6 Meet the Living Primates

Quadrupedalism, walking on all fours, is the most common form of locomotion among primates. Quadrupedal animals usually have legs and arms that are about the same length and a tail for balance. Arboreal quadrupeds (Figure 6.11a) usually have shorter arms and legs and longer tails, while terrestrial quadrupeds (Figure 6.11b) have longer arms and legs and, often, shorter tails. These differences relate to the lower centre of gravity needed by arboreal quadrupeds for balance in trees and the longer tail required for better balance when moving along the tops of branches. Terrestrial quadrupeds have longer limbs to help them cover more distance more efficiently.

The third form of locomotion seen in primates is brachiation, the way of moving you used if you played on “monkey bars” as a child. Brachiation involves swinging below branches by the hands (Figure 6.12a). To be an efficient brachiator, a primate needs to have longer arms than legs, flexible shoulders and wrists, a short lower back, and no tail (Figure 6.12b). Some primates move via semi-brachiation, in which they swing below branches but do not have all of the same specializations as brachiators. Semi-brachiators have flexible shoulders, but their arms and legs are about the same length, which is useful because they are quadrupedal when on the ground. They also use long prehensile tails as a third limb when swinging (Figure 6.13). The underside of the tail has a tactile pad, resembling your fingerprints, for better grip.

Lastly, humans move around on two feet, called bipedalism. Some nonhuman primates will occasionally travel on two feet but do so awkwardly and never for long distances. Among mammals, only humans have evolved to walk with a striding gait on two legs as a primary form of locomotion.

Primate Diversity

As we begin exploring the different taxa of primates, it is important to keep in mind the hierarchical nature of taxonomic classification and how this relates to the key characteristics that will be covered. Figure 6.14 summarizes the major taxonomic groups of primates that you will learn about here. If you locate humans on the chart, you can trace our classification and see all of the categories getting more inclusive as you work your way up to the Order Primates. This means that humans will have the key traits of each of those groups. It is a good idea to refer to the figure to orient yourself as we discuss each taxon.

Suborder Strepsirrhini

The Order Primates is subdivided into Suborder Strepsirrhini and Suborder Haplorrhini, which, according to molecular estimates, split about 70–80 million years ago (Pozzi et al. 2014). The strepsirrhines include the groups commonly called lemurs, lorises, and galagos (Figure 6.15). Strepsirrhines differ from haplorrhines in many ways, most of which involve retaining ancestral traits from the earliest primates. Strepsirrhines do have two key derived traits that evolved after they diverged from the haplorrhines: the grooming claw (Figure 6.16) on the second digit of each foot, and the tooth comb (or dental comb) located on the lower, front teeth (Figure 6.17). In most strepsirrhines, there are six teeth in the toothcomb—four incisors and two canines. Other than the tooth comb, the teeth of strepsirrhines are fairly simple and are neither large or distinctive relative to haplorrhines.

Compared to haplorrhines, strepsirrhines rely more on nonvisual senses. Strepsirrhines get their name because they have wet noses (rhinariums) like cats and dogs, a trait that, along with a longer snout, reflect strepsirrhines’ greater reliance on olfaction relative to haplorrhines. Many strepsirrhines use scent marking, including rubbing scent glands or urine on objects in the environment to communicate with others. Additionally, many strepsirrhines have mobile ears that they use to locate insect prey and predators. While strepsirrhines have a better sense of smell than haplorrhines, their visual adaptations are more ancestral. Strepsirrhines have less convergent eyes than haplorrhines and therefore all have postorbital bars, whereas haplorrhines have full postorbital closure (see Figure 6.2). All strepsirrhines have a tapetum lucidum, a reflective layer at the back of the eye that reflects light and thereby enhances the ability to see in low-light conditions. It is the same layer that causes your dog or cat to have “yellow eye” when you take photos of them with the flash on. This is a trait thought to be ancestral among mammals as a whole.

Strepsirrhines also differ from haplorrhines in some aspects of their ecology and behaviour. The majority of strepsirrhines are solitary, traveling alone to search for food; a few taxa are more social. Most strepsirrhines are also nocturnal and arboreal. Strepsirrhines are, on average, smaller than haplorrhines, and so many of them have a diet consisting of insects and fruit, with few taxa eating primarily leaves. Lastly, most strepsirrhines are good at leaping, with several taxa specialized for vertical clinging and leaping. In fact, among primates, all but one of the vertical clinger leapers belong to the Suborder Strepsirrhini.

Strepsirrhines can be found all across Asia, Africa, and on the island of Madagascar (Figure 6.18). The Suborder Strepsirrhini is divided into two groups: (1) the lemurs of Madagascar and (2) the lorises, pottos, and galagos of Africa and Asia. By molecular estimates, these two groups split about 65 million years ago (Pozzi Et al. 2014).

Lemurs of Madagascar

Madagascar is an island off the east coast of Africa, and it is roughly the size of California, Oregon, and Washington combined. It has been separated from Africa for about 130 million years and from India for about 85 million years, which means it was already an island when strepsirrhines got there approximately 60–70 million years ago. Only a few mammal species ever reached Madagascar, and so when lemurs arrived they were able to flourish into a variety of forms.

The lemurs of Madagascar are much more diverse compared to their mainland counterparts, the lorises and galagos. While many Malagasy strepsirrhines are nocturnal, plenty of others are diurnal or cathemeral. They range in body size from the smallest of all primates, the mouse lemur, some species of which weigh a little over an ounce (see Figure 6.15), up to the largest of all strepsirrhines, the indri, which weighs up to about 20 pounds (Figure 6.19). Lemurs include species that are insectivorous, frugivorous, and folivorous. A couple of members of this group have unusual diets for primates, including the gummivorous fork-marked and bamboo lemurs, who are able to metabolize the cyanide in bamboo. The most unique lemur is the aye-aye (depicted in Figure 6.15). This nocturnal lemur has rodent-like front teeth that grow continuously and a long-bony middle finger that it uses to fish grubs out of wood. It has a very large brain compared to other strepsirrhines, which it fuels with a diet that includes bird’s eggs and other animal matter. Based on genetic estimates and morphological studies, it is believed that aye-ayes were the first lemurs to separate from all other strepsirrhines and to evolve on their own since strepsirrhines arrived in Madagascar (Matsui Et al. 2009).

Lemurs are also diverse in terms of social behaviour: Many lemurs are solitary foragers, some live in pairs, others in small groups, still others in larger groups, and some, like the red-ruffed lemur, live in unique and complex social groups (Vasey 2006). Lemurs include some of the best vertical clingers and leapers, and while many lemurs are quadrupedal, even the quadrupedal lemurs are quite adept at leaping. Malagasy strepsirrhines also exhibit a few unusual traits. They are highly seasonal breeders, often mating only during a short window once a year (Wright 1999). Female ring-tailed lemurs, for example, come into estrus one day a year for a mere six hours. Unlike most primates, where males are typically large and dominant, Malagasy strepsirrhines feature socially dominant females that are similar in size to males and have priority access to resources.

Lorises, Pottos, and Galagos of Asia and Africa

Unlike the lemurs of Madagascar, lorises, pottos, and galagos live in areas where they share their environments with monkeys and apes, who often eat similar foods. Lorises live across South and Southeast Asia, while pottos and galagos live across Central Africa. Because of competition with larger-bodied monkeys and apes, mainland strepsirrhines are more restricted in the niches they can fill in their environments and so are less diverse than the lemurs.

The strepsirrhines of Africa and Asia are all nocturnal and solitary, with little variation in body size and diet. For the most part, the diet of lorises, pottos, and galagos consists of fruits and insects. A couple of species eat more gum, but overall the diet of this group is narrow when compared to the Malagasy lemurs. Lorises (Figure 6.20) and pottos are known for being slow, quadrupedal climbers, moving quietly through the forests to avoid being detected by predators. These strepsirrhines have developed additional defences against predators. Lorises, for example, eat a lot of caterpillars, which makes their saliva slightly toxic. Loris mothers bathe their young in this toxic saliva, making the babies unappealing to predators. In comparison to the slow-moving lorises and pottos, galagos are active quadrupedal runners and leapers that scurry about the forests at night. Galagos make distinctive calls that sound like a baby crying, which has led to their nickname “bushbabies.” Figure 6.21 summarizes the key differences between these two groups of strepsirrhines.

Figure 6.21: Strepsirrhini at a glance: This table summarizes the key differences between the two groups of strepsirrhines. Credit: Strepsirrhines at a glance table (Figure 5.19) original to Explorations: An Open Invitation to Biological Anthropology by Stephanie Etting is a collective work under a CC BY-NC-SA 4.0 License. [Includes Ringtailed Lemurs in Berenty by David Dennis, CC BY-SA 2.0; Komba ušatá by Petr Hamerník, CC BY-SA 4.0.]

	Lemurs	Lorises, Pottos, and Galagos
Geographic range	Madagascar	South and Southeast Asia Central Africa
Activity patterns	Diurnal, nocturnal, or cathemeral	Nocturnal
Dietary types	Insectivore, frugivore, or folivore	Insectivore, frugivore
Social groupings	Solitary, pairs, or small to large groups	Solitary
Forms of locomotion	Vertical clinger leapers, quadrupedal	Slow quadrupedal climbers and active quadrupedal runners

Suborder Haplorrhini

When the two primate suborders split from one another, strepsirrhines retained more ancestral traits while haplorrhines developed more derived traits, which are discussed below.

As mentioned earlier, haplorrhines have better vision than strepsirrhines. This is demonstrated by the full postorbital closure protecting the more convergent eyes that haplorrhines possess (with one exception seen in Figure 6.2). Most haplorrhines are trichromatic, and all have a fovea, a depression in the retina at the back of the eye containing concentrations of cells that allows them to see things very close up in great detail. The heavier reliance on vision over olfaction is also reflected in the shorter snouts ending with the dry nose (no rhinarium) of haplorrhines. All but two genera of living haplorrhines are active during the day, so this group lacks the tapetum lucidum that is so useful to nocturnal species. On average, haplorrhines also have larger brains relative to their body size when compared with strepsirrhines.

The Haplorrhini differ from the Strepsirrhini in their ecology and behaviour as well. Haplorrhines are generally larger than strepsirrhines, and they tend to be folivorous and frugivorous. This dietary difference is reflected in the teeth of haplorrhines, which are broader with more surface area for chewing. The larger body size of this taxon also influences locomotion. Only one haplorrhine is a vertical clinger and leaper. Most members of this suborder are quadrupedal, with one subgroup specialized for brachiation. A few haplorrhine taxa are monomorphic, meaning males and females are the same size, but many members of this group show moderate to high sexual dimorphism in body size and canine size. Haplorrhines also differ in social behaviour. All but two haplorrhines live in groups, which is very different from the primarily solitary strepsirrhines. Differences between the two suborders are summarized in Figure 6.22.

Figure 6.22: Suborders at a glance: This table summarizes the key differences between the two primate suborders. Credit: Suborders at a glance table (Figure 5.20) original to Explorations: An Open Invitation to Biological Anthropology by Stephanie Etting is a collective work under a CC BY-NC-SA 4.0 License. [Includes Black-and-White Ruffed Lemur, Mantadia, Madagascar by Frank Vassen, CC BY 2.0; Crab eating macaque face by Bruce89, CC BY-SA 4.0.]

	Suborder Strepsirrhini	Suborder Haplorrhini
Sensory adaptations	Rhinarium Longer snout Eyes less convergent Postorbital bar Tapetum lucidum Mobile ears	No rhinarium Short snout Eyes more convergent Postorbital plate No tapetum lucidum Many are trichromatic Fovea
Dietary differences	Mostly insectivores and frugivores, few folivores	Few insectivores, mostly frugivores and folivores
Activity patterns and Ecology	Mostly nocturnal, few diurnal or cathemeral Almost entirely arboreal	Only two are nocturnal, rest are diurnal Many arboreal taxa, also many terrestrial taxa
Social groupings	Mostly solitary, some pairs, small to large groups	Only two are solitary, all others live in pairs, small to very large groups
Sexual dimorphism	Minimal to none	Few taxa have little/none, many taxa show moderate to high dimorphism

Suborder Haplorrhini is divided into three infraorders: Tarsiiformes, which includes the tarsiers of Asia; Platyrrhini, which includes the monkeys of Central and South America; and Catarrhini, a group that includes the monkeys of Asia and Africa, apes, and humans. According to molecular estimates, tarsiers split from the other haplorrhines close to 70 million years ago, and platyrrhines split from catarrhines close to 46 million years ago (Pozzi Et al. 2014).

Infraorder Tarsiiformes of Asia

Today, the Infraorder Tarsiiformes includes only one genus, Tarsius (Figure 6.23). Tarsiers are small-bodied primates that live in Southeast Asian forests (Figure 6.24) and possess an unusual collection of traits that have led to some debate about their position in the primate taxonomy. They are widely considered members of the haplorrhine group because they share several derived traits with monkeys, apes, and humans, including dry noses, a fovea, not having a tapetum lucidum, and eyes that are more convergent. Tarsiers also have some traits that are more like strepsirrhines and some that are unique. Tarsiers are the only haplorrhine that are specialized vertical clinger leapers, a form of locomotion only otherwise seen in some strepsirrhines. Tarsiers actually get their name because their ankle (tarsal) bones are elongated to provide a lever for vertical clinging and leaping. Tarsiiformes are also small, with most species weighing between 100 and 150 grams. Like strepsirrhines, tarsiers are nocturnal, but because they lack a tapetum lucidum, tarsiers compensate by having enormous eyes. In fact, each eye of a tarsier is larger than its brain. These large eyes allow enough light in for tarsiers to still be able to see well at night without the reflecting layer in their eyes. To protect their large eyes, tarsiers have a partially closed postorbital plate that appears somewhat intermediate between the postorbital bar of strepsirrhines and the full postorbital closure of other haplorrhines (Figure 6.25). Tarsiers have different dental formulas on their upper and lower teeth. On the top, the dental formula is 2:1:3:3, but on the bottom it is 1:1:3:3. Other unusual traits of tarsiers include having two grooming claws on each foot and the ability to rotate their heads around 180 degrees, a trait useful in locating insect prey. The tarsier diet is considered faunivorous because it consists entirely of animal matter, making them the only primate not to eat any vegetation. They are only one of two living haplorrhines to be solitary, the other being the orangutan. Most tarsiers are not sexually dimorphic, like strepsirrhines, although males of a few species are slightly larger than females.

Two alternative classifications have emerged due to the unusual mix of traits that tarsiers have. Historically, tarsiers were grouped with lemurs, lorises, and galagos into a suborder called Prosimii. This classification was based on tarsiers, lemurs, lorises, and galagos all having grooming claws and similar lifestyles. Monkeys, apes, and humans were then separated into a suborder called the Anthropoidea. These suborder groupings were based on grade rather than clade. Today, most people use Suborders Strepsirrhini and Haplorrhini, which are clade groupings based on the derived traits that tarsiers share with monkeys, apes, and humans. The Strepsirrhini/Haplorrhini dichotomy is also supported by the genetic evidence that indicates tarsiers are more closely related to monkeys, apes, and humans (Jameson Et al. 2011). Figure 6.26 summarizes the unusual mix of traits seen in tarsiers.

Figure 6.26: Tarsiers at a glance: Tarsiers have a mix of traits that lead to debate about their classification. While they have some unique characteristics, they also have traits that superficially resemble strepsirrhines, and many derived traits shared with haplorrhines. Credit: Tarsiers at a glance table (Figure 5.24) original to Explorations: An Open Invitation to Biological Anthropology by Stephanie Etting is under a CC BY-NC 4.0 License.

Like Strepsirrhini	Unique	Like Haplorrhini
Very small Nocturnal Highly insectivorous Solitary Vertical clinger-leapers Little/no sexual dimorphism	Two grooming claws 2:1:3:3/1:1:3:3 dental formula Do not eat vegetation Can rotate their heads nearly 180 degrees	Almost full PO closure More convergent eyes No tapetum lucidum No rhinarium Genetic evidence Fovea

Infraorder Platyrrhini of Central and South America

The platyrrhines are the only nonhuman primates in Central and South America (Figure 6.27) and so, like the lemurs of Madagascar, have diversified into a variety of forms in the absence of competition. Infraorder Platyrrhini get their name from their distinctive nose shape. “Platy” means flat and “rhini” refers to noses, and, indeed, platyrrhines have noses that are flat and wide, with nostrils that are far apart, facing outward, and usually round in shape (Figure 6.28). This nose shape is very different from what we see in catarrhines.

On average, platyrrhines are smaller and less sexually dimorphic than catarrhines, and they have retained the more ancestral primate dental formula of 2:1:3:3. Platyrrhines are all highly arboreal, whereas many catarrhines spend significant time on the ground. The monkeys in Central and South America also differ in having less well-developed vision. This is reflected in the wiring in the visual system of the brain as well as in their polymorphic color vision. The genes that enable individuals to distinguish reds and yellows from blues and greens are on the X chromosome. Different genes code for being able to see different wavelengths of light so to distinguish between them you need to be heterozygous for seeing colour. The X chromosomes of platyrrhines each carry the genes for seeing one wavelength, so male platyrrhines (with only one X chromosome) are always dichromatic. Female platyrrhines can be dichromatic (if they are homozygous for one version of the colour vision gene) or trichromatic (if they are heterozygous) (Kawamura Et al. 2012). We currently know of two exceptions to this pattern among platyrrhines. Nocturnal owl monkeys are monochromatic, meaning that they cannot distinguish any colours. The other exception are howler monkeys, which have evolved to have two colour vision genes on each X chromosome. This means that both male and female howler monkeys are able to see reds and yellows. By contrast, catarrhine males and females are all trichromatic.

Platyrrhines include the smallest of the monkeys, the marmosets and tamarins (Figure 6.29), all of which weigh less than one kilogram and live in cooperative family groups, wherein usually only one female reproduces and everyone else helps carry and raise the offspring. They are unusual primates in that they regularly produce twins. Marmosets and tamarins largely eat gums and saps, so these monkeys have evolved claw-like nails that enable them to cling to the sides of tree trunks like squirrels as well as special teeth that allow them to gnaw through bark. Except for the Goeldi’s monkey, these small monkeys have one fewer molar than other platyrrhines, giving them a dental formula of 2:1:3:2.

The largest platyrrhines are a family that include spider monkeys, woolly spider monkeys, woolly monkeys, and howler monkeys (Figure 6.30). These monkeys can weigh up to 9–15 kg and have evolved prehensile tails that can hold their entire body weight. It is among this group that we see semi-brachiators, like the spider monkey (see Figure 6.13). To make them more efficient in this form of locomotion, spider monkeys evolved to not have thumbs so that their hands work more like hooks that can easily let go of branches while swinging. Howler monkeys are another well-known member of this group, earning their name due to their loud calls, which can be heard miles away. To make these loud vocalizations, howler monkeys have a specialized vocal system that includes a large larynx and hyoid bone. Howler monkeys are the most folivorous of the platyrrhines and are known for spending a large portion of their day digesting their food.

There are many other monkeys in Central and South America, including the gregarious capuchins (see Figure 6.28) and squirrel monkeys, the pair-living titi monkeys, and the nocturnal owl monkeys. There are also the seed-eating saki monkeys and uakaris. In many areas across Central and South America, multiple species of platyrrhines share the forests, with some even traveling together in association. According to molecular evidence, the diversity of platyrrhines that we see today seems to have originated about 25 million years ago (Schneider & Sampaio 2015). Figure 6.31 summarizes the key traits of platyrrhines relative to the other infraorders of Haplorrhini.

Figure 6.31: Platyrrhini at a glance: Summary of the key traits we use to distinguish platyrrhines. Traits indicated with an * are those with exceptions detailed in the text. Credit: Platyrrhini at a glance table (Figure 5.29) original to Explorations: An Open Invitation to Biological Anthropology by Stephanie Etting is under a CC BY-NC 4.0 License.

Platyrrhini traits

Flat nose with rounded nostrils pointing to the side Highly arboreal Less sexually dimorphic on average 2:1:3:3 dental formula* Polymorphic colour vision*

Infraorder Catarrhini of Asia and Africa

Infraorder Catarrhini includes Superfamily Cercopithecoidea (the monkeys of Africa and Asia) and Superfamily Hominoidea (apes and humans). Nonhuman catarrhines are found all over Africa and South and Southeast Asia, with some being found as far north as Japan. The most northerly and southerly catarrhines are cercopithecoid monkeys. In contrast, apes are less tolerant of drier, more seasonal environments and so have a relatively restricted geographic range.

Relative to other haplorrhine infraorders, catarrhines are distinguished by several characteristics. Catarrhines have a distinctive nose shape, with teardrop-shaped nostrils that are close together and point downward (Figure 6.32) and one fewer premolar than most other primates, giving us a dental formula of 2:1:2:3 (Figure 6.33). On average, catarrhines are the largest and most sexually dimorphic of all primates. Gorillas are the largest living primates, with males weighing up to 220 kg. The most sexually dimorphic of all primates are mandrills. Mandrill males not only have much more vibrant colouration than mandrill females but also have larger canines and can weigh up to three times more (Setchell Et al. 2001). The larger body size of catarrhines is related to the more terrestrial lifestyle of many members of this infraorder. In fact, the most terrestrial of living primates can be found in this group. Among all primates, vision is the most developed in catarrhines. Catarrhines independently evolved the same adaptation as howler monkeys in having each X chromosome with genes to distinguish both reds and yellows, so all male and female catarrhines are trichromatic, which is useful for these diurnal primates.

The two superfamilies of catarrhines—Superfamily Cercopithecoidea, the monkeys of Africa and Asia, and Superfamily Hominoidea, which includes apes and humans—are believed to have split about 32 million years ago based on molecular evidence (Pozzi Et al. 2014). This fits with the fossil record, which shows evidence of these lineages by about 25 million years ago (see Chapters 8-9).

Superfamily Cercopithecoidea of Africa and Asia

Compared to hominoids, cercopithecoids have an ancestral quadrupedal body plan with two key derived traits. The first derived trait of cercopithecoids is their bilophodont molars (“bi” meaning two, “loph” referring to ridge, and “dont” meaning tooth). If you refer back to Figure 6.33, you will see how the molars of cercopithecoids have four cusps arranged in a square pattern and have two ridges connecting them. It is thought that this molar enabled these monkeys to eat a wide range of foods, thus allowing them to live in habitats that apes cannot. The other key derived trait that all cercopithecoids share is having ischial callosities (Figure 6.34). The ischium is the part of your pelvis that you are sitting on right now (see Appendix A: Osteology). In cercopithecoids, this part of the pelvis has a flattened surface that, in living animals, has callused skin over it. These function as seat pads for cercopithecoids, who often sit above branches when feeding and resting.

Cercopithecoid monkeys are the most geographically widespread group of nonhuman primates (Figure 6.35). Since their divergence from hominoids, this monkey group has increased in numbers and diversity due, in part, to their fast reproductive rates. On average, cercopithecoids will reproduce every one to two years, whereas hominoids will reproduce once every four to nine years, depending on the taxon.

Cercopithecoidea is split into two groups, the leaf monkeys and the cheek-pouch monkeys. Both groups coexist in Asia and Africa; however, the majority of leaf monkey species live in Asia with only a few taxa in Africa. In contrast, only one genus of cheek-pouch monkey lives in Asia, and all the rest of them in Africa. As you can probably guess based on their names, the two groups differ in terms of diet. Leaf monkeys are primarily folivores, with some species eating a significant amount of seeds. Cheek-pouch monkeys tend to be more frugivorous or omnivorous, with one taxon, geladas, eating primarily grasses. The two groups also differ in some other interesting ways. Leaf monkeys tend to produce infants with natal coats—infants whose fur is a completely different colour from their parents (Figure 6.36). Leaf monkeys are also known for having odd noses (Figure 6.37), and so they are sometimes called “odd-nosed monkeys.” Cheek-pouch monkeys are able to pack food into their cheek pouches (Figure 6.38), thus allowing them to move to a location safe from predators or aggressive individuals of their own species where they can eat in peace.

Superfamily Hominoidea of Africa and Asia

Superfamily Hominoidea of Africa and Asia (Figure 6.39) includes the largest of the living primates: apes and humans. Whereas cercopithecoid monkeys have bilophodont molars, hominoids have the more ancestral Y-5 molars, which feature five cusps separated by a “Y”-shaped groove pattern (see Figure 6.33). The Y-5 molar was present in the common ancestors of hominoids and cercopithecoids, thus it is the more ancestral molar pattern of the two. Hominoids differ the most from other primates in our body plans, due to the unique form of locomotion that hominoids are adapted for: brachiation (Figure 6.40).

To successfully swing below branches, many changes to the body needed to occur. Hominoid arms are much longer than the legs to increase reach, and the lower back is shorter and less flexible to increase control when swinging. The torso, shoulders, and arms of hominoids have evolved to increase range of motion and flexibility (see again Figure 6.12). The clavicle, or collar bone, is longer to stabilize the shoulder joint out to the side, thus enabling us to rotate our arms 360 degrees. Hominoid rib cages are wider side to side and shallower front to back than those of cercopithecoids and we do not have tails, as tails are useful for balance when running on all fours but generally not useful while swinging. Hominoids also have modified ulnae, one of the two bones in the forearm (see Appendix A: Osteology). At the elbow end of the ulna, hominoids have a short olecranon process, which allows for improved extension in our arms. At the wrist end of the ulna, hominoids have a short styloid process, which enables us to have very flexible wrists, a trait critical for swinging. Both the olecranon process and styloid process are long in quadrupedal animals who carry much of their weight on their forelimbs when traveling and who therefore need greater stability rather than flexibility in those joints.

Figure 6.40: Quadrupedalism vs. brachiation: Summary of the key anatomical differences between a quadrupedal primate and one adapted for brachiation. To view these traits using photos of bones, check out the interactive skeletal websites in “Further Explorations” below. Credit: Quadrupedalism vs. Brachiation table (Figure 5.39) original to Explorations: An Open Invitation to Biological Anthropology by Stephanie Etting is under a CC BY-NC 4.0 License.

	Quadrupedalism	Brachiation
Arm length vs. leg length	About equal	Arms are longer
Shoulder position	More on the front	Out to the side
Ribcage shape	Deep front-to-back Narrow side-to-side	Shallow front-to-back Wide side-to-side
Length of lower back	Long	Short
Collar bone length	Short	Long
Ulnar olecranon process	Long	Short
Ulnar styloid process	Long	Short
Tail	Short to long	None

Apes and humans also differ from other primates in behaviour and life history characteristics. Hominoids all seem to show some degree of female dispersal at sexual maturity but, as you will learn in Chapter 7, it is more common that males leave. Some apes show males dispersing in addition to females, but the hominoid tendency for female dispersal is a bit unusual among primates. Our superfamily is also characterized by the most extended life histories of all primates. All members of this group take a long time to grow and reproduce much less frequently compared to cercopithecoids. The slow pace of this life history is likely related to why hominoids have decreased in diversity since they first evolved. Figure 6.41 summarizes the key traits of Infraorder Catarrhini and its two superfamilies. Today, there are only five types of hominoids left: gibbons and siamangs, orangutans, gorillas, chimpanzees and bonobos, and humans.

Figure 6.41a: Catarrhini at a glance: Summary of key traits of the Infraorder Catarrhini. Credit: Catarrhini at a glance (Figure 5.40) original to Explorations: An Open Invitation to Biological Anthropology by Stephanie Etting is a collective work under a CC BY-NC 4.0 License. [Includes Duskyleafmonkey1 by Robertpollai, CC BY 3.0 AT; Male Bornean Orangutan – Big Cheeks by Eric Kilby, CC BY-SA 2.0.]

Infraorder Catarrhini
Downward facing, tear-drop shaped nostrils, close together Arboreal and more terrestrial taxa On average, largest primates On average, most sexually dimorphic taxonomic group 2:1:2:3 dental formula All trichromatic

Figure 6.41b: Characteristics used to distinguish between the two Catarrhini superfamilies. Credit: Catarrhini at a glance (Figure 5.40) original to Explorations: An Open Invitation to Biological Anthropology by Stephanie Etting is a collective work under a CC BY-NC 4.0 License. [Includes Duskyleafmonkey1 by Robertpollai, CC BY 3.0 AT; Male Bornean Orangutan – Big Cheeks by Eric Kilby, CC BY-SA 2.0.]

Superfamily Cercopithecoidea	Superfamily Hominoidea
Wide geographic distribution Bilophodont molars Ischial callosities Reproduce every 1–2 years	Tropical forests of Africa and Asia Y-5 molars Adaptations for brachiation Reproduce every 4–9 years

Family Hylobatidae of Southeast Asia

The number of genera in this group has been changing in recent years, but the taxa broadly encompasses gibbons and siamangs. Both are found across Southeast Asian tropical forests. Gibbons weigh, on average, about 13 pounds and tend to be more frugivorous, whereas siamangs are larger than gibbons and also more folivorous. Unlike the larger-bodied apes (orangutans, chimps, bonobos, and gorillas) who make nests to sleep in every night, gibbons and siamangs will develop callused patches on their ischium resembling ischial callosities. Gibbon species are quite variable in their colouration and markings, while siamangs are all black with big throat sacs that are used in their exuberant vocalizations (Figure 6.42). Both gibbons and siamangs live in pairs with very little sexual dimorphism, although males and females do differ in colouration in some gibbon species.

Pongo of Southeast Asia

The Genus Pongo refers to orangutans. These large red apes are found in Southeast Asia, with the two well-known species each living on the islands of Borneo and Sumatra. A third, very rare species, was recently discovered in Southern Sumatra (Nater Et al. 2017). Orangutans are highly frugivorous but will supplement their diet with leaves and bark when fruit is less available. As mentioned earlier, orangutans are the only diurnal, solitary taxon among primates and are extremely slow to reproduce, producing only one offspring about every seven to nine years. They are highly sexually dimorphic (Figure 6.43 a & b), with fully developed, “flanged” males being approximately twice the size of females. These males have large throat sacs; long, shaggy coats; and cheek flanges. The skulls of male orangutans often feature a sagittal crest, which is believed to function as additional attachment area for chewing muscles as well as a trait used in sexual competition (Balolia, Soligo, & Wood 2017). An unusual feature of orangutan biology is male bimaturism. Male orangutans are known to delay maturation until one of the more dominant, flanged males disappears. The males that delay maturation are called “unflanged” males, and they can remain in this state for their entire life. Unflanged males resemble females in their size and appearance and will sneak copulations with females while avoiding the bigger, flanged males. Flanged and unflanged male orangutans represent alternative reproductive strategies, both of which successfully produce offspring (Utami Et al. 2002).

 

Gorilla of Africa

There are several species of gorillas that can be found across Central Africa. Gorilla males, like orangutan males, are about twice the size of female gorillas (Figures 6.44a & b). When on the ground, gorillas use a form of quadrupedalism called knuckle-walking, wherein the fingers are curled under and the weight is carried on the knuckles. Male gorillas have a large sagittal crest and large canines compared with females. Adult male gorillas are often called “silverbacks” because when they reach about twelve to thirteen years old, the hair on their backs turns silvery grey. Gorillas typically live in groups of one male and several females. Gorillas are considered folivorous, although some species can be more frugivorous depending on fruit seasonality (Remis 1997).

Pan of Africa

The Genus Pan includes two species: Pan troglodytes (the common chimpanzee) and Pan paniscus (the bonobo). These species are separated by the Congo River, with chimpanzees ranging across West and Central Africa and bonobos located in a restricted area south of the Congo River. Chimpanzees and bonobos both have broad, largely frugivorous diets.The two species differ morphologically in that bonobos are slightly smaller, have their hair parted down the middle of their foreheads, and are born with dark faces (Figure 6.45). In contrast, chimpanzees do not have the distinctive parted hair and are born with light faces that darken as they mature (Figure 6.46). Chimpanzees and bonobos live in a grouping called a fission-fusion community, which you will learn more about in Chapter 6. Both species are moderately sexually dimorphic, with males about 20% larger than females. When on the ground, chimpanzees and bonobos knuckle-walk like gorillas do.

Homo

The last member of the Hominoidea to discuss is our own taxon, Genus Homo. Later chapters will discuss the many extinct species of Homo, but today there is only one living species of Homo, our own species, sapiens. While it is interesting to focus on how humans differ from apes in many aspects of our morphology, behaviour, and life history, one objective of this chapter, and of biological anthropology in general, is to understand our place in nature. This means looking for aspects of human biology that link us to the taxonomic diversity we have discussed. To that end, here we will focus on similarities humans share with other hominoids.

Like other hominoids, humans lack a tail and possess upper-body adaptations for brachiation. While our lower body has been modified for a bipedal gait, we are still able to swing from branches and throw a baseball, all thanks to our mobile shoulder joint. Humans, like other hominoids, also have a Y-5 cusp pattern on our molars. All hominoids, including humans, have an extended life history, taking time to grow and develop, and reproducing slowly over a long life span. Lastly, while humans show a great deal of variation across cultures, many human societies show tendencies for female dispersal (Burton Et al. 1996).

Among the hominoids, humans show particular affinities with other members of the African Clade, Pan and Gorilla. Humans share over 96% of our DNA with gorillas (Scally Et al. 2012), and over 98% with Pan (Ebersberger Et al. 2002). Even without this strong genetic evidence, the African Clade of hominoids share many morphological similarities, including having wide-set eye sockets and backward-sweeping cheekbones. Today, Pan and Gorilla knuckle-walk when on the ground, and it has been suggested the last common ancestor of chimpanzees, bonobos, gorillas, and humans did as well (Richmond, Begun, & Strait 2001). Further, humans, chimpanzees, and bonobos all live in fission-fusion social groups characterized by shared behaviours, like male cooperation in hunting and territoriality, as well as tool use.

Summary

The Order Primates is a diverse and fascinating group of animals united in sharing a suite of characteristics—visual specialization, grasping hands and feet, large brains, and extended life histories—that differentiates us from other groups of mammals. In this chapter, we surveyed the major taxonomic groups of primates, discussing where humans fit among our close relatives as well as discovering that primates are interesting animals in their own right. We discussed a range of key traits used to distinguish between the many taxa of living primates, including dietary, locomotor, and behavioural characteristics. Because of our long, shared evolutionary history with these animals, nonhuman primates provide a crucial resource for understanding our current biology. In Chapter 7, you will discover the fascinating and complex social behaviours of nonhuman primates, which provide further insight into our evolutionary biology.

Key Terms

Activity pattern: Refers to the time of day an animal is typically active.

African clade: A grouping that includes gorillas, chimpanzees, bonobos, humans, and their extinct relatives.

Analogy: When two or more taxa exhibit similar traits that have evolved independently, the similar traits evolve due to similar selective pressures. (Also sometimes called convergent evolution, parallel evolution, or homoplasy.)

Ancestral trait: A trait that has been inherited from a distant ancestor.

Arboreal: A descriptor for an organism that spends most of its time in trees.

Asian clade: A grouping that includes orangutang and their extinct relatives.

Bilophodont: Molar pattern of cercopithecoid monkeys in which there are usually four cusps that are arranged in a square pattern and connected by two ridges.

Bipedalism: Walking on two legs.

Brachiation: A form of locomotion in which the organism swings below branches using the forelimbs.

Bunodont: Low, rounded cusps on the cheek teeth.

Canines: In most primates, these are the longest of the teeth, often conical in shape and used as a weapon against predators or others of their species.

Cathemeral: Active throughout the 24-hour period.

Clade: A grouping based on ancestral relationships; a branch of the evolutionary tree.

Cusps: The bumps on the chewing surface of the premolars and molars, which can be quite sharp in some species.

Dental formula: The number of each type of tooth in one quadrant of the mouth, written as number of incisors: canines: premolars: molars.

Derived trait: A trait that has been recently modified, most helpful when assigning taxonomic classification.

Diastema: A space between the teeth, usually for large canines to fit when the mouth is closed.

Dichromatic: Being able to see only blues and greens.

Diurnal: Active during the day.

Dry nose: The nose and upper lip are separated and the upper lip can move independently; sometimes referred to as a “hairy” or “mobile” upper lip.

Ethnoprimatology: A subarea of anthropology that studies the complexities of human-primate relationships in the modern environment.

Evolutionary trade-off: When an organism, which is limited in the time and energy it can put into aspects of its biology and behaviour, is shaped by natural selection to invest in one adaptation at the expense of another.

Faunivorous: Having a diet consisting entirely of animal matter: insects, eggs, lizards, etc.

Folivore: Having a diet consisting primarily of leaves.

Fovea: A depressed area in the retina at the back of the eye containing a concentration of cells that allow one to focus on objects very close to one’s face.

Frugivore: Having a diet consisting primarily of fruit.

Generalized trait: A trait that is useful for a wide range of tasks.

Grade: A grouping based on overall similarity in lifestyle, appearance, and behaviour.

Grooming claw: A claw present on the second pedal digit in strepsirrhines.

Gummivore: Having a diet consisting primarily of gums and saps.

Heterodont: Having different types of teeth.

Homology: When two or more taxa share characteristics because they inherited them from a common ancestor.

Hone: When primates sharpen their canines by wearing them on adjacent teeth.

Incisors: The spatula-shaped teeth at the front of the mouth.

Insectivore: Having a diet consisting primarily of insects.

Ischial callosities: Modified seat bones of the pelvis that are flattened and over which calluses form; function as seat pads for sitting and resting atop branches.

Knuckle-walking: A form of quadrupedal movement used by Gorilla and Pan when on the ground, wherein the front limbs are supported on the knuckles of the hands.

Life history: Refers to an organism’s pace of growth, reproduction, lifespan, etc.

Locomotion: How an organism moves around.

Male bimaturism: Refers to the alternative reproductive strategies in orangutans in which males can delay maturation, sometimes indefinitely, until a fully mature, “flanged” male disappears.

Molars: The largest teeth at the back of the mouth; used for chewing. In primates, these teeth usually have between three and five cusps.

Monochromatic: Being able to see only in shades of light to dark, no colour.

Monomorphic: When males and females of a species do not exhibit significant sexual dimorphism.

Natal coat: Refers to the contrasting fur colour of baby leaf monkeys compared to adults.

Nocturnal: Active at night.

Olecranon process: Bony projection at the elbow end of the ulna.

Opposable thumb or opposable big toe: Having thumbs and toes that go in a different direction from the rest of the fingers, allows for grasping with hands and feet.

Pentadactyly: Having five digits or fingers and toes.

Polymorphic colour vision: A system in which individuals of a species vary in their abilities to see colour. In primates, it refers to males being dichromatic and females being either trichromatic or dichromatic.

Postorbital bar: A bony ring that surrounds the eye socket, open at the back.

Postorbital closure/plate: A bony plate that provides protection to the side and back of the eye.

Prehensile tail: A tail that is able to hold the full body weight of an organism, which often has a tactile pad on the underside of the tip for improved grip.

Premolars: Smaller than the molars, used for chewing. In primates, these teeth usually have one or two cusps.

Quadrupedalism: Moving around on all fours.

Rhinariums: Wet noses; resulting from naked skin of the nose which connects to the upper lip and smell-sensitive structures along the roof of the mouth.

Sagittal crest: A bony ridge along the top/middle of the skull, used for attachment of chewing muscles.

Scent marking: The behaviour of rubbing scent glands or urine onto objects as a way of communicating with others.

Semi-brachiation: A form of locomotion in which an organism swings below branches using a combination of forelimbs and prehensile tail.

Sexually dimorphic: When a species exhibits sex differences in morphology, behaviour, hormones, and/or colouration.

Shearing crests: Sharpened ridges that connect cusps on a bilophodont molar.

Specialized trait: A trait that has been modified for a specific purpose.

Styloid process of ulna: A bony projection of the ulna at the end near the wrist.

Tactile pads: Sensitive skin at the fingertips for sense of touch. Animals with a prehensile tail have a tactile pad on the underside of the tail as well.

Tapetum lucidum: Reflecting layer at the back of the eye that magnifies light.

Terrestrial: A descriptor for an organism that spends most of its time on the ground.

Tetrachromatic: Having the ability to see reds, yellows, blues, greens, and ultraviolet.

Tooth comb or dental comb: A trait of the front, lower teeth of strepsirrhines in which, typically, the four incisors and canines are long and thin and protrude outward.

Trichromatic colour vision: Being able to distinguish yellows and reds in addition to blues and greens.

Vertical clinging and leaping: A locomotor pattern in which animals are oriented upright while clinging to vertical branches, push off with hind legs, and land oriented upright on another vertical branch.

Y-5 molar: Molar cusp pattern in which five molar cusps are separated by a “Y”-shaped groove pattern.

For Further Exploration

Animal Diversity Web. This website is hosted by the Zoology Department at the University of Michigan. It has photographs of skulls, teeth, hands, arms, and feet of many primate species.

eSkeletons. This website is hosted by the Department of Anthropology at University of Texas, Austin. It is an interactive website where you can compare specific bones from different species of primates.

Fleagle, John G. 2013. Primate Adaptation and Evolution. Third edition. San Diego: Academic Press.

Fuentes, Agustín, and Kimberley J. Hockings. 2010. “The Ethnoprimatological Approach in Primatology.” American Journal of Primatology 72 (10): 841–847.

Rowe, Noel. 1996. Pictorial Guide to the Living Primates. Charlestown, RI: Pogonias Press.

Whitehead, Paul F., William K. Sacco, and Susan B. Hochgraf. 2005. A Photographic Atlas for Physical Anthropology. Englewood, CO: Morton Publishing.

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Acknowledgements

The author would very much like to thank the editors for the opportunity to contribute to this textbook, along with anonymous reviewers who provided useful feedback on earlier drafts of this chapter. She would particularly like to thank Karin Enstam Jaffe for her support and encouragement during the writing of this chapter and its revision. Most of all, the author would like to thank all of the Introduction to Biological Anthropology students that she has had over the years who have listened to her lecture endlessly on these animals that she finds so fascinating and who have helped her to hone her pedagogy in a field that she loves.