reproductive strategies have
evolved to maximize individual reproductive success. These strategies
are divided into those dealing with offspring production and care
parental investment) and those that maximize mating success sexual
selection). Because the reproductive physiology of male and female
primates differs males produce sperm and cannot gestate or lactate;
females produce eggs and gestate and lactate), males and females differ
with regard to parental investment and sexual selection strategies.
Female strategies, on the one hand, focus on obtaining the food
necessary to sustain a pregnancy and choosing the best male s) to father
offspring. Male strategies, on the other hand, focus on obtaining access
to receptive females.


    Parental Investment

Biologically speaking, parental investment is any time or energy a
parent devotes to the current offspring that enhances its survival and
eventual reproductive success) at the expense of the parent’s ability to
invest in the next offspring Trivers 1972). Female primates invest more
heavily in offspring than males. Even before conception, females produce
energy-laden eggs, and will be responsible for sustaining a fertilized
egg until it implants in the uterus. After that, they invest in
pregnancy and lactation Figure 6.1a). Because all of this investment is
energetically expensive, female primates can only produce one offspring
or litter) at a time. A species’ interbirth interval is determined by
the length of time necessary to maximize each offspring’s survival
without jeopardizing the female’s ability to produce the greatest number
of offspring possible. If a female invests too little i.e., weans an
offspring too early), she may give birth to many offspring, but very few
if any) of them will survive. If she invests too much i.e., nurses an
offspring even though it could be weaned), she ensures the survival of
that individual offspring but will not be able to produce very many
during her lifetime. To maximize her reproductive success, a female must
invest just long enough to ensure the greatest number of offspring
survive to reproduce.

We often think of maternal care as a natural, instinctive behavior. Yet
this is not the case. Zoos, for example, almost always have nurseries
where infants are cared for by zookeepers if their mothers will not care
for them. These exhibits are among the most popular because the babies
are so cute and so much fun to watch. And the caretaking positions in
zoo nurseries are often among the most coveted by zoo personnel for the
same reasons. But if maternal behavior is instinctive, why do zoo
nurseries even exist? The answer is that in many species, including
primates, maternal behavior is not purely instinctual; it is dependent
on social learning behavior learned by observing and imitating others),
as well. Captive female primates, including gorillas and chimpanzees,
who have not had the opportunity to observe their mother or other
females care for infants do not know how to care for their own
offspring. Although it is preferred that the mother care for her infant,
in cases when she will not, humans must step in to ensure the offspring
survives. When hand-rearing by humans is necessary, the infant is
returned to the group as soon as possible in the hopes that it will
learn species-typical behavior from its mother and other conspecifics.
Observations such as these indicate that maternal behavior is learned,
not innate, and that maternal care is critically important to the social
and psychological development of young primates.

Although females invest more in offspring than males, there are some
conditions under which males will invest. Male investment takes many
forms, ranging from carrying or grooming infants to sharing food with
them, to protecting them from infanticide killing of infants of one’s
own species) or predators, to simply tolerating their presence. A male
who has some degree of paternity certainty, or confidence that he is the
father, is more likely to invest in an offspring than a male who does
not because any investment in the offspring may increase his own
reproductive success. Males appear to use a very simple rule, “Have I
recently mated with this infant’s mother?”, to determine their paternity
certainty. For example, male mantled howler monkeys only care for
infants they may have fathered while Hanuman langur males protect and
never attack infants who might be their own Borries et al. 1999; Clarke
et al. 1998). During my fieldwork in Kenya, I observed the first
suspected case of infanticide in patas monkeys Enstam et al. 2002),
committed by the only resident male over a 10-year study period who took
over the group too late in the breeding season to have fathered any of
the offspring. It is certainly not a perfect rule, and males may
sometimes invest in an offspring they did not father. However, this is
less costly than killing your own infant.


    Sexual Selection

Sexual selection, or selection for traits that maximize mating success,
comes in two forms. Intrasexual selection is selection for traits that
enhance the ability of members of one sex to compete amongst themselves
“intrasexual” = within one sex). Intersexual selection is selection for
traits that enhance the ability of one sex to attract the other
“intersexual” = between the sexes). Intrasexual selection most often
operates on males. In the wild, adult females are either pregnant or
lactating for most of their adult lives. So the ratio of sexually
available males to sexually receptive females the operational sex ratio)
usually includes more males than females. The result? Receptive females
are a scarce resource over which males compete. Intrasexual selection
favors traits that make a male a better competitor i.e., a winner).
Competition between males hereafter referred to as male-male
competition) can take many forms but comes in two main categories:
direct competition and indirect competition just like competition
between females for food). Intersexual selection also tends to operate
on males, selecting traits that make a male more attractive to females.
Females, in turn, choose among potential fathers. Because female
primates invest more in offspring production and care than males see the
“Parental Investment” section), they pay a significantly higher cost if
the offspring dies before maturity or reaches maturity but does not
reproduce. Thus, it benefits a female primate to be choosy, and this
requires males to display traits that tell a female why she should
choose him, and not another male, as her mate.


      Intrasexual Selection: Competition for Mates

Figure 6.19a

If females live together in groups, a male or males) may be able to
monopolize access to them. Under such circumstances, intrasexual
selection favors traits like large body size Figure 6.19a) and large
canines, which increase a male’s competitive ability in fights with
other males. Because females don’t possess these same traits, males and
females of some species look different, which is called sexual
dimorphism Figure 6.19a). We will discuss sexual dimorphism in greater
detail in the next section. In some species, a single, highly
competitive male is able to defend a group of females from other males.
Males may use vocalizations, displays, or physical combat to defend
their group of females from extra-group males. In other species, it is
impossible for a single male to monopolize a group of females. In these
species, groups contain multiple females and multiple males. In combat
between two males, the stronger, larger male is more likely to win, all
else being equal. However,

Figure 6.19b

when groups contain multiple males, males have the opportunity to form
coalitions, or temporary alliances to cooperate in an effort to enhance
their competitive ability.

If one male cannot keep another from mating with a female, indirect
competition occurs. Indirect competition can take many forms, but in all
cases, the males do not interact; they may, in fact, never even see each
other. Sperm competition occurs when multiple males mate with the same
female in

Figure 6.20b

relatively close succession. males. secondary sexual characteristics
associated with adult Under such circumstances,

the male that produces the greatest quantity of long-lived sperm should
have a better chance of fertilizing the female’s egg. Evidence for sperm
competition comes from correlations between mating system and testes
weight, which is used as a proxy for sperm production Harcourt et al.
1981). Take chimpanzees and gorillas as an example. Chimpanzees live in
groups with multiple adult males and females while gorilla troops
contain one adult male the silverback) and multiple females for more
information on social and mating systems, see the next section). Because
male chimpanzees cannot keep others from mating with females, producing
greater quantities of sperm is perhaps their best way to ensure
paternity. Male gorillas who are able to monopolize a group of females
through direct competition with other males) do not need to compete with
sperm, and so they do not need to produce it in large amounts.
Therefore, although male gorillas are much larger in body size, male
chimpanzees have larger testicles to produce more sperm. In other
species, males engage in alternative mating strategies. Orangutans are
socially solitary, but a single large adult male’s territory overlaps
the territories of multiple females. The male actively keeps other males
out and away from the females. A non-territorial male may compete
directly with a territorial male, but this is dangerous and can result
in serious injury. Some males avoid this by delaying the development of
secondary sexual characteristics, or traits associated with sexual
maturity. In orangutans, these traits include large cheek phalanges, a
throat sac, and large body size Figure 6.20a). Males that do not develop
these traits look like juveniles Figure 6.20b) and seem to use their
non-threatening appearance to sneak into the territories of fully
developed males to mate with females. The mechanism that results in the
two male morphologies is not well understood, but males lacking
secondary sexual characteristics have lower testosterone levels Marty et
al. 2015). Lastly, males may compete indirectly by committing
infanticide. Infanticide occurs in many primate species, including red
howler monkeys, chacma baboons, crab-eating macaques, diademed sifakas,
ring-tailed lemurs, Hanuman langurs, and mountain gorillas. If a male
kills a competitor’s infant, the mother will resume ovulation more
quickly, providing the infanticidal male with an opportunity to father
her next infant. Thus, under the right circumstances, an infanticidal
male benefits by removing his competitor’s genes from the gene pool
while adding his own to it.

Figure 6.20a

Although more rare than male-male competition, females sometimes compete
for mates. The callitrichids, the primate family that includes marmosets
and tamarins, are unusual in their reproductive pattern.

give birth to twins Figure 6.21a–b), sometimes producing litters twice a
year. A nother interesting characteristic of callitrichid reproductive
behavior is the fact that often only one female reproduces, a phenomenon
that is achieved through reproductive suppression Digby et al. 2011).
The mechanisms differ across species but generally involve the
prevention of reproduction by subordinate females through physiological
and/or behavioral means. These subordinate females are often the older
daughters of the breeding female. In some species, the dominant female
emits chemicals that delay ovulation in subordinates. In others, she
physically breaks up matings between males and subordinate females.
Regardless of the exact mechanism, the goal is the same: to limit the
opportunities for subordinate females to become pregnant. But why?
Although a breeding female can give birth to triplets or quadruplets, it
is rare for more than two offspring from each litter to survive. Even
ensuring the survival of twins is more than the mother can manage by
herself. To maximize her offsprings’ survival, she needs all group
members, including other reproductive age) females, to care for her
offspring instead of focusing on their own. It is clear that this
strategy helps the breeding female’s reproductive success. But why would
her reproductive-age daughters “agree” to stay in their natal group and
help mom raise their siblings instead of dispersing to another group and
breeding themselves? If a subordinate female cannot find a group to
transfer into as the breeding female, she has two options: stay in her
natal group and raise younger siblings, or transfer to another group as
a subordinate and raise the offspring of a female to whom she is not
related. Because she shares genes with her siblings 50% if they are full
siblings, 25% if they are half siblings), some of the subordinate
female’s genes get passed down if her siblings survive and reproduce. On
the one hand, fewer of the female’s genes get passed down through
siblings called indirect fitness) than if she had produced her own
offspring called direct fitness). But, on the other hand, she passes on
more genes by raising her siblings than if she helped to raise the
offspring of a female to whom she was not related. Not surprisingly,
subordinate females rarely leave their natal group unless a breeding
position opens in another group.

Figure 6.21a


      Intersexual Selection: Mate Choice

Breeding females often

twins. Figure 6.21b A common marmoset family with

As we discussed at the beginning of this section, female primates are
choosy because it is more costly for them in terms of reproductive
success) if they produce an offspring that either does not survive or
that survives but cannot or does not reproduce. But what is it that they
are choosing in males? Like all other examples of primate behavior and
ecology, there is both species-level and individual-level variation in
female choice. In many animals, including humans, females choose a male
who can provide important resources, such as food, paternal care, or
protection. Examples of such direct benefits are rare in primates, since
most females do not require males to supply them these resources. Female
mountain gorillas and chacma baboons, however, may choose males based on
who can protect them from infanticidal males Henzi and Barrett 2003; van
Schaik and Kappeler 1997). More commonly, female primates obtain
indirect i.e., genetic) benefits from choosing one male over another.
Often the specific criteria by which females select mates is unknown.
However, if a female chooses a healthy as indicated by traits like a
plush coat, bright coloration, or large body size) or older male, she
may obtain genes for her offspring that code for health or longevity. If
a male’s rank is determined by competitive

ability that has a genetic component, females who choose such males may
acquire these genes and qualities) for their offspring. Females in some
species appear to prefer new immigrants, sometimes even “sneaking”
copulations with males who are not established members of their groups.
Such a preference may provide their offspring with novel genes and
increase genetic variation for more about the importance of genetic
variation, see Chapter 4). Lastly, female choice does not necessarily
imply that females are choosing only one male with whom to mate. In many
species, females actively choose to mate with multiple males. The most
likely explanation for this phenomenon is an attempt to avoid
infanticide by ensuring that multiple males think they are possibly the
father. This is called paternity confusion. In such cases, females may
not be choosing mates based on direct resource-based) or indirect
genetic) benefits but, rather, ensuring that any male who might be in
close proximity to her infant after birth will not kill it.

Female choice is often more subtle than male-male competition, so it can
be more difficult to study. However, as more research is conducted, we
better understand the ways that female primates exert their choice. In
many species, females actively solicit sexual interactions with some
males and not others. In other cases, females reject advances by some
males and not others. Grey-cheeked mangabeys in Kibale National Park,
Uganda, exert female choice in multiple ways Arlet et al. 2007; Smith
1994). They present their hindquarters which signals interest in mating)
significantly more to high-ranking and immigrant males; they refuse to
mate with some males; and most mate with multiple males when they are
receptive. These results indicate that rather than being passive actors
who accept matings with eager males, female primates actively
participate in choosing amongst suitors.


    Social and Mating Systems

Sometimes the terms social system and mating system are used
interchangeably, but there are important differences between the two
terms. A social system describes the typical number of males and females
of all age classes that live together. A mating system describes which
male s) and female s) mate. Two species can have the same social system
but a different mating system and vice versa. For example, the mating
system of both orangutans and mountain gorillas is polygyny—that is, one
male mating with multiple females—but the social systems of these two
great apes is very different. The home range of one large adult male
orangutan overlaps the home ranges of many females, with whom he mates,
but they do not travel together as a cohesive group Figure 6.22a).
Mountain gorillas travel in cohesive one-male, multi-female groups
consisting of a silverback male, multiple females, and their dependent
young, and the silverback male mates with the females of his group
Figure 6.22b). So how is it that two species can have the same mating
system and different social systems or, alternately, the same social
system and different mating systems? It all depends on how food,
females, and males are distributed.

We can understand primate social and mating systems by thinking of
layers of a map. The first layer is food distribution. Because female
reproductive success is limited by access to food, females “map onto
food” and form the second layer of the map. If food exists in large
clumps that can feed multiple individuals like fruit), females can also
exist in “clumps” i.e., groups) and will benefit from doing so because
living in groups helps with defense of food sources. Finally, because
male reproductive success is limited by access to females, males “map
onto females” forming the third layer of the map. If females live in
cohesive groups, one or a few males have the opportunity to monopolize
them. If females are widely distributed, it is more difficult sometimes
impossible) for males to monopolize multiple females.

Key: = adult male; species) or group’s home range; open red circle
represents individual female home ranges solitary species).
Illustrations by Karin Enstam Jaffe.

= adult female; open black circle represents the outline of the male’s
home range solitary

Figure 6.22a

Figure 6.22b

Figure 6.22c

Figure 6.22d


      When Females Are Solitary

Figure 6.22e

When food is distributed in such a way that females are unable to live
in close proximity to each other, they must spread out to avoid too much
competition. A male may choose to guard one female, try to monopolize
multiple females by himself, cooperate with other males to monopolize
multiple females, or cooperate with other males to help raise the
offspring of an individual female. The difference in these male
strategies is illustrated by the gibbon, orangutan, chimpanzee, and tamarin.

Both gibbon and orangutan females eat fruit found in relatively small
patches that does not support groups, so females of both species are
solitary. However, the way in which males map onto the distribution of
females is quite different. A male gibbon guards a single female,
resulting in a monogamous mating system Figure 6.22c). A pair of gibbons
form a long-term bond that includes defending a territory and relatively
high paternity certainty that results in male care of offspring. Mated
pairs defend their territory by calling together in a patterned
vocalization called a duet. These coordinated vocalizations tell other
gibbons that the territory is occupied and to stay away. Because most males

get a mate, male-male competition is relaxed, and there is little
pressure for males to develop large body size or weaponry to use in
competition with other males. Thus, it is not surprising that male and
female gibbons exhibit sexual monomorphism, meaning that males and
females are similar in body size and often look alike. Because males and
females both exclude same-sex competitors, the social group consists of
an adult male, an adult female, and their dependent offspring, sometimes
referred to as a family group.

Like gibbons, orangutan females are also solitary. But unlike gibbon
males, who cannot monopolize access to multiple females, a male
orangutan has a very large home range that overlaps the home ranges of
two or more females Figure 6.22a). The females do not regularly travel
with each other or the male, but he mates with them, resulting in a
polygynous mating system but a solitary social system. Because some
males monopolize multiple females, many male orangutans do not have
access to females. Male-male competition is intense, and males benefit
from large body size, weaponry, and other traits that increase their
competitiveness. The result is significant sexual dimorphism. Male
orangutans are twice the size of females and have large canines, cheek
phalanges, and throat sacs Figure 6.20a) that help them defend their
home range and females) through direct fighting) and indirect
territorial vocalizations) competition with other males. As we discussed
in the previous section, the competition is so intense that some males
remain in a state of arrested development Figure 6.20b).

Chimpanzees have a fluid social system referred to as fission-fusion.
When food is plentiful, female chimpanzees of the same community travel
together within their community territory. When food is scarce, the
group “fissions” and females travel independently, with their dependent
offspring, in their own range but still within the community territory.
Because male chimpanzees are philopatric and related to one another,
they share more genes in common than males in other primate species who
are unrelated. The high degree of relatedness results in high levels of
cooperation see the discussion of chimpanzee cooperative hunting in the
“Why Do Primates Live in Groups?” section) and reduced sexual
competition between males. Even males who do not father their own
offspring have some genes passed on by male relatives who do this is
another example of indirect fitness). Male chimpanzees do compete to be
at the top of the dominance hierarchy so as to obtain priority of access
to females. However, no male in the community is excluded from mating
with community females, so chimpanzees practice polygamy as a mating
system in which multiple males mate with multiple females), even though
females are solitary for some of the year. Competition between males is
relaxed because they are related and all get to mate. This results in
reduced sexual dimorphism. Unlike orangutan males, male chimpanzees are
only about 25% heavier than females. But like orangutans, male
chimpanzees compete indirectly, particularly through sperm competition.

Although there are many examples of multiple males living in groups with
multiple females we’ll discuss some examples below), it is rare for
multiple males to live with a single breeding female, a mating system
referred to as polyandry Figure 6.22d). Yet this is the pattern we often
see in the callitrichids: tamarins and marmosets. As we discussed in the
“Parental Investment” section, due to their rapid reproductive rate and
propensity for twinning Figure 6.21a–b), breeding females need help from
all group members to raise their offspring, and they suppress
reproduction in other females in their group, effectively making
breeding females solitary. In some callitrichid species, the dominant
male fathers most or all of the offspring, but the males in the group
are relatives so they benefit genetically, similar to chimpanzee males
Baker et al. 1993). In other species, males are not related, but the
breeding female mates with all the males in the group, so every male has
a chance of being the father of the offspring Díaz-Muñoz 2011). In both
cases, males help rear offspring because they cannot afford not to do
so. Although social systems differ across tamarin and marmoset species,
and even across populations of the same species, polyandry is common
among callitrichids but extremely rare in other primates.


  SPECIAL TOPIC: WOMEN IN PRIMATOLOGY: MEET “THE TRIMATES”

While many STEM Science, Technology, Engineering, and Math) fields have
traditionally been, and continue to be, dominated by men, primatology
has a long history of significant research conducted by women. This is
due, in part, to the fact that three of the most well-known
primatologists are women, making it clear that this is a field in which
women can excel. In the early 1960s, British paleoanthropologist Louis
Leakey see Chapters 9 and 10 for more about Louis Leakey’s work) was
looking for students to study the great apes in hopes of shedding light
on the behavior of our early ancestors. He chose Jane Goodall Figure
6.23a) to study chimpanzees, Dian Fossey Figure 6.23b) to study mountain
gorillas, and Birute Galdikas Figure 6.23c) to study orangutans. These
three women, sometimes referred to as Leakey’s “Trimates,” have
transformed our understanding of ape and primate) behavior through their
work.

Figure 6.23a

research on the Gombe chimpanzees spans over half a century.

Arriving at the Gombe Stream Reserve in Tanzania in 1960, Jane Goodall
Figure 6.23a) was the first scientist to conduct a long-term study of
wild nonhuman primates. Until then, most field studies lasted less than
a year. By 1961, she had made two astounding observations that forced us
to reconsider what differentiates humans from the rest of the primate
order: She observed chimpanzees eating a colobus monkey, the first
reported evidence of meat eating in our closest relatives she later
observed them hunting and killing other mammals and sharing the meat)
and also discovered that chimpanzees make and use tools by stripping
leaves off twigs to “fish” for termites. After several decades of study,
her work has produced long-term data on chimpanzee mating strategies,
mother-infant bonds, and aggression within and between communities. When
her study group, the Kasakela community, fissioned in the mid-1970s, she
observed males of the larger community attack and kill those of the
smaller one. This behavior, which Goodall compared to human warfare, is
now known to be typical of wild chimpanzees and is another behavior we
share with our closest relatives. In the mid-1980s, Goodall transitioned
from field researcher to conservationist and activist, advocating for
the humane

use of nonhuman animals Stanford 2017).

In 1967, Dian Fossey Figure 6.23b) began her long-term study of mountain
gorillas and founded the Karisoke Research Center in Rwanda. Through
patience and hard work, Fossey habituated several groups of gorillas to
the presence of human observers, and their research over several decades
has formed the foundation of our understanding of gorilla social
behavior, ecology, and life history. Gaining the gorillas’ trust was
difficult as they were fearful of humans they had known only as
poachers. Censuses of the Virunga gorilla population in the 1970s by
Fossey and her colleagues estimated a population of fewer than 300. This
represented a decline of 40% from the previous decade. The primary
causes of this decline were habitat loss and illegal hunting. Fossey’s
advocacy for 1985. mountain gorilla conservation kicked into high gear
when, at the end of 1977, poachers killed her favorite gorilla, Digit,
as he protected his group. A year later, poachers attacked one of her
main study groups and killed several gorillas as they tried to kidnap an
infant to sell to a zoo. Her efforts to publicize the killings led to
the development of conservation programs that ultimately saved the
mountain gorilla. By the end of the 1980s, the population had begun to
recover and continues to increase. Tragically, Dian Fossey was murdered
in her research cabin at Karisoke in December 1985; the case remains
unsolved Stewart 2017).

Figure 6.23c

work on behalf of orangutans spans 40 years.

Figure 6.23b

Birute Galdikas Figure 6.23c) began her study of orangutans in
Kalimantan, Borneo, in 1971 and set up a field station called Camp
Leakey. Hers was the first long-term study conducted on the Bornean
orangutan. Her research still continues, and over 150,000 hours of
observational data have been collected by Galdikas and her colleagues,
focusing on the life histories of individual orangutans. While
conducting her behavioral research, Galdikas discovered that the pet
trade and habitat loss were adversely affecting the orangutan
population. She began working with the Indonesian government to
confiscate orangutans that had been removed from the wild illegally,
many of whom ended up as pets. Taking these orphaned orangutans back to
Camp Leakey, Galdikas’s conservation efforts began to extend beyond
advocacy and into rehabilitation and forest preservation Bell 2017). If
you would like to learn more about primate conservation, please see
Appendix B.


    When Females Live in Groups

When females live together, either because their food is abundant in the
case of folivores) or because their food is distributed in large patches
that are worth defending in the case of frugivores), males have the
opportunity to monopolize multiple females. Sometimes a single male is
able to monopolize a group of females. Other times, a male may not be
able to exclude other males from the group.

Generally speaking, when female groups are small and cohesive, it tends
to be easier for a single male to monopolize a group of females.
Mountain gorillas, hanuman langurs, red howler monkeys, and patas
monkeys are examples of single-male, multi-female groups, which consist
of one adult resident male, multiple adult females, and their dependent
offspring. The mating system for single-male, multi-female groups is
polygyny Figure 6.22b). Because a relatively small number of males
monopolize all the breeding females, there are many adult males who do
not have mates. A s with orangutans, this results in strong competition
between males, resulting in sexual dimorphism where males are much
larger than females. In mountain gorillas, fights between silverbacks
can be intense. Males can use their large canines to cause serious
wounds that may even result in death Fossey 1983).

When a single male cannot monopolize a group of females, often because
the group consists of many females that may be spread out over a wide
area, the result is a multi-male, multi-female group consisting of
multiple adult males, multiple adult females, and their dependent
offspring Figure 6.22e). Olive baboons, ring-tailed lemurs, and squirrel
monkeys are examples of primate species with this type of social system.
Because a single male cannot exclude others in the group from mating,
the mating system in multi-male, multi-female groups is polygamy, but
that does not mean that all males have equal reproductive success. When
multiple males live in a group, they often form a dominance hierarchy
that determines their priority of access to females in the group. This
is similar to the way a female dominance hierarchy determines a female’s
priority of access to food. Because their place in the hierarchy can
affect their reproductive success, males in multi-male groups engage in
male-male competition, but because it is rare for males to be excluded
from mating altogether, the level of competition, and degree of sexual
dimorphism, is less extreme than what we see in polygynous species.


  COMMUNICATION

In its most basic form, communication occurs when one individual the
sender) emits a signal that conveys information, which is detected by
another individual. We have discussed several aspects of primate
sociality in this chapter, all of which require the communication of
information between individuals. But, how does a female chimpanzee
communicate her sexual availability? How does a vervet monkey
communicate the approach of a leopard or that a python is nearby? How
does a dominant or subordinate) macaque signal its place in the
dominance hierarchy? How do solitary, nocturnal primates, like the slow
loris, communicate information about themselves to conspecifics?


    Forms of Communication

Primate communication comes in four forms: vocal, visual, olfactory, and
tactile. Species vary in their reliance on each. Because it is difficult
to see others in the dark, and because nocturnal primates avoid
predators by remaining quiet, species like the slow loris and the aye-
aye rely heavily on scent-marking to communicate with conspecifics.
Diurnal species tend to rely more heavily on visual and vocal forms of
communication.


      Vocal Communication

Primates use sound to claim and maintain a territory, make contact with
other group members, or to communicate danger or threats, among other
things. Loud calls are designed to travel great distances and are used
in territorial defense by many primate species including indris,
orangutans, gibbons, howler monkeys, and siamangs. In dense forest,
where visual communication can be difficult, loud calls can be useful in
signaling to conspecifics that a group or individual occupies a specific
area. Howler monkeys are named for their loud calls, or “roars,” which
can be heard one kilometer or more away Schön Ybarra 1986). Howler group
roars may act to maintain distance between neighboring groups or keep
extra-group males from entering the home range Schön Ybarra 1986;
Sekulic 1982).

Other vocalizations are intended to communicate with individuals in
one’s own group. These include vocalizations given as part of threat
displays or dominance interactions, as well as contact calls that
provide information about location to other group members. Baboons have
a rich repertoire of vocalizations for communicating with other group
members Fischer et al. 2008; Ransom 1981). Adult males give specific
vocalizations during threat displays and physical confrontations.
Subordinates “screech” when retreating from a dominant individual,
signaling submission. Since baboons rely on membership in their group
for finding food and detecting predators, a baboon separated from his
group will vocalize in an attempt to regain contact. Young baboons emit
their own contact calls when separated from their mothers.

Alarm-calling behavior is widespread in primates. Often, alarm calls
serve to notify conspecifics of potential danger, as is the case with
vervet monkeys Figures 6.4a, 6.11b). Research by Dorothy Cheney, Robert
Seyfarth, and others has shown that: 1) vervets classify predators based
on hunting style; 2) alarm calls convey information to other vervets
about that hunting style; and 3) other vervets respond in ways
appropriate for evading that type of predator Seyfarth et al. 1980a).
When a vervet gives a “leopard” alarm call [directed at mammalian
carnivores like leopards Figure 6.15a) and dogs], monkeys on the ground
climb the nearest tree, while monkeys already in trees stay there or
climb higher. Since most mammalian carnivores hunt on the ground,
getting into, and staying in, a tall tree is the best option for escape.
When the distinct “snake” alarm call is given, vervets stand on their
hind legs and look down at the ground. Since snakes, like pythons Figure
6.15g) are not pursuit predators, locating them so as to avoid them is
the best strategy. Lastly, when an “eagle” alarm call is given, vervets
look up or run into bushes, both of which are useful responses for
avoiding hawks and eagles Figure 6.15e), which attack from above.
Vervets clearly understand the meaning of each type of alarm call, as
they respond appropriately even when they do not see the actual predator
Seyfarth et al.1980b). Such semantic communication, which involves the
systematic use of signals to refer to objects in the environment, was
once believed to be unique to humans. It may be a precursor to the
symbolic capacities of human language.

Research on other African monkeys indicates that some species use alarm
calls to signal to the predator that it has been detected. Diana
monkeys, Campbell’s guenons, and sooty mangabeys of the Taï forest give
alarm calls to leopards but not chimpanzees Zuberbühler et al. 1997).
Because leopards Figure 6.15a) are stealth predators, they rely on the
element of surprise to sneak up on their prey. Alarm calling at leopards
appears to tell the leopard that it has been seen and therefore its
chance of success will be low. Leopards are more likely to stop hunting
after an alarm call has been emitted. Unlike leopards, chimpanzees are
pursuit predators and may even use alarm calls to locate potential prey.
With such a predator, prey are better off remaining as silent as
possible so as not to alert the predator to their location Boesch and
Boesch 1989; Zuberbühler et al. 1999).


      Visual Communication

Visual signals are an important component of nonhuman primate behavior,
alone or in combination with other forms


      Visual Communication

Visual signals are an important component of nonhuman primate behavior,
alone or in combination with other forms of communication. Some visual
signals are common to all nonhuman primates. For example, piloerection,
or raising one’s hair or fur, is used in aggressive interactions to make
an individual appear larger than it actually is. The females of many Old
World primate species, including macaques, baboons, and chimpanzees,
signal sexual receptivity through changes in the size, shape, and,
often, color of their hindquarters, called a sexual swelling Figure
6.24a). The sexual swelling reaches its maximum size at ovulation. When
females are not receptive, either because they are pregnant or are
nursing, they do not display a sexual swelling Figure 6.24b). Thus, its
presence or absence signals a female’s reproductive state. In some
species, females use other visual cues to indicate sexual receptivity.
Common marmoset females solicit mating through tongue-flicking displays
directed at males, while female patas monkeys engage in a more elaborate
visual display. When soliciting mating, the female crouches in front of
the male and looks back at him while blowing air into her cheeks; she
also may drool and curl her tail Chism et al. 1984).

Figure 6.24a

Figure 6.24b

Monkeys and apes also use a diversity of facial expressions in visual
communication. Showing your teeth in a “smile” sends a signal of
friendship in humans. Displaying teeth in this way is a sign of anxiety
or fear in Old World monkeys. That male mandrill you see “yawning” at
your local zoo is actually displaying his teeth to signal tension or
threaten a rival Figure 6.25). Male gelada baboons use “lip flips,” in
which the gums and teeth are exposed by flipping the upper lip up over
the nostrils Figure 6.26), and “raised eyelids,” in which the pale
eyelids are exposed by pulling the scalp back as threatening gestures
Aich et al. 1990). Submissive males respond by fleeing or presenting
their hindquarters. In the Smithsonian Channel video 1 , male gelada
baboons use the lip flip in competition with other males.

Figure 6.25

Figure 6.26

Primates also communicate through color. In some species, facial
coloration provides information about individual health or status to
conspecifics. Mandrills are a good example of this. Female mandrill
faces are brighter during ovulation, which may function to communicate
reproductive state to males Setchell et al. 2006). Redness of male
mandrill faces is correlated with androgen levels. Thus, facial
coloration can, on the one hand, communicate information about
competitiveness to other males and information about reproductive
fitness to females Figure 6.27; Setchell et al. 2008). On the other
hand, the variation in facial coloration among New World monkeys,
ranging from very simple Figure 6.28a) to highly complex color patterns
Figure 6.28b), appears to be linked to species recognition, or the
ability to distinguish conspecifics from other species. Species with
more complex facial color patterns tend to be those that are sympatric
with a larger number of other primate species. In such circumstances,
distinct facial coloration and patterning may help individuals recognize
conspecifics and reduce the chances of mating with another species
Santana et al. 2012).

Figure 6.27

Figure 6.28a and 6.28b A ukari displaying bold but simple facial
coloration (left). Figure 6.28b A white-bellied spider monkey displaying
a complex facial color pattern (right).

1. Smithsonian Channel. June 9, 2017. “Why These Vegetarian Monkeys Have
Sharp Predator Teeth.” Accessed July 25, 2019. https:// <https://>
www.youtube.com/watch?time_continue=145&v=aC6iYj_EBjY


      Olfactory Communication

All primates use scent to communicate. Females secrete chemicals from
their anogenital region the area of the anus and genitals) that provide
males with information about their reproductive state. In some species,
like macaques and chimpanzees, this olfactory signal is enhanced by a
sexual swelling a visual signal; see Figure 6.24a and discussion above).
Olfactory communication is particularly important for New World monkeys,
lemurs, and lorises. Male and female squirrel monkeys engage in “urine
washing,” in which an individual urinates on its hands and feet and then
uses them to spread urine all over its body. The function of urine
washing may include marking trails for other group members to follow,
self-cleaning or controlling body temperature, dominance displays,
enhanced grasping ability while climbing, or communicating reproductive
state Boinski 1992). During aggressive interactions with other males,
male ring-tailed lemurs rub their tails with scent from glands on their
wrists and chests. They then waive their tails toward their opponent,
who responds with his own “stinky tail” display, physical aggression, or
by fleeing Jolly 1966). Both sexes use their anogenital scent glands to
mark substrates like saplings, fallen trees, or tree trunks) in their
group’s territory Jolly 1966). Males also leave visual and scent marks
during “spur marking,” in which they impregnate a substrate with scent
from their wrist gland after using a thorny “spur” near the gland to cut
into it Figure 6.29). Because substrate marking behavior occurs where
the ranges of two groups overlap, and increases during the mating
season, the primary function is believed to reinforce territorial
boundaries Mertl-Millhollen 1988).


      Tactile Communication

Figure 6.29

Tactile communication, or touch, is very important in all primate
species. Physical contact is used to comfort and reassure, is part of
courtship and mating, and is used to establish dominance and alliances.
Grooming is an important and clearly enjoyable form of tactile
communication for all primates Figure 6.30a–d). Not only does grooming
serve to clean the skin and fur, removing parasites and debris, but it
is an important affiliative non-aggressive) behavior that helps
reinforce social bonds, repair relationships, and cement alliances.
Among chimpanzees, subordinates groom dominants in an effort to receive
benefits such as protection, acceptance, and reciprocal grooming. When
yellow baboon females engage in more grooming activity as both givers
and receivers), their offspring have an increased chance of surviving to
one year Silk et al. 2003). Although the mechanism behind this
relationship is unknown, close associations with group members may
provide females and their young offspring with protection from
harassment or access to valuable resources that enhance infant survival.
Social integration, as exemplified by grooming, is of significant
adaptive value to primates.

Figure 6.30a

Figure 6.30c


  THE QUESTION OF CULTURE

Figure 6.30b

Figure 6.30d

It may be surprising in a chapter on nonhuman primates to see a
discussion of culture. After all, culture is considered by many,
including cultural anthropologists, to be a distinguishing
characteristic of humans. Indeed, some anthropologists question claims
of culture in primates and other animals. Definitions of animal culture
focus on specific behaviors that are unique to one population.
Anthropological definitions of human culture emphasize shared ideology
e.g., values, morals, beliefs) and symbols, not just behavior. Using
this definition, some cultural anthropologists view primates as lacking
culture because of the absence of symbolic life e.g., religion).
However, the longer we study primate groups and populations, the more
insight we gain into primate behavioral variation. If we define culture
as the transmission of behavior from one generation to the next through
social learning, then we must view at least some of the behavioral
variation we see in primates as forms of cultural tradition, or a
distinctive pattern of behavior shared by multiple individuals in a
social group that persists over time Whitten 2001).


    Examples of Culture in Primates


      Chimpanzee Culture

Due to both their high level of intelligence and the large number of
long-term studies on several different populations, chimpanzees provide
the best example of cultural tradition in primates. Research on a
variety of animals, including fish, rodents, birds, and monkeys indicate
the transmission of a single behavior pattern through social learning,
resulting in cultural variation. But chimpanzees, along with orangutans,
are the only species other than humans to express cultural

variation in multiple behavioral patterns. Examining behavioral
variation across chimpanzee study sites, researchers have identified
over 40 cultural traditions, or distinct behavioral patterns, in
chimpanzees Whiten 2011). These cultural traditions span the gamut from
population-specific prey preferences to tool-use techniques, hunting
strategies, and social behaviors.

It is not just the sheer number of cultural traditions that make
chimpanzee culture so fascinating. It is that each chimpanzee community
displays a unique cultural profile defined by a subset of the known
traditions. For example, in Tanzania, chimpanzees fish for termites by
poking twigs which they’ve stripped) into termite mounds. But in Gambia,
they use modified twigs to extract honey from holes in trees. In
Fongoli, Sénégal, chimpanzees use sticks as “spears” that they stab into
tree cavities to hunt for galagos Figure 6.31). Multiple chimpanzee
populations use use a “hammer and anvil” to crack open nuts, but the
techniques differ. In some populations, chimps place a nut on a large
flat rock and use a stone “hammer” to crack it open; in others, they use
pieces of wood. Chimpanzees in Guinea use three stones for nut cracking:
one as the anvil, the second one as the hammer, and a third as a wedge
to secure the anvil McGrew 1998). The National Geographic video “Chimps
and Tools” n.d.)2 provides a glimpse into some of the known variation in
chimpanzee tool use. Because the cultural traditions are so diverse and
unique, if a researcher can observe enough of a chimpanzee’s behavior,
that individual can be assigned to a specific community, much in the
same way a human being can be associated with a specific culture based
on his or her behavior Whiten 2011).

Figure 6.31

So how do chimpanzee cultures develop, and how does cultural
transmission occur? Although we do not know for sure how chimpanzee
cultural traditions develop initially, it is possible that different
groups invent, either accidentally or deliberately, certain behaviors
that other individuals copy. There is little evidence currently to
support the idea that chimpanzees actively teach one another a new
behavior, so it appears that they learn through observation and
practice. This lack of teaching is one reason that some primatologists
call the traditions in chimpanzees and other primates) “pre culture.”
However, immigration between communities does appear to be an important
avenue of cultural transmission in

2. National Geographic. n.d. “Chimps and Tools.” Accessed July 25, 2019.
https://video.nationalgeographic.com/video/00000144-0a1e-d3cb-
a96c-7b1fadbd0000 <https://video.nationalgeographic.com/video/
00000144-0a1e-d3cb-a96c-7b1fadbd0000>

chimpanzees, much as it is between human cultures. Immigrants typically
females) may bring cultural traditions to their new community, which
residents observe and learn. Conversely, immigrants may observe and
learn a cultural tradition practiced in their new community Whiten 2011).


      Cultural Transmission in Macaques

Figure 6.32

Two monkey species are well known for behavioral variation that has been
called “pre-cultural” by some primatologists: Japanese macaques and
capuchins. The transmission of unique foraging behaviors through a
provisioned group of Japanese macaques on Koshima Island is well known
McGrew 1998). In an effort to keep the monkeys nearby, researchers
provided them with piles of sweet potatoes. A juvenile female named Imo
spontaneously washed a muddy sweet potato in a stream. This new food
processing technique first spread among other juveniles and then
gradually to older individuals. Within 30 years, it had spread across
generations, and 46 of 57 monkeys in the group engaged in the behavior.
Another example comes from a group living far to the north, in the snowy
forests of Honshu. Researchers threw apples into hot springs to record
the monkeys’ behavior. Not only did the monkeys enter the springs to
retrieve the apples, but over multiple years, they learned to immerse
themselves in the hot springs to keep warm when not foraging McGrew
1998; Figure 6.32; watch Japanese macaques using hot springs in the
National Geographic video “Meditative Snow Monkeys Hang Out in Hot
Springs” n.d.)3. Some primatologists discount the significance of these
pre)cultural traditions since they began as a result of humans providing
food to the monkeys and are therefore not “natural” behaviors. However,
the behaviors have changed over time, even though the underlying
provisioning either did not change or ceased altogether McGrew 1998).
For example, although sweet potato washing started in freshwater, it
gradually shifted to seawater, apparently to add salt for flavor. Thirty
years after the behavior started, the most common form involved dipping
the potato into salt water, even if it was clean. Similarly, female
macaques entering the hot springs initially left their young infants at
the edge, but today juveniles play and even swim underwater in the hot
springs. These examples share several characteristics with human
culture, including invention or modification of behavior, transmission
of behavior between individuals, and the persistence of the behavior
across generations McGrew 1998).


  CONCLUSION

Primates are socially complex and extremely intelligent. Highly
adaptable, they display significant variation in diet, habitat, and
behavior. By studying primates in their natural habitats, we learn how
their behavior and morphology are influenced by ecology, including the
foods they eat and the other species with which they live. A s our
closest living relatives, primates provide important insights into the
evolution of human social behavior, language, and culture. These are
topics you will learn about in later chapters of this book.

 3. National Geographic. n.d. “Meditative Snow Monkeys Hang Out in Hot
    Springs.” Accessed July 25,
  2019. https://video.nationalgeographic.com/video/short-film-showcase/
        00000149-d415-de71- a9eb-dc9539210000


    Review Questions

  * If anthropology is the study of humans, why do some anthropologists
    study primates?
  * What is the nature of interactions between primates and other
    members of their broader ecological communities, including other
    species of primates?
  * What is the difference between a social system and a mating system?
    Describe the variety of social and mating systems observed in
    primates. How do primatologists use the distribution of food,
    females, and males to understand this variation, including the fact
    that two species can have the same mating system but different
    social systems? Compare and contrast male and female mating
    strategies. Why and how, do females choose a potential mate? Why and
    how do males compete for potential mates?
  * What are the costs and benefits of group living? If living in a
    group is beneficial for most primates, why do some individuals
    disperse and leave their group? How do the costs and benefits of
    dispersal differ for males and females?
  * Discuss the variation in primate communication. How is communication
    between primates similar to and different from communication between
    humans?
  * What is the evidence for cultural variation in primates? How do
    primatologists think cultural transmission occurs in primates? How
    do you think this process compares to cultural transmission in humans?


    Key Terms

Abundance: How much food is available in a given area.

Affiliative: A description of non-aggressive social interactions and
associations between individuals. Allopatric: Two or more species that
do not overlap in geographic distribution. Anogenital: Relating to the
anus and genitals. Basal metabolic rate: The rate at which an individual
uses energy when at rest. Carnivores: Organisms whose diet consists
primarily of animal tissue. Coalition: A temporary group composed of two
or more individuals who work together to achieve a common goal. It is
often used in reference to male-male competition, such as when two less-
competitive males join forces against a more-competitive male.
Competitive exclusion principle: The idea that two species that compete
for the exact same resources cannot coexist. Conspecifics: Members of
the same species.

Culture: The transmission of behavior from one generation to the next
through observation and imitation.

Cultural tradition: A distinctive pattern of behavior shared by multiple
individuals in a social group, which persists over time and is acquired
through social learning.

Crypsis: The ability to avoid detection by other organisms.

Day-range length: The distance traveled in a day.

Direct fitness: An individual’s genetic contribution to future
generations that is due to offspring production. Dispersal: To leave
one’s group or area. This may or may not involve entering another group.
Distribution: How food is spread out. Dominance hierarchy: The ranked
organization of individuals established by the outcome of aggressive-
submissive interactions. Feeding: The act of consuming food. Fission-
fusion: Societies in which group composition is flexible, such as
chimpanzee and spider monkey societies. Individuals may break up into
smaller feeding groups fission) and combine into larger groups fusion).
Fitness: An individual’s reproductive success relative to other members
of the same species. Foraging: The act of searching for food. Folivores:
Organisms whose diet consists primarily of leaves. Frugivores: Organisms
whose diet consists primarily of fruit. Home range: The area a group or
individual uses over a given period of time often over a year).
Inbreeding: Reproduction between relatives. Inbreeding depression:
Harmful genetic effects of breeding between relatives. Indirect fitness:
An individual’s genetic contribution to future generations that is due
to the reproduction of non descent relatives. Infanticide: The killing
of infants of one’s own species. Insectivores: Organisms whose diets
consist primarily of insects. Intrasexual selection: Selection for
traits that enhance the ability of members of one sex to compete amongst
themselves. Interbirth interval: The length of time between successive
births. Intersexual selection: The selection for traits that enhance the
ability of the members of one sex to attract the attention of the other.
Mating system: A way of describing which male s) and female s) mate.
Mobbing: Cooperatively attacking or harassing a predator.

Monogamous: A mating system in which one male mates with one female.

Natal group: The group into which an organism is born.

Natal dispersal: Emigrating from the group into which one is born.
Niche: The role of a species in its environment; how it meets its needs
for food, shelter, etc. Niche partitioning: The process by which
potentially competing species reduce competition by using the
environment differently. Omnivores: Organisms whose diet consists of
plant and animal matter. Operational sex ratio: The ratio of sexually
active or available) males to sexually active or available) females.
Parental investment: Any time or energy a parent devotes to the current
offspring that enhances its survival and eventual reproductive success)
at the expense of the parent’s ability to invest in the next offspring.
Paternity certainty: Confidence in which male fathered an offspring.
Paternity confusion: When males are uncertain if they fathered an
offspring. This is often a female strategy to reduce the chance of
infanticide. Philopatric: Remaining in the group of one’s birth.
Piloerection: Raising one’s hair or fur in an effort to look bigger.
Polyandry: A mating system in which multiple males mate with a single
breeding female. Polygamy: A mating system in which multiple males mate
with multiple females. Polygyny: A mating system in which one male mates
with multiple females. Polyspecific associations: Associations between
two or more different species involving behavioral changes by at least
one of the associated species. Primate community: All living organisms
that occur in an area that includes primates. Primatologist: A scientist
who studies primate behavior and/or ecology. Primatology: The scientific
field that studies primate behavior and/or ecology. Receptive: A term
used to describe females who are ready for sexual reproduction i.e., not
pregnant or nursing). Reproductive success: An individual’s genetic
contribution to future generations. Reproductive suppression: The
prevention or inhibition of reproduction of healthy adults. Secondary
sexual characteristics: Characteristics that appear at time of sexual
maturity. These are not directly involved in reproduction, but they
provide individuals an advantage in courtship and competition for mates.
Semantic communication: The systematic use of signals to refer to
objects in the environment. Sexual dimorphism: When males and females of
a species have different morphological traits. Sexual monomorphism: When
males and females of a species have similar morphological traits.

Sexual selection: The selection for traits that increase mating success.
This occurs via intersexual selection and intrasexual selection.

Sexual swelling: Area of the hindquarters that change in size, shape and
often color over the course of a female’s reproductive cycle, reaching
maximum size at ovulation. Occurs in many Old World primate species.

Social learning: The idea that new behaviors can be acquired by
observing and imitating others. Social system: A way of describing the
typical number of males and females of all age classes that live
together. Solitary: Living alone. Species recognition: Recognition of
conspecifics. Sperm competition: Competition between sperm of two or
more different males to fertilize the same egg. Sympatric: Two or more
species that overlap in geographic distribution. Territory: A home range
whose boundary is defended from intrusion by conspecifics. Vertebrates:
The group of animals characterized by an internal spinal column or
backbone. This includes fish, amphibians, reptiles, birds, and mammals.
Vigilance: Watchful behavior to detect or in response to potential
danger, usually in the form of predators or potential competitors.


    About the Author


      Karin Enstam Jaffe


      Sonoma State University, karin.jaffe@sonoma.edu

Karin Enstam Jaffe

Dr. Karin Enstam Jaffe has loved primates since she was five years old.
As an undergraduate at U.C. San Diego, she participated in projects
studying orangutans, langurs, and Mona monkeys. She earned her Ph.D. in
Anthropology from U.C. Davis studying vervet and patas monkey anti-
predator behavior. Dr. Jaffe has over 20 years of experience studying
primate behavior in Kenya and Grenada and at the San Diego Zoo, San
Francisco Zoo, and Safari West Wildlife Preserve in Sonoma County,
California. She has been a faculty member in the Anthropology Department
at Sonoma State University since August 2002. A dedicated teacher-
scholar, Dr. Jaffe has won several teaching, scholarship, and mentoring
awards, including SSU’s Excellence in Teaching Award, Educational
Experience Enhancement Award, and the President’s Excellence in
Scholarship Award. In addition to teaching, she is a Research Associate
at Oakland Zoo, where she has been involved in behavioral enrichment
research involving ring tailed lemurs, chimpanzees, and sun bears, as
well as a study of the social network of hamadryas baboons.


    For Further Exploration

Fossey, Dian. 1983. Gorillas in the Mist. London: Hodder & Stoughton.
Goodall, Jane. 1971. In the Shadow of Man. Boston: Houghton Mifflin.
Rowe, Noel, and Marc Myers, eds. 2016. All the World’s Primates.
Charleston, Rhode Island: Pogonias Press. Strier, Karen B. 2017. Primate
Behavioral Ecology. 5th ed. New York: Routledge. Primate Info Net
http://pin.primate.wisc.edu/) <http://pin.primate.wisc.edu/)> is an
information service of the National Primate Research Center at

the University of Wisconsin, Madison. It includes Primate Factsheets,
primate news and publications, a list of primate-related jobs, and an
international directory of primatology, among other information.

Primate Specialist Group http://www.primate-sg.org/) <http://
www.primate-sg.org/)> is a collection of scientists and conservationists
who work in

dozens of African, Asian, and Latin American nations to promote research
on primate conservation.


    References

Aich, H., R. Moos-Heilen, and E. Zimmermann. 1990. “Vocalizations of
Adult Gelada Baboons Theropithecus gelada):

Acoustic Structure and Behavioural Context.” Folia Primatologica 55 3–
4): 109–132.

Arlet, Małgorzata E., Freerk Molleman, and Colin Chapman. 2007.
“Indications for Female Mate Choice in Grey

Cheeked Mangabeys Lophocebus albigena johnstoni in Kibale National Park,
Uganda.” Acta Ethologica 10 2): 89–95.


      Baker, Andrew J., James M. Dietz, and Devra G. Kleiman. 1993.
      “Behavioural Evidence for Monopolization of Paternity in

Multi-Male Groups of Golden Lion Tamarins.” Animal Behaviour 46 6):
1,091–1,103.

Bell, Sarah A. 2017. “Galdikas, Birute.” In The International
Encyclopedia of Primatology, Volume A–G, edited by Agustín

Fuentes, 445–446. Malden, Massachusetts: John Wiley & Sons.

Boesch, Christophe. 2002. “Cooperative Hunting Roles Among Taï
Chimpanzees.” Human Nature 13 1): 27–46. Boesch, Christophe, and Hedwige
Boesch. 1989. “Hunting Behavior of Wild Chimpanzees in the Taï National
Park.”

American Journal of Physical Anthropology 78 4): 547–573.

Boinski, S. 1992. “Olfactory Communication among Costa Rican Squirrel
Monkeys: A Field Study.” Folia Primatologica 59

3): 127–136.


      Borries, Carola, Kristin Launhardt, Cornelia Epplen, Jörg T.
      Epplen, and Paul Winkler. 1999. “Males as Infant Protectors

in Hanuman Langurs Presbytis entellus) Living in Multimale Groups:
Defence Pattern, Paternity, and Sexual Behaviour.” Behavioral Ecology
and Sociobiology 46 5): 350–356.

Chapman, Colin A., and Carlos A. Peres. 2001. “Primate Conservation in
the New Millennium: The Role of Scientists.”

Evolutionary Anthropology: Issues, News, and Reviews 10 1): 16–33.


      Cheney, D. L., and R. M. Seyfarth. 1987. “The Influence of
      Intergroup Competition on the Survival and Reproduction of

Female Vervet Monkeys.” Behavioral Ecology and Sociobiology 21 6): 375–386.

Chism, J. B., T. E. Rowell, and D. Olson. 1984. “Life History Patterns
of Female Patas Monkeys.” In Female Primates:

Studies of Women Primatologists, edited by Meredith Small, 175–190. New
York: A.R. Liss.


      Clarke, Margaret R., Kenneth E. Glander, and Evan L. Zucker. 1998.
      “Infant-Nonmother Interactions in Free-Ranging

Howlers Alouatta palliata) in Costa Rica. International Journal of
Primatology 19 3): 451–472.

Crockett, Carolyn M., and Theresa Pope. 1988. “Inferring Patterns of
Aggression from Red Howler Monkey Injuries.”

American Journal of Primatology 15 4): 289–308.


      Díaz-Muñoz, Samuel L. 2011. “Paternity and Relatedness in a
      Polyandrous Nonhuman Primate: Testing Adaptive

Hypotheses of Male Reproductive Cooperation.” Animal Behaviour 82 3):
563–571.


      Digby, Leslie J., Stephen F. Ferrari, and Wendy Saltzman. 2007)
      2011. “Callitrichines: The Role of Competition in

Cooperatively Breeding Species.” In Primates in Perspective, edited by
Christina J. Campbell, AugustÍn Fuentes, Katherine C. MacKinnon, Simon
K. Bearder, and Rebecca M. Stumpf, 91–10. Second edition, New York:
Oxford University Press.

Eckardt, Winnie, and Klaus Zuberbühler. 2004. “Cooperation and
Competition in Two Forest Monkeys.” Behavioral

Ecology 15 3): 400–411.

Enstam, Karin L., and Lynne A. Isbell. 2002. “Comparison of Responses to
Alarm Calls by Patas Erythrocebus patas) and Vervet Cercopithecus
aethiops) Monkeys in Relation to Habitat Structure.” American Journal of
Physical Anthropology 119 1): 3–14.


      Enstam, Karin L., Lynne A. Isbell, and Thomas W. de Maar. 2002.
      “Male Demography, Female Mating Behavior, and

Infanticide in Wild Patas Monkeys Erythrocebus patas).” International
Journal of Primatology. 23 1): 85–104.

Fedigan, Linda Marie. 1990. “Vertebrate Predation in Cebus capucinus:
Meat Eating in a Neotropical Monkey.” Folia

Primatologica 54 3–4): 196–205.


      Fischer, Julia, Kurt Hammerschmidt, Dorothy L. Cheney, and Robert
      M. Seyfarth. 2008. “Acoustic Features of Female

Chacma Baboon Barks.” Ethology 107 1): 33–54.

Fossey, Dian. 1983. Gorillas in the Mist. London: Hodder & Stoughton.
Gardner, Charlie J., Patrick Radolalaina, Mahandry Rajerison, and Harry
W. Greene. 2015. “Cooperative Rescue and

Predator Fatality Involving a Group-Living Strepsirrhine, Coquerel’s
Sifaka Propithecus coquereli), and a Madagascar Ground Boa Acrantophis
madagascariensis).” Primates 56 2): 127–129.


      Gautier-Hion, Annie, René Quris, and Jean-Pierre Gautier. 1983.
      “Monospecific vs. Polyspecific Life: A Comparative

Study of Foraging and Antipredator Tactics in a Community of
Cercopithecus Monkeys.” Behavioral Ecology and Sociobiology 12 4): 325–335.


      Harcourt, A. H., P. H. Harvey, S. G. Larson, and R. V. Short.
      1981. “Testis Weight, Body Weight and Breeding System in

Primates.” Nature 293 5,827): 55–57.


      Henzi, Peter, and Louise Barrett. 2003. “Evolutionary Ecology,
      Sexual Conflict, and Behavioral Differentiation among

Baboon Populations.” Evolutionary Anthropology 12 5): 217–230.


      Isbell, Lynne A. 1991. “Contest and Scramble Competition: Patterns
      of Female Aggression and Ranging Behavior Among

Primates.” Behavioral Ecology 2 2): 143–155.


      Isbell, Lynne A., Dorothy L. Cheney, and Robert M. Seyfarth. 1990.
      “Costs and Benefits of Home Range Shifts Among

Vervet Monkeys Cercopithecus aethiops) in Amboseli National Park,
Kenya.” Behavioral Ecology and Sociobiology 27 5): 351–358.


      Isbell, Lynne A., and Dirk Van Vuren. 1996. “Differential Costs of
      Locational and Social Dispersal and Their

Consequences for Female Group-Living Primates.” Behaviour 133 1–2): 1–36.

Jolly, Alison. 1966. Lemur Behavior: A Madagascar Field Study. Chicago:
University of Chicago Press. Lutz, Clayton L., Duane R. Diefenbach, and
Christopher S. Rosenberry. 2016. “Proximate Influences on Female Dispersal

in White-Tailed Deer.” Journal of Wildlife Management 80 7): 1,218–1,226.

Marty, Pascal R., Maria A. van Noordwijk, Michael Heistermann, Erik P.
Willems, Lynda P. Dunkel, Manuela Cadilek, Muhammad Agil, and Tony
Weingrill. 2015. “Endocrinological Correlates of Male Bimaturism in Wild
Bornean Orangutans.” American Journal of Primatology 77 11): 1,170–1,178.

McGrew, W. C. 1998. “Culture in Nonhuman Primates?” Annual Review of
Anthropology 27 1): 301–328. Mertl-Millhollen, Anne S. 1988. “Olfactory
Demarcation of Territorial but Not Home Range Boundaries by Lemur catta.”

Folia Primatologica 50 3–4): 175–187.

National Geographic. n.d. “Chimps and Tools.” Accessed July 25, 2019.
https://video.nationalgeographic.com/video/ <https://
video.nationalgeographic.com/video/>

00000144-0a1e-d3cb-a96c-7b1fadbd0000

National Geographic. n.d. “Meditative Snow Monkeys Hang Out in Hot
Springs.” Accessed July 25, 2019.

https://video.nationalgeographic.com/video/short-film-showcase/00000149-
d415-de71-a9eb-dc9539210000 <https://video.nationalgeographic.com/video/
short-film-showcase/00000149-d415-de71-a9eb-dc9539210000>

Nekaris, K. Anne-Isola, Richard S. Moore, E. Johanna Rode, and Bryan G.
Fry. 2013. “Mad, Bad, and Dangerous to Know:

The Biochemistry, Ecology, and Evolution of Slow Loris Venom.” The
Journal of Venomous Animals and Toxins Including Tropical Diseases 19
1): 21.

Peres, Carlosa. 1992. “Prey-Capture Benefits in a Mixed-Species Group of
Amazonian Tamarins, Saguinus fuscicollis and

S. mystax.” Behavioral Ecology and Sociobiology 31 5): 339–347. https://
doi.org/10.1007/bf00177774. <https://doi.org/10.1007/bf00177774.>

Raboy, Becky E., Gustavo R. Canale, and James M. Dietz. 2008. “Ecology
of Callithrix kuhlii and a Review of Eastern

Brazilian Marmosets.” International Journal of Primatology 29 2): 449–467.

Ransom, Timothy W. 1981. Beach Troop of the Gombe. East Brunswick, New
Jersey: Bucknell University Press. Santana, Sharlene E., Jessica Lynch
Alfaro, and Michael E. Alfaro. 2012. “Adaptive Evolution of Facial
Colour Patterns in

Neotropical Primates.” Proceedings of the Royal Society B: Biological
Sciences 279 1,736): 2,204–2,211.

Schön Ybarra, M. A. 1986. “Loud Calls of Adult Male Red Howling Monkeys
Alouatta seniculus).” Folia Primatologica 47

4): 204–216.


      Schwitzer, Christoph, Russell A. Mittermeier, Anthony B. Rylands,
      Federica Chiozza, Elizabeth A. Williamson, Elizabeth

J. Macfie, Janette Wallis, and Alison Cotton. 2017. Primates in Peril:
The World’s 25 Most Endangered Primates 2016–2018. Arlington, VA: IUCN
SSC Primate Specialist Group PSG), International Primatological Society
IPS), Conservation International CI), and Bristol Zoological Society.

Sekulic, Ranka. 1982. “The Function of Howling in Red Howler Monkeys
Alouatta seniculus).” Behaviour 81 1): 38–54. Setchell, Joanna M., Tessa
Smith, E. Jean Wickings, and Leslie A. Knapp. 2008. “Social Correlates
of Testosterone and

Ornamentation in Male Mandrills.” Hormones and Behavior 54 3): 365–372.


      Setchell, Joanna M., E. Jean Wickings, and Leslie A. Knapp. 2006.
      “Signal Content of Red Facial Coloration in Female

Mandrills Mandrillus sphinx).” Proceedings of the Royal Society B:
Biological Sciences 273 1599): 2395–2400.


      Seyfarth, R. M., D. L. Cheney, and P. Marler. 1980a. “Monkey
      Responses to Three Different Alarm Calls: Evidence of

Predator Classification and Semantic Communication.” Science 210 4,471):
801–803.


      Seyfarth, Robert M., Dorothy L. Cheney, and Peter Marler. 1980b.
      “Vervet Monkey Alarm Calls: Semantic

Communication in a Free-Ranging Primate.” Animal Behaviour 28 4): 1,070–
1,094.

Silk, Joan B., Susan C. Alberts, and Jeanne Altmann. 2003. “Social Bonds
of Female Baboons Enhance Infant Survival.”

Science 302 5,648): 1,231–1,234.

Smith, David Glenn. 1994. “Male Dominance and Reproductive Success in a
Captive Group of Rhesus Macaques Macaca

mulatta).” Behaviour 129 3): 225–242.

Smithsonian Channel. June 9, 2017. “Why These Vegetarian Monkeys Have
Sharp Predator Teeth.” Accessed July 25,


      2019. https://www.youtube.com/watch?
      time_continue=145&v=aC6iYj_EBjY <https://www.youtube.com/watch?
      time_continue=145&v=aC6iYj_EBjY>

Stanford, Craig B. 2017. “Goodall, Jane.” In The International
Encyclopedia of Primatology, Volume A–G, edited by Agustín

Fuentes, 471–472. Malden, Massachusetts: John Wiley & Sons.


        Stewart, Kelly. 2017. “Fossey, Dian.” In The International
        Encyclopedia of Primatology, Volume A–G, edited by Agustín

Fuentes, 432–433. Malden, Massachusetts: John Wiley & Sons.


      Stumpf, R. M., M. Emery Thompson, M. N. Muller, and R. W.
      Wrangham. 2009. “The Context of Female Dispersal in

Kanyawara Chimpanzees.” Behaviour 146 4–5): 629–656.

Swedell, Larissa, and Amy Schreier. 2006. “Male Aggression toward
Females in Hamadryas Baboons: Conditioning,

Coercion, and Control.” In Sexual Coercion in Primates and Humans,
edited by Martin N. Muller and Richard W. Wrangham, 244–268. Cambridge,
Massachusetts: Harvard University Press.

Terborgh, John. 1984. Five New World Primates: A Study in Comparative
Ecology. Princeton: Princeton University Press. Trivers, Robert L. 1972.
“Parental Investment and Sexual Selection.” In Sexual Selection and the
Descent of Man, 1871–1971,

edited by Bernard Campbell, 136–179. Chicago: Aldine.

van Schaik, Carel P., and Peter M. Kappeler. 1997. “Infanticide Risk and
the Evolution of Male-Female Association in

Primates.” Proceedings of the Royal Society B: Biological Sciences 264
1,388): 1,687–1,694.

Whiten, Andrew. 2011. “The Scope of Culture in Chimpanzees, Humans and
Ancestral Apes.” Philosophical Transactions

of the Royal Society of London B: Biological Sciences 366 1,567): 997–1,007.

Whitten, Patricia L. 1983. “Diet and Dominance among Female Vervet
Monkeys Cercopithecus aethiops).” American

Journal of Primatology 5 2): 139–159.

Wiens, Frank, and Annette Zitzmann. 2003. “Social Structure of the
Solitary Slow Loris Nycticebus coucang Lorisidae).”

Journal of Zoology 261 1): 35–46.

Zuberbühler, Klaus, David Jenny, and Redouan Bshary. 1999. “The Predator
Deterrence Function of Primate Alarm Calls.”

Ethology 105 6): 477–490.


      Zuberbühler, Klaus, Ronald Noë, and Robert M. Seyfarth. 1997.
      “Diana Monkey Long-Distance Calls: Messages for

Conspecifics and Predators.” Animal Behaviour 53 3): 589–604.


    Acknowledgements

The author is grateful to the editors for the opportunity to contribute
to this open-source textbook. She thanks Stephanie Etting for her
encouragement and support during the writing of this chapter. Her
suggestions, along with comments made by two anonymous reviewers on an
earlier version of this chapter, improved the final version
considerably. Finally, she thanks all the primatologists who came before
her, especially her advisor, Lynne A. Isbell, for their tireless efforts
to understand the behavior and ecology of the living primates. Without
their work, this chapter would not have been possible.


    Figure Attributions

Figure 6.1a Snow monkey baby milk time by Daisuke tashiro is used under
a CC BY-SA 2.0 License. Figure 6.1b Stone tool use by a capuchin monkey
by Tiago Falótico is used under a CC BY-SA 4.0 License. Figure 6.2
Laikipia location map by Nairobi123 is used under a CC BY-SA 3.0
License. Figure 6.3a Female patas monkey with infant by Karin Enstam
Jaffe is under a CC BY-NC 4.0 License. Figure 6.3b Patas habitat in
Laikipia, Kenya by Karin Enstam Jaffe is under a CC BY-NC 4.0 License.
Figure 6.3a Monkey 27996706462) by Martie Swart from Johannesburg, South
Africa is under a CC BY 2.0 License. Figure 6.4b Vervet habitat in
Laikipia, Kenya by Karin Enstam Jaffe is under a CC BY-NC 4.0 License.
Figure 6.5 Karin Enstam Jaffe observing patas monkeys in Laikipia, Kenya
by Rebecca Chancellor is under a CC BY-NC 4.0 License. Figure 6.6a
Spectral Tarsier Tarsius tarsier 7911549768) by Bernard DUPONT from
FRANCE has been modified

cropped) and is used under a CC BY-SA 2.0 License.

Figure 6.6b Mountain gorilla Gorilla beringei beringei) eating by
Charles J Sharp creator QS:P170,Q54800218 is used under a CC BY-SA 4.0
License.

Figure 6.7 Food abundance and food scarcity by Karin Enstam Jaffe
original to Explorations: An Open Invitation to Biological Anthropology
is under a CC BY-NC 4.0 License.

Figure 6.8 Food distribution patterns by Karin Enstam Jaffe original to
Explorations: An Open Invitation to Biological Anthropology is under a
CC BY-NC 4.0 License.

Figure 6.9 Food distribution patterns of folivores, frugivores, and
insectivores a derivative work by Karin Enstam Jaffe original to
Explorations: An Open Invitation to Biological Anthropology is under a
CC BY-NC 4.0 License. [Includes Green fruit tree, Lemon tree, and
Ladybug image, all from publicdomainvectors.org designated to the public
domain

CC0)].

Figure 6.10 Termite mound-Tanzania by Vierka Maráková, Slovakia
Krokodild) has been designated to the public domain CC0).

Figure 6.11a Patas Monkey Jr by alex roberts from San Francisco, USA is
used under a CC BY-SA 2.0 License.

Figure 6.11b Chlorocebus pygerythrus by Xlandfair at English Wikipedia
has been designated to the public domain

CC0).

Figure 6.11c Male Olive Baboon 2 by ryan harvey from Portland, OR is
used under a CC BY-SA 2.0 License. Figure 6.11d Komba ušatá2 by Petr
Hamerník is used under a CC BY-SA 4.0 License. Figure 6.12 Muriquis 3 by
Mônica Imbuzeiro is used under a CC BY-SA 4.0 License. Figure 6.13
Examples of primate communities table original to Explorations: An Open
Invitation to Biological Anthropology by Karin Enstam Jaffe is under a
CC BY-NC 4.0 License. Figure 6.14a Lion tailed macaque eating Lizard by
Prasadchangarath is used under a CC BY-SA 4.0 License. Figure 6.14b
Gombe Stream NP Beute by Ikiwaner is used under a GNU License. Figure
6.15a Leopard africa by JanErkamp at the English Wikipedia is used under
a CC BY-SA 3.0 License. Figure 6.15b Jaguar Panthera onca palustris)
male Rio Negro 2 by Charles J Sharp creator QS:P170,Q54800218 is used
under a CC BY-SA 4.0 License. Figure 6.15c Male Tiger Ranthambhore
3646793728) by Koshy Koshy is used under a CC BY 2.0 License. Figure
6.15d Fosa fotovideo by Bertal is used under a CC BY-SA 3.0 License.
Figure 6.15e Martial eagle Polemaetus bellicosus) by Charles J Sharp
creator QS:P170,Q54800218 is used under a CC BY-SA 4.0 License. Figure
6.15f Harpy Eagle with wings lifted by Jonathan Wilkins is used under a
CC BY-SA 3.0 License. Figure 6.15g Python natalensis G. J. Alexander by
Graham J. Alexander, University of the Witwatersrand has been designated
to the public domain CC0). Figure 6.16 Slow Loris by Jmiksanek is used
under a CC BY-SA 3.0 License. Figure 6.17 Monkey group by
Natureloverperson is used under a CC BY-SA 4.0 License. Figure 6.18a
Deforestation near Bukit Tiga Puluh NP by Aidenvironment 1998) is used
under a CC BY-SA 2.0 License. Figure 6.18b Lemur poaching 004 by author
who does not wish to be named for safety reasons is used under a CC BY
SA 3.0 License. Figure 6.19a Dierenpark Emmen baboon 2679944324) by
robin bos from heerenveen, the Netherlands is used under a CC BY 2.0
License. Figure 6.19b Male Gelada Baboon, Chenek, Simien Mountains
6190375633) by Rod Waddington from Kergunyah, Australia has been
modified cropped) and is used under a CC BY-SA 2.0 License. Figure 6.20a
Azy orangutan) at the Indianapolis Zoo by Tom Britt is used under a CC
BY 2.0 License. Figure 6.20b Orangutan male 15433476577) by Russ is used
under a CC BY 2.0 License. Figure 6.21a Emperor Tamarin with babies sf
by Brocken Inaglory is used under a CC BY-SA 3.0 License. Figure 6.21b
Family of Common Marmoset – REGUA – Brazil MG 9480 12930855765) by
Francesco Veronesi from Italy is used under a CC BY-SA 2.0 License.

Figure 6.22 Social and Mating Systems by Karin Enstam Jaffe original to
Explorations: An Open Invitation to Biological Anthropology is under a
CC BY-NC 4.0 License.

Figure 6.23a Jane Goodall HK by Jeekc is used under a CC BY-SA 3.0
License. Figure 6.23b US-223658 Dian Fossey 2925879356) by Mary-Lynn is
used under a CC BY 2.0 License. Figure 6.23c Dr Birute Galdikas by Simon
Fraser University – University Communications is used under a CC BY 2.0
License. Figure 6.24a Sexual swelling in female Hamadryas baboon by
Mamoritai is used under a CC BY-SA 2.0 License. Figure 6.24b Hamadryas
baboon at Giza Zoo by Hatem Moushir 36 by Hatem Moushir is used under a
CC BY-SA 3.0 License. Figure 6.25 Mandrill 08 by SuperJew is used under
a CC BY-SA 4.0 License. Figure 6.26 BabouinGeladaAuReveil by BluesyPete
is used under a CC BY-SA 3.0 License. Figure 6.27 Mandrill 09 by
SuperJew is used under a CC BY-SA 4.0 License. Figure 6.28a Uakari by
Coada dragos is used under a CC BY-SA 4.0 License. Figure 6.28b Ateles
belzebuth White-bellied spider monkey) 2 by Ewa is used under a CC BY
2.0 License. Figure 6.29 Lemur catta 004 by Alex Dunkel Visionholder) is
used under a CC BY-SA 3.0 License. Figure 6.30a Yakushima macaques
grooming each other by Grendelkhan is used under a CC BY-SA 4.0 License.
Figure 6.30b Tufted capuchin monkeys grooming session III by Adrian
Soldati is used under a CC BY-SA 4.0 License. Figure 6.30c Baboons
Wunania 012018 by Kim Toogood is used under a CC BY-SA 4.0 License.
Figure 6.30d Black-and-white ruffed lemur 03 by Mattis2412 has been
designated to the public domain CC0 1.0). Figure 6.31 Pan troglodytes,
tool use in Senegal by J. D. Pruetz, P. Bertolani, K. Boyer Ontl, S.
Lindshield, M. Shelley, and E. G. Wessling is used under a CC BY 4.0
License. Figure 6.32 Jigokudani hotspring in Nagano Japan 001 by
Yosemite is used under a CC BY-SA 3.0 License.