5.4: 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 5.14 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.

Figure 5.14: This taxonomy chart shows the major groups of primate taxa, starting with the largest category (Order) and moving to more specific categories and examples. Credit: Primate taxonomy char (Figure 5.11) 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 Lemur catta Linnaeus, 1759 by Roberto Díaz Sibaja, CC BY 3.0; Lorisoidea original to Explorations: An Open Invitation to Biological Anthropology by Katie Nelson, CC BY-NC 4.0; Tarsiiformes original to Explorations: An Open Invitation to Biological Anthropology by Mary Nelson, CC BY-NC 4.0; Cebinae Bonaparte, 1831 by Sarah Werning, CC BY 3.0; Colobus guereza Ruppell, 1835 by Yan Wong, designated to the public domain (CC0); Papio cynocephalus by Owen Jones, designated to the public domain (CC0); animals silhouette wolf elephant (2755766) by mohamed_hassan, Pixabay License.] [Image Description].

Suborder Strepsirrhini

Figure 5.15: (Clockwise from top right) sifaka, black-and-white ruffed lemur, loris, galago, slender loris, mouse lemur, aye-aye, and ring-tailed lemur. Credit: Extant Strepsirrhini a collective work by Mark Dumont is under a CC BY-SA 3.0 License. [Includes Katta család by Veszprémi Állatkert, CC BY-SA 3.0; Aye-aye at night in the wild in Madagascar by Frank Vassen, CC BY 2.0; Diademed ready to push off by Michael Hogan, designated to the public domain (CC0); Juvenile Black-and-White Ruffed Lemur, Mantadia, Madagascar by Frank Vassen, CC BY 2.0; Microcebus murinus -Artis Zoo, Amsterdam, Netherlands-8a by Arjan Haverkamp, CC BY 2.0; Slow Loris by Jmiksanek, CC BY-SA 3.0; Slender Loris by Kalyan Varma (Kalyanvarma), CC BY-SA 4.0; Garnett’s Galago (Greater Bushbaby) by Mark Dumont, CC BY 2.0.]

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 5.15). 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 5.16) on the second digit of each foot, and the tooth comb (or dental comb) located on the lower, front teeth (Figure 5.17). 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.

Figure 5.16: The foot of a ring-tailed lemur showing its grooming claw on the second digit. Credit: Lemur catta toilet claw by Alex Dunkel (Maky) is under a CC BY 3.0 License.

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 5.2). 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.

Figure 5.17: The lower front teeth of a ring-tailed lemur showing the six teeth of the tooth comb: four incisors and two canines. The teeth that superficially look like canines are premolars. Credit: Lemur catta toothcomb by Alex Dunkel (Maky) is under a CC BY 3.0 license.

Strepsirrhines also differ from haplorrhines in some aspects of their ecology and behavior. 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 5.18). 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).

Figure 5.18: Geographic distribution of living strepsirrhines. Lemurs live only on Madagascar, while lorises and galagos live across Central Africa and South and Southeast Asia. Credit: Geographic distribution of living strepsirrhines (Figure 5.16) original to Explorations: An Open Invitation to Biological Anthropology by Elyssa Ebding at GeoPlace, California State University, Chico is under a CC BY-NC 4.0 License.

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 5.15), up to the largest of all strepsirrhines, the indri, which weighs up to about 20 pounds (Figure 5.19). 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 5.15). 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).

Figure 5.19: Indris, the largest of the lemurs. These folivorous lemurs are vertical clingers and leapers and live in pairs. Credit: Indri indri 0003 by Christophe Germain is under a CC BY-SA 4.0 License.

Lemurs are also diverse in terms of social behavior: 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

Figure 5.20: This slow loris, like all others in this taxonomic group, is solitary and nocturnal, with a diet heavy in insects and fruit. Credit: Nycticebus coucang 002 by David Haring / Duke Lemur Center is under a CC BY-SA 3.0 License.

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 5.20) 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 defenses 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 5.21 summarizes the key differences between these two groups of strepsirrhines.

Figure 5.21: 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 5.2). 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 behavior 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 behavior. 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 5.22.

Figure 5.22: 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

Figure 5.23: Tarsiers are the only living representatives of this Infraorder. Credit: Tarsier Sanctuary, Corella, Bohol (2052878890) by yeowatzup is under a CC BY 2.0 License.

Figure 5.24: Tarsiiformes are found in the tropical forests of multiple islands in Southeast Asia including Sumatra, Borneo, Celebes, and the Philippines. Credit: Infraorder Tarsiiformes of Asia map (Figure 5.22) original to Explorations: An Open Invitation to Biological Anthropology by Elyssa Ebding at GeoPlace, California State University, Chico is under a CC BY-NC 4.0 License.

Today, the Infraorder Tarsiiformes includes only one genus, Tarsius (Figure 5.23). Tarsiers are small-bodied primates that live in Southeast Asian forests (Figure 5.24) 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 5.25). 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.

Figure 5.25: Skull of a tarsier showing very large eye sockets and partially closed postorbital plates. Credit: Tarsier skull by Andrew Bardwell is under a CC BY-SA 2.0 License.

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 5.26 summarizes the unusual mix of traits seen in tarsiers.

Figure 5.26: 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

Figure 5.27: Geographic distribution of the platyrrhines across the southern part of Central America and the tropical and termporate regions of South America. Credit: Infraorder Platyrrhini map original to Explorations: An Open Invitation to Biological Anthropology by Elyssa Ebding at GeoPlace, California State University, Chico is under a CC BY-NC 4.0 License.

The platyrrhines are the only nonhuman primates in Central and South America (Figure 5.27) 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 5.28). 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 color. 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 color 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 colors. The other exception are howler monkeys, which have evolved to have two color 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.

Figure 5.28: A capuchin monkey demonstrating a typical platyrrhine nose shape with round nostrils pointing outward on a flat nose. Credit: CARABLANCA – panoramio by Manuel Velazquez is under a CC BY 3.0 License.

Platyrrhines include the smallest of the monkeys, the marmosets and tamarins (Figure 5.29), 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.

Figure 5.29: Clockwise from top right: golden-headed lion tamarin, pygmy marmoset, Goeldi’s monkey, bare-eared marmoset, emperor tamarin, and common marmoset. Credit: Callitrichinae genus by Miguelrangeljr is a collective work under a CC BY-SA 3.0 License. [Includes Weißbüschelaffe_(Callithrix_jacchus) by Raymond, CC BY-SA 4.0; Leontopithecus chrysomelas (portrait) by Hans Hillewaert, CC BY-SA 4.0; Emperor_Tamarin_portrait_2_edit1 by Brocken Inaglory, CC BY-SA 4.0; Dværgsilkeabe_Callithrix_pygmaea by Malene Thyssen (User Malene), GNU Free Documentation License; Mico_argentatus_(portrait) by Hans Hillewaert, CC BY-SA 4.0; Titi Monkey by Jeff Kubina, CC BY-SA 2.0].]

The largest platyrrhines are a family that include spider monkeys, woolly spider monkeys, woolly monkeys, and howler monkeys (Figure 5.30). 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 5.13). 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.

Figure 5.30: Clockwise from top right: howler monkey, woolly monkey, woolly spider monkey, and spider monkey. Credit: Atelidae Family by Miguelrangeljr is a collective work under a CC BY-SA 3.0 License. [Includes Ateles marginatus (Sao Paulo zoo) by Miguelrangeljr, CC BY-SA 3.0; Alouatta caraya male by Miguelrangeljr, CC BY-SA 3.0; Lagothrix lagotricha (walking) by Hans Hillewaert, CC BY-SA 3.0; Brachyteles hypoxanthus2 by Paulo B. Chaves, CC BY 2.0.]

There are many other monkeys in Central and South America, including the gregarious capuchins (see Figure 5.28) 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 and Sampaio 2015). Figure 5.31 summarizes the key traits of platyrrhines relative to the other infraorders of Haplorrhini.

Platyrrhini traits

1. Flat nose with rounded nostrils pointing to the side
2. Highly arboreal
3. Less sexually dimorphic on average
4. 2:1:3:3 dental formula*
5. Polymorphic color vision*

Figure 5.31: 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.

Infraorder Catarrhini of Asia and Africa

Figure 5.32: A Wolf’s guenon demonstrating a typical catarrhine nose with teardrop-shaped nostrils close together and pointed downward. Credit: Wolf’s Guenon Picking Up Food (19095137693) by Eric Kilby is under a CC BY-SA 2.0 License.

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 5.32) and one fewer premolar than most other primates, giving us a dental formula of 2:1:2:3 (Figure 5.33). 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 coloration 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.

Figure 5.33: Catarrhines have two premolars whereas most other primate taxa (including platyrrhini) have three premolars. This image also shows one of the derived traits of cercopithecoids, their bilophodont molars, which differ from the more ancestral Y-5 molars of apes and humans. Credit: Platyrrhini vs. Catarrhini dentition 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 Cebus apella (brown capuchin) at Animal Diversity Web by Phil Myers, CC BY-NC-SA 3.0; Lophocebus albigena (gray-cheeked mangaby) at Animal Diversity Web by Phil Myers, CC BY-NC-SA 3.0; Symphalangus syndactylus (siamang) at Animal Diversity Web by Phil Myers, CC BY-NC-SA 3.0.]

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 Chapter 8).

Superfamily Cercopithecoidea of Africa and Asia

Figure 5.34: The second derived trait of cercopithecoids are their ischial callosities, shown here on a crested black macaque. Credit: Sulawesi trsr DSCN0572 v1 by T. R. Shankar Ramanis is under a CC BY-SA 3.0 License.

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 5.33, 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 5.34). 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.

Figure 5.35: Geographic distribution of the cercopithecoid monkeys. Catarrhines have the widest geographic distribution due to the success of cercopithecoids who are found all across subsaharan Africa and southern Asia. Credit: Superfamily Cercopithecoidea map (Figure 5.33) original to Explorations: An Open Invitation to Biological Anthropology by Elyssa Ebding at GeoPlace, California State University, Chico is under a CC BY-NC 4.0 License.

Cercopithecoid monkeys are the most geographically widespread group of nonhuman primates (Figure 5.35). 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.

Figure 5.36: Silver leaf monkey infants are born with orange fur, dramatically contrasting the adult coat color of their mothers. After a few months, the infants gradually change color to that of their parents. Credit: Silverleaf Monkey (Kuala Lumpur) by Andrea Lai from Auckland, New Zealand, is under a CC BY 2.0 License.

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 color from their parents (Figure 5.36). Leaf monkeys are also known for having odd noses (Figure 5.37), and so they are sometimes called “odd-nosed monkeys.” Cheek-pouch monkeys are able to pack food into their cheek pouches (Figure 5.38), thus allowing them to move to a location safe from predators or aggressive individuals of their own species where they can eat in peace.

Figure 5.37: Proboscis monkeys are one of several “odd-nosed” leaf monkeys. Male proboscis monkeys, like this one, have large, pendulous noses, while females have much smaller noses. Credit: Proboscis monkey (Nasalis larvatus) male head by Charles J Sharp creator QS:P170,Q54800218 is under a CC BY-SA 4.0 License.

Figure 5.38: This bonnet macaque has filled its cheek pouches with food, an adaptation that is useful in transporting food to a safer location to eat. Credit: Bonnet macaque DSC 0893 by T. R. Shankar Raman is under a CC BY-SA 4.0 License.

Superfamily Hominoidea of Africa and Asia

Figure 5.39: Geographic distribution of apes across Central and West Africa and Southeast Asia. Hominoids overlap geographically with cercopithecoid monkeys but have a lower tolerance for seasonal environments and so are found only in tropical forests across these regions. Credit: Superfamily Hominoidea map (Figure 5.38) original to Explorations: An Open Invitation to Biological Anthropology by Elyssa Ebding at GeoPlace, California State University, Chico is under a CC BY-NC 4.0 License.

Superfamily Hominoidea of Africa and Asia (Figure 5.39) 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 5.33). 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 5.40).

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 5.12). 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 5.40: 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 behavior and life history characteristics. Hominoids all seem to show some degree of female dispersal at sexual maturity but, as you will learn in Chapter 6, 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 5.41 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.

Infraorder Catarrhini

1. Downard facing, tear-drop shaped nostrils, close together
2. Arboreal and more terrestrial taxa
3. On average, largest primates
4. On average, most sexually dimorphic taxonomic group
5. 2:1:2:3
6. All trichromatic

Figure 5.41a: 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.]

Figure 5.41b: 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

Figure 5.42: Siamangs are the largest of the Hylobatidae family. They are all black with a throat sac that can become inflated to give out loud calls. Credit: Shout (373310729) by su neko is under a CC BY-SA 2.0 License.

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 coloration and markings, while siamangs are all black with big throat sacs that are used in their exuberant vocalizations (Figure 5.42). Both gibbons and siamangs live in pairs with very little sexual dimorphism, although males and females do differ in coloration 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 5.43 a and 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, and 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).

Figure 5.43: (a) A female orangutan eating fruit with her infant nearby and (b) a flanged adult male eating leaves. Male orangutans are about twice the size of females and have a longer coat length, cheek flanges, and throat sac. Credit: a. Orang Utan (Pongo pygmaeus) female with baby (8066259067) by Bernard DUPONT is under a CC BY-SA 2.0 Licence. b. Orangutan -Zoologischer Garten Berlin-8a by David Forsman is under a CC BY 2.0 License.

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 (Figure 5.44a and 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 gray. 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).

Figure 5.44: (a) A female gorilla with her two offspring and (b) a silverback adult male. Male gorillas are about twice the size of females. They also differ from females in having a large sagittal crest and a silver back, which appears as they mature. Credit: a. Enzo naomi echo by Zoostar is under a CC BY 3.0 License. b. Male gorilla in SF zoo by Brocken Inaglory is under a CC BY-SA 3.0 License.

Pan of Africa

Figure 5.45: Bonobo (Pan paniscus). You can see the distinctive hair-part on this bonobo. Credit: Bonobo male Jasongo 15yo Twycross 582a (2014 11 14 01 04 18 UTC) by William H. Calvin is under a CC BY-SA 4.0 License.

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 5.45). In contrast, chimpanzees do not have the distinctive parted hair and are born with light faces that darken as they mature (Figure 5.46). 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.

Figure 5.46: A common chimpanzee (Pan troglodytes) female (center) and her offspring. Note the pink face of the youngest individual. Bonobos are born with dark-skinned faces, but chimpanzees are born with pink faces that darken with age. Credit: Chimpanzees in Uganda (5984913059) by USAID Africa Bureau uploaded by Elitre is in the public domain.

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, behavior, 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, and Strait 2001). Further, humans, chimpanzees, and bonobos all live in fission-fusion social groups characterized by shared behaviors, like male cooperation in hunting and territoriality, as well as tool use.

Special Topic: Primates in Culture and Religion

One of the best parts of teaching anthropology for me is getting to spend time watching primates at zoos. What I also find interesting is watching people watch primates. I have very often heard a parent and child walk up to a chimpanzee enclosure and exclaim “Look at the monkeys!” The parent and child often don’t know that a chimpanzee is not a monkey, nor are they likely to know that chimpanzees share more than 98% of their DNA with us. What strikes me as significant is that, although most people do not know the difference between a monkey, an ape, and a lemur, they nonetheless recognize something in the animals as being similar to themselves. In fact, recognition of similarities between humans and other primates is very ancient, dating back far earlier than Linnaeus. For many of us, we only ever get to see primates in zoos and animal parks, but in many areas of the world, humans have coexisted with these animals for thousands of years. In areas where humans and primates have a long, shared history, nonhuman primates often play key roles in creation myths and cultural symbolism.

Hamadryas baboons feature significantly in Ancient Egyptian iconography. Ancient Egyptian deities and beliefs transformed over time, as did the role of hamadryas baboons. Early on, baboons were thought to represent dead ancestors, and one monkey deity, called Babi or Baba, was thought to feed off of dead souls. Later, baboons became the totem animal for Thoth, the deity of science, writing, wisdom, and measurement, who also wrote the Book of the Dead. Sunbathing hamadryas baboons led ancient Egyptians to associate them with Ra, the sun god, who was the son of Thoth. During mummification, human organs were removed and put into canopic jars, one of which was topped with the head of the baboon-headed god, Hapi. Hamadryas baboons were also often kept as pets, as depicted in hieroglyphics, and occasionally mummified as well.

On Madagascar, indris and aye-ayes play roles in the creation myths and omens of local people.There are many myths regarding the origins of indris and their relationship to humans, including one where two brothers living in the forest separated, with one brother leaving the forest and becoming a human while the other stayed in the forest to become the indri. Like humans, indris have long legs, no tail, and upright posture. They are considered sacred and are therefore protected. Unfortunately, the aye-aye is not treated with the same reverence. Because of their unusual appearance (see Figure 5.15), aye-ayes are seen as omens of death.They are usually killed when encountered because it is believed that someone will die if an aye-aye points at them.

In India, monkeys play a key role in the Hindu religion. Hanuman, who resembles a monkey, is a key figure in the Ramayana. Hanuman is thought to be a guardian deity, and so local monkeys like Hanuman langurs and macaques are protected in India (Figure 5.47). In Thailand, where Hinduism is also practiced, the Hindu reverence for monkeys extends to “monkey feasts,” where large quantities of food are spread out in gratitude to the monkeys for bringing good fortune.

Figure 5.47: Because of important monkey-like figures in the Hindu religion, macaques are protected in India and often live near temples where they are fed by local peoples. Credit: Macaque India 4 by Thomas Schoch (Mosmas) is under a CC BY-SA 3.0 License.

The people of Japan have coexisted with Japanese macaques for thousands of years, and so monkeys play key roles in both of the major Japanese religions. In the Shinto religion, macaques are thought of as messengers between the spirit world and humans, and monkey symbols are thought to be good luck. The other major religion in Japan is Buddhism, and monkeys play a role in symbolism of this religion as well. The “Three Wise Monkeys” who see no evil, speak no evil, and hear no evil derive from Buddhist iconography of monkeys.

In Central and South America, monkeys feature often in Mayan and Aztec stories. In the Mayan creation story, the Popol Vuh, the “hero brothers,” are actually a howler monkey and a spider monkey, who represent ancestors of humans in the story. In the Aztec religion, spider monkeys are associated with the god of arts, pleasure, and playfulness. A spider monkey is also represented in a Peruvian Nazca geoglyph, a large design made on the ground by moving rocks.

In many of these regions today, the relationships between humans and nonhuman primates are complicated. The bushmeat and pet trades make these animals valuable at the expense of many animals’ lives, and in some areas, nonhuman primates have become pests who raid crop fields and consume valuable foods. All of this has led to the development of a new subarea of anthropology called Ethnoprimatology, which involves studying the political, economic, symbolic, and practical relationships between humans and nonhuman primates.This field highlights the particular challenges for humans of having to coexist with animals with whom we share so much in common. It also provides insight into some of the challenges facing primate conservation efforts (see Appendix B: Primate Conservation).