Meet the Living Primates - Explorations: An Open Invitation to Biological Anthropology PDF

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Home Read Sign in Search in book … Want to create or adapt books like this? Learn more about how Pressbooks supports open publishing practices. CONTENTS EXPLORATIONS: AN OPEN INVITATION TO BIOLOGICAL ANTHROPOLOGY, 2ND EDITION 5. Meet the Living Primates Stephanie Etting, Ph.D., Sacramento City College This chapter is a revision from “Chapter 5: Meet the Living Primates” by Stephanie Etting. In Explorations: An Open Invitation to Biological Anthropology, first edition, edited by Beth Shook, Katie Nelson, Kelsie Aguilera, and Lara Braff, which is licensed under CC BY-NC 4.0. Learning Objectives Previous: Forces of Evolution Next: Primate Ecology and Behavior Describe how studying nonhuman primates is important in anthropology. Compare two ways of categorizing taxa: grades and clades. Define different types of traits used to evaluate primate taxa. Identify key ways that primates differ from other mammals. Distinguish between the major primate taxa using their key characteristics. Describe your place in nature by learning your taxonomic classification. You may be wondering why a field dedicated to the study of humans includes discussions of nonhuman animals. Our primary goal in biological anthropology is to understand how humans are similar to and different from the rest of the natural world, why we have the traits we have, and how we got to be the way we are. But to fully grasp our place in nature, we must look to our closest living relatives, the nonhuman primates. In this chapter, we focus on the organization and diversity within the Order Primates. Studying Primates in Biological Anthropology Primates are one of at least twenty Orders belonging to the Class Mammalia, and probably one of the oldest. One genetic estimate puts the origin of primates at approximately 91 million years ago (mya), predating the extinction of the dinosaurs (Bininda-Emonds et al. 2007). Today, the Order Primates is a diverse group of animals that includes lemurs and lorises, tarsiers, monkeys, apes, and humans, all of which are united in sharing a suite of anatomical, behavioral, and life history characteristics. While nonhuman primates are fascinating animals in their own right, their close relationship to humans makes them ideal for studying humans via homology, looking at traits that are shared between taxa because they inherited the trait from a common ancestor. For example, humans (genus Homo) and chimpanzees (genus Pan) both share the trait of male cooperation in hunting. This trait—along with many others that chimpanzees and humans share—is likely homologous, meaning it was probably passed down from the last common ancestor of Homo and Pan, which lived about 6–8 million years ago. Nonhuman primates also make excellent comparators for learning about humans via analogy. Many nonhuman primates live in environments similar to those in which our ancestors lived and therefore exhibit traits similar to what we see in humans. For example, baboons and humans both have long legs. In humans, this is because about 1.7 million years ago, our ancestors moved into savanna habitats where longer legs helped them move more efficiently over long distances. Baboons, who also live in savanna habitats, independently evolved longer arms and legs for the same reason—to be able to cover more ground, more efficiently. This means that having long legs is an analogous trait in baboons and humans: —that is, this adaptation evolved independently in the two species but for the same purpose. Using homology and analogy, our closest living relatives provide the critical context in which to understand human biology, morphology, and behavior. It is only by studying how humans compare with our primate relatives that we can fully comprehend our place in nature. Ways of Organizing Taxa You learned in Chapter 2 about Linnaeus and the hierarchical nature of taxonomic classification. Our goal in classifying taxa is to create categories that reflect clade relationships. A clade is a grouping of organisms based on relatedness that reflects a branch of the evolutionary tree. Clade relationships are determined using traits shared by groups of taxa as well as genetic similarities. An example of a clade would be a grouping that includes humans, chimpanzees, bonobos, and gorillas (Figure 5.1). These taxa are in what is referred to as the African clade of hominoids (a taxonomic group you will learn about later in this chapter). The African clade grouping reflects how humans, chimpanzees, bonobos, and gorillas all share a more recent ancestor with each other than any of them do with other species—that is, we are on the same branch of the evolutionary tree. We know members of the African clade are most closely related based on shared morphological traits as well as genetic similarities. Excluded from this grouping is the orangutan, which is considered a member of the Asian clade of hominoids. Figure 5.1: Grades vs. Clades. A grade grouping of apes places orangutans, gorillas, chimpanzees, and bonobos together based on their similar appearance and lifestyle, but excludes humans. Clade classification is based on shared derived traits and genetic evidence (both reflecting close evolutionary relationships). A clade grouping of apes places humans with gorillas, chimpanzees, and bonobos., whereas orangutans are separated. Credit: Grades vs. clades comparison (Figure 5.12) 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 Orangutan on a tree (Unsplash) by Dawn Armfield, public domain (CC0 1.0); Gorilla Profile (17997840570) by Charlie Marshall from Bristol UK, modified (cropped), CC BY 2.0 License; Chimpanzee (14679767561) by Magnus Johansson, modified (cropped), CC BY-SA 2.0; Pointing finger (1922074) by truthseeker08, Pixabay License.] In contrast, grades are groupings that reflect levels of adaptation or overall similarity and not necessarily evolutionary relationships. An example of a grade would be placing orangutans, gorillas, bonobos, and chimpanzees into a group, and excluding humans. Grouping in this way is based on the superficial similarities of the apes in being large-bodied, having lots of body hair, living in tropical forests, climbing and sleeping in trees, and so on. According to these criteria, humans seem to be unusual in that we differ in our morphology, behavior, and ecology. Separating humans from the large-bodied apes is the system that was used historically. We now know that grouping orangutans, gorillas, bonobos, and chimpanzees and excluding humans does not accurately reflect our true evolutionary relationships. Since our goal in taxonomic classification is to organize animals to reflect their evolutionary relationships, we prefer to use clade classifications. Types of Traits When evaluating relationships between taxa, we use key traits that allow us to determine which species are most closely related to one another. Traits can be either ancestral or derived. Ancestral traits are those that a taxon has because it has inherited the trait from a distant ancestor. For example, all primates have body hair because we are mammals and all mammals share an ancestor hundreds of millions of years ago that had body hair. This trait has been passed down to all mammals from a shared ancestor, so all mammals alive today have body hair. Derived traits are those that have been more recently altered. This type of trait is most useful when we are trying to distinguish one group from another because derived traits tell us which taxa are more closely related to each other. For example, humans walk on two legs.The many adaptations that humans possess that allow us to move in this way evolved after humans split from the Genus Pan. This means that when we find fossil taxa that share derived traits for walking on two legs, we can conclude that they are likely more closely related to humans than to chimpanzees and bonobos. There are a couple of other important points about ancestral and derived traits that will become apparent as we discuss primate diversity. First, the terms ancestral and derived are relative terms, meaning that a trait can be either one depending on the taxa being compared. For example, in the previous paragraph, body hair was used as an example for an ancestral trait among primates. All mammals have body hair because we share a distant ancestor who had this trait. The presence of body hair therefore doesn’t allow you to distinguish whether monkeys are more closely related to apes or lemurs because they all share this trait. However, if we are comparing mammals to birds and fish, then body hair becomes a derived trait of mammals. It evolved after mammals diverged from birds and fish, and it tells us that all mammals are more closely related to each other than they are to birds or fish.The second important point is that very often when one lineage splits into two, one taxon will stay more similar to the last common ancestor in retaining more ancestral traits, whereas the other lineage will usually become more different from the last common ancestor by developing more derived traits. This will become very apparent when we discuss the two suborders of primates, Strepsirrhini and Haplorrhini. When these two lineages diverged, strepsirrhines retained more ancestral traits (those present in the earliest primates) and haplorrhines developed more derived traits (became more different from ancestral primates). There are two other types of traits that will be relevant to our discussions here: generalized and specialized traits. Generalized traits are those characteristics that are useful for a wide range of things. Having opposable thumbs that go in a different direction than the rest of your fingers is a very useful, generalized trait. You can hold a pen, grab a branch, peel a banana, or text your friends all thanks to your opposable thumbs! Specialized traits are those that have been modified for a specific purpose. These traits may not have a wide range of uses, but they will be very efficient at their job. Hooves in horses are a good example of a specialized trait: they allow horses to run quickly on the ground on all fours. You can think of generalized traits as a Swiss Army knife, useful for a wide range of tasks but not particularly good at any one of them. That is, if you’re in a bind, then a Swiss Army knife can be very useful to cut a rope or fix a loose screw, but if you were going to build furniture or fix a kitchen sink, then you’d want specialized tools for the job. As we will see, most primate traits tend to be generalized. What Makes Something a Primate? The Order Primates is distinguished from other groups of mammals in having a suite of characteristics. This means that there is no individual trait that you can use to instantly identify an animal as a primate; instead, you have to look for animals that possess a collection of traits. What this also means is that each individual trait we discuss may be found in nonprimates, but if you see an animal that has most or all of these traits, there is a good chance it is a primate. Primates are most distinguishable from other organisms in traits related to our vision. Our Order relies on vision as a primary sense, which is reflected in many areas of our anatomy and behavior. All primates have eyes that face forward with convergent (overlapping) visual fields. So if you cover one eye with your hand, you can still see most of the room with your other one. This also means that we cannot see on the sides or behind us as well as some other animals can. In order to protect the sides of the eyes from the muscles we use for chewing, all primates have at least a postorbital bar, a bony ring around the outside of the eye (Figure 5.2). Primate taxa with more convergent eyes need extra protection, so animals with greater orbital convergence will have a postorbital plate or postorbital closure in addition to the bar (Figure 5.2).The postorbital bar is a derived trait of primates, appearing in our earliest ancestors. Figure 5.2: All primates have bony protection around their eyes. Some have a postorbital bar only (right), but many have full postorbital closure, also called a postorbital plate, that completely protects the back of the eye socket (left). Credit: Postorbital bar/Postorbital closure (Figure 5.1) a derivative work original to Explorations: An Open Invitation to Biological Anthropology by Stephanie Etting is under a CC BY-NC-SA 4.0 License. [Includes Otolemur crassicaudatus (greater galago) by Animal Diversity Web, CC BY-NC-SA 3.0; Macaca fascicularis (long-tailed macaque) by Animal Diversity Web, CC BY-NC-SA 3.0.] Another distinctive trait of our Order is that many primates have trichromatic color vision, the ability to distinguish reds and yellows in addition to blues and greens. Birds, fish, and reptiles are tetrachromatic (they can see reds, yellows, blues, greens, and even ultraviolet), but most mammals, including some primates, are only dichromatic (they see only in blues and greens). It is thought that the nocturnal ancestors of mammals benefited from seeing better at night rather than in color, and so dichromacy is the ancestral condition for mammals. Trichromatic primates are known to use their color vision for all sorts of purposes: finding young leaves and ripe fruits, identifying other species, and evaluating signals of health and fertility. The primate visual system uses a lot of energy, so primates have compensated by cutting back on other sensory systems, particularly our sense of smell. Compared to other mammals, primates have reduced snouts, another derived trait that appears even in the earliest primate ancestors. There is variation across primate taxa in how much snouts are reduced. Those with a better sense of smell usually have poorer vision than those with a relatively dull sense of smell. The reason for this is that all organisms have a limited amount of energy to spend on running our bodies, so we make evolutionary trade-offs, as energy spent on one trait cuts back on energy spent on another. So primates with better vision are spending more energy on vision and thus have a poorer smell (and shorter snout), and those who spend less energy on vision will have a better sense of smell (and a longer snout). Primates also differ from other mammals in the size and complexity of our brains. On average, primates have brains that are twice as big for their body size when compared to other mammals. Not unexpectedly, the visual centers of the brain are larger in primates and the wiring is different from that in other animals, reflecting our reliance on this sense. The neocortex, which is used for higher functions like consciousness and language in humans, as well as sensory perception and spatial awareness, is also larger in primates relative to other animals. In nonprimates this part of the brain is often smooth, but in primates it is made up of many folds, which increase the surface area. It has been proposed that the more complex neocortex of primates is related to diet, with fruit-eating primates having larger relative brain sizes than leaf-eating primates, due to the more challenging cognitive demands required to find and process fruits (Clutton-Brock and Harvey 1980). An alternative hypothesis argues that larger brain size is necessary for navigating the complexities of primate social life, with larger brains occurring in species who live in bigger, more complex groups relative to those living in pairs or solitarily (Dunbar 1998). There seems to be support for both hypotheses, as large brains are a benefit under both sets of selective pressures. Animals with large brains usually have extended life history patterns, and primates are no exception. Life history refers to the pace at which an organism grows, reproduces, and ages. Some animals grow very quickly and reproduce many offspring in a short time frame but do not live very long. Other animals grow slowly, reproduce few offspring, reproduce infrequently, and live a long time. Primates are all in the “slow lane” of life history patterns. Compared to animals of similar body size, primates grow and develop more slowly, have fewer offspring per pregnancy, reproduce less often, and live longer. Primates also invest heavily in each offspring. With a few exceptions, most primates only have one offspring at a time. A group of small-bodied monkeys in South America regularly give birth to twins, and some lemurs can give birth to multiple offspring at a time, but these primates are the exception rather than the rule. Primates also reproduce relatively infrequently. The fastest-reproducing primates will produce offspring about every six months, while the slowest, the orangutan, reproduces only once every seven to nine years. This very slow reproductive rate makes the orangutan the slowest-reproducing animal on the planet! Primates are also characterized by having long lifespans. The group that includes humans and large- bodied apes has the most extended life history patterns among all primates, with some large-bodied apes estimated to live up to 58 years in the wild (Robson et al. 2006). Primates also differ from other animals in our hands and feet. The Order Primates is a largely arboreal taxonomic group, meaning that most primates spend a significant amount of their time in trees. As a result, the hands and feet of primates have evolved to move in a three-dimensional environment. Primates have the generalized trait of pentadactyly— possessing five digits (fingers and toes) on each limb. Many nonprimates, like dogs and horses, have fewer digits because they are specialized for high-speed, terrestrial (on the ground) running. Pentadactyly is also an ancestral trait, one that dates back to the earliest four-footed animals. Primates today have opposable thumbs and, with the exception of humans, opposable big toes (Figure 5.3). Opposable thumbs and toes are a derived trait that appeared in the earliest primate fossils about 55 million years ago. Having thumbs and big toes that go in a different direction from the rest of the fingers and toes allow primates to be excellent climbers in trees as well as to manipulate objects. Our ability to manipulate objects is further enhanced by the flattened nails on the backs of our fingers and toes that we possess in Figure 5.3: These drawings of the hands and feet of the place of the claws and hooves that many other different primates show the opposable thumbs and big toes, pentadactyly, flattened nails, and tactile pads mammals have. On the other side of our digits, we characteristic of our Order. Credit: PrimateFeet by have sensitive tactile pads that allow us to have a Richard Lydekker, original from The Royal Natural fine sense of touch. Primates use this fine sense of History 1:15 (1893), is in the public domain. touch for handling food and, in many species, grooming themselves and others. In primates, grooming is an important social currency, through which individuals forge and maintain social bonds. Lastly, primates are very social animals. All primates, even those that search for food alone, establish strong social networks within species. Unlike many animals, primates do not migrate: they stay in a relatively stable area for their whole life, often interacting with the same individuals for their long lives. The long-term relationships that primates form with others of their species lead to complex and fascinating social behaviors (see Chapter 6). Finally, nonhuman primates show a clear preference for tropical regions of the world. Most primates are found between the Tropic of Cancer and the Tropic of Capricorn, with only a few taxa living outside these regions. Figure 5.4 shows a summary of primate traits. Primate suite of traits Convergent eyes Postorbital bar Many have trichromatic color vision Short snouts Opposable thumbs and big toes Pentadactyly Lattened nails Tactile pads Highly arboreal Large brains Extended life histories Live in tropics Figure 5.4: Primate Traits at a Glance: This list summarizes the suite of traits that differentiate primates from other mammals. Credit: Primate at a glance table (Figure 5.3) by Stephanie Etting original to Explorations: An Open Invitation to Biological Anthropology is under a CC BY-NC 4.0 License. Key Traits Used to Distinguish Between Primate Taxa When placing primate species into specific taxonomic groups, we focus on dental characteristics, behavioral adaptations, and locomotor adaptations. Differences in these characteristics across groups reflect constraints of evolutionary history as well as variation in adaptations. Dental Characteristics Teeth may not seem like the most exciting topic with which to start, but we can learn a tremendous amount about an organism from its teeth. First, teeth are vital to survival. Wild animals do not have the benefit of knives and forks; they rely on their teeth to process their food. Because of this, teeth of any species have evolved to reflect what that organism eats and therefore have a lot to tell us about their diet. Second, variation in tooth size, shape, and number reveals an organism’s evolutionary history. Some taxa have more teeth than others or different forms of teeth. Furthermore, differences in teeth between males and females can tell us about competition over mates (see Chapter 6). Lastly, teeth are overly represented in the fossil record. Enamel is hard, and there is little meat on jaws so carnivores and scavengers often leave them behind. Sometimes, the only remains we have from an extinct taxon is its teeth! Like other mammals, primates are heterodont: they have multiple types of teeth that are used for different purposes. We have incisors for slicing; premolars and molars for grinding up our food; and canines, which most primates (not humans) use as weapons against predators and each other. The sizes of canines vary across species and can often be sexually dimorphic, with males tending to have larger canines than females. Some nonhuman primates hone, or sharpen, their canines by gnashing the teeth together to sharpen the sides. The upper canine Figure 5.5: This picture of an open-mouthed Hamadryas baboon demonstrates the diastema sharpens on the first lower premolar and the lower canine between his upper canine and front teeth. This sharpens on the front of the upper canine. As canines get space is taken up by his lower canine when he larger, they require a space to fit in order for the jaws to closes his mouth. Credit: Ha,ha,ha …. close. This space between the teeth is called a diastema (14986571843) by Rolf Dietrich Brecher from (Figure 5.5). Germany is under a CC BY-SA 2.0 License. We use a dental formula to specify how many incisors, canines, premolars, and molars are in each quadrant of the mouth (half of the top or bottom). For example, Figure 5.6 shows half of the lower teeth of a human. You can see that in half of the mandible, there are two incisors, one canine, two premolars, and three molars. This dental formula is written as 2:1:2:3. (The first number represents the number of incisors, followed by the number of canines, premolars, and molars). To determine the dental formula, you need to be able to identify the different types of teeth. You can recognize incisors because they often look like spatulas with a flat, blade-like surface. Premolars and molars can be differentiated by the number of cusps that they have. Cusps are the bumps that you can feel with your tongue on the surface of your back teeth. Premolars are smaller than molars and, in primates, often have one or two cusps on them. Molars are bigger, providing a larger chewing surface, and have more cusps. Depending on the species and whether you’re looking at upper or lower teeth, primate molars can have between three and five cusps. Molar cusps can also vary between taxa in how they are arranged; you will learn more about this later in this chapter. Canines are often easy to distinguish because, in most taxa, they are much longer and more conical than the other teeth. Teeth also directly reflect an organism’s diet. Primates are known to eat a wide range of plant parts, insects, gums, and, rarely, meat. While all Figure 5.6: This drawing shows primates eat a variety of foods, what differs among primates are the half of the human mandible. With proportions of each of these food items in the diet. That is, two primates the four types of teeth labeled, living in the same forest may be eating the same foods but in vastly you can determine that the different proportions, and so we would categorize them as different dental formula is 2:1:2:3. Credit: dietary types. The most common dietary types among primates are Gray997 by Henry Vandyke Carter, original in Henry Gray those whose diets consist primarily of fruit (frugivores), those who eat (1918) Anatomy of the Human mostly insects (insectivores), and those who eat primarily leaves Body, Plate 997, is in the public (folivores). A few primate taxa are gummivores, specializing in eating domain. gums and saps, but we will only focus on the adaptations found in the three primary dietary groups. Frugivores Plants want animals to eat their fruits because, in doing so, animals eat the seeds of the fruit and then disperse them far away from the parent plant. Therefore, plants often “advertise” fruits by making them colorful and easy to spot, full of easy-to-digest sugars that make them taste good and, often, easy to chew and digest (not being too fibrous or tough). For these reasons, frugivores often do not need a lot of specialized traits to consume a diet rich in fruits (Figure 5.7). Their molars usually have a broad chewing surface with low, rounded cusps (referred to as bunodont molars). Frugivores have large incisors for slicing through the outer coatings on fruit, and they tend to have stomachs, colons, and small intestines that are intermediate in terms of size and complexity between insectivores and folivores (Chivers and Hladik 1980). They are also usually of intermediate body size between the other two dietary types. Because fruit does not contain protein, frugivores must supplement their diet with protein from insects, leaves, and/or seeds. Frugivores who get protein by eating seeds evolved to have thicker enamel on their teeth to protect them from excessive wear. Figure 5.7: Frugivores are characterized by large incisors, bunodont molars, and digestive tracts that are intermediate in complexity between the other two dietary types. Credit: Papio papio (Guinea baboon).jpg by Phil Myers on Animal Diversity Web is under a CC BY- NC-SA 3.0 License. Insectivores While insects can be difficult to find and catch, they are easy to chew and digest. As a result, insectivorous primates usually have small molars with pointed cusps to puncture the exoskeleton of the insects (Figure 5.8), and they have simple stomachs and colons with a long small intestine to process the insects. Nutritionally, insects provide a lot of protein and fat but are not plentiful enough in the environment to support large-bodied animals, so insectivores are usually the smallest of the primates. Figure 5.8: Insectivores need sharp, pointed molar cusps to break through the exoskeletons of insects. Insects are easy to digest, so these primates have simple digestive tracts. Credit: Tarsier (an insectivor)’s teeth original to Explorations: An Open Invitation to Biological Anthropology (2nd ed.) by Stephanie Etting is a collective work under a CC BY-NC-SA 3.0 License. [Includes Lower_lateral1942 by Phil Myers on Animal Diversity Web, CC BY-NC-SA 3.0; Ventral by Phil Myers on Animal Diversity Web, CC BY- NC-SA 3.0.] Folivores Plants rely on leaves to get energy from the sun, so plants do not want animals to eat their leaves (unlike their fruit). As a result, plants evolved to try to discourage animals from eating their leaves. Leaves often carry toxins, taste bitter, are very fibrous and difficult to chew, and are made of large cellulose molecules that are difficult to break down into usable sugars. Thus, animals who eat leaves need a lot of specialized traits (Figure 5.9). Folivorous primates have broad molars with high, sharp cusps connected by shearing crests. These molar traits allow folivores to physically break down fibrous leaves when chewing. Folivores then chemically break down cellulose molecules into usable energy. To do this, some folivores have complex stomachs with multiple compartments, while others have large, long intestines and special gut bacteria that can break up cellulose. Folivores are usually the largest bodied of all primates, and they tend to spend a large portion of their day digesting their food, so they are less active than frugivores or insectivores. Figure 5.9: To derive energy from leaves, folivores, like this Trachypithecus (dusky leaf monkey), have smaller incisors and high sharp molar cusps connected by shearing crests. Credit: Trachypithecus obscurus (dusky leaf monkey) upper teeth by Phil Myers on Animal Diversity Web has been modified (background removed, labels added by Stephanie Etting) is under a CC BY-NC- SA 3.0 License. Behavioral Adaptations Since Chapter 6 is dedicated to primate behavior, we will only briefly discuss variations in activity patterns, social grouping, and habitat use. Primate groups differ in activity patterns: whether they are active during the day (diurnal), at night (nocturnal), or through the 24-hour period (cathemeral). Primate taxa vary in social groupings: some are primarily solitary, others live in pairs, and still others live in groups of varying sizes and compositions. Lastly, some taxa are primarily arboreal while others are more terrestrial. Locomotor Adaptations Finally, primate groups vary in their adaptations for different forms of locomotion, or how they move around. Living primates are known to move by vertical clinging and leaping, quadrupedalism, brachiation, and bipedalism. Vertical clinging and leaping is when an animal grasps a vertical branch with its body upright, pushes off with long hind legs, and then lands on another vertical support branch (Figure 5.10a). Animals who move in this way usually have longer legs than arms, long fingers and toes, and smaller bodies. Vertical clinger leapers also tend to have elongated ankle bones, which serve as a lever to help them push off with their legs and leap to another branch (Figure 5.10b). Figure 5.10: Vertical clingers and leapers have longer legs than arms, long lower backs, and long fingers and toes. They also have elongated ankle bones to help them push off when leaping. Credit: a. Propithecus vertical clinging and leaping by Terpsichores is under a CC BY-SA 3.0 License. b. Tarsier skeleton by Emőke Dénes has been modified (background removed) by Stephanie Etting and is under a CC BY-SA 4.0 License. Original Spectral tarsier (Tarsius tarsier) skeleton at the Cambridge University Museum of Zoology, England.) 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 5.11a) usually have shorter arms and legs and longer tails, while terrestrial quadrupeds (Figure 5.11b) have longer arms and legs and, often, shorter tails. These differences relate to the lower center 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. Figure 5.11: Two examples of quadrupedal primates. The capuchin monkey skeleton on the left (a) is a typical arboreal quadruped with shorter arms and legs, longer fingers and toes, and a long tail. The baboon skeleton on the right (b) is a terrestrial quadruped with relatively long arms and legs, shorter fingers and toes, and a short tail. Credit: a. Capuchin monkey skeleton by Henri-Marie Ducrotay de Blainville is in the public domain. b. Baboon by Henri-Marie Ducrotay de Blainville is in the public domain. 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 5.12a). 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 5.12b). 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 5.13). The underside of the tail has a tactile pad, resembling your fingerprints, for better grip. Figure 5.12: a. Example of brachiation. b. Skeleton of a typical brachiator, showing longer arms than legs, short back, and lack of a tail. Credit: a. Brachiator (Figure 5.9b) original to Explorations: An Open Invitation to Biological Anthropology by Mary Nelson is under a CC BY-NC 4.0 License. b. Skeleton of Gibbon (Giboia) by Joxerra Aihartza is under a Free Art License. Figure 5.13. Spider monkeys are considered semi-brachiators, as they can swing below branches but use their tails as a third limb. On the ground they move via quadrupedal locomotion. Credit: Ateles-fusciceps 54724770b by LeaMaimone is under a CC BY 2.5 License. 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 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. 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 Figure 5.16: The foot of a ring- and predators. While strepsirrhines have a better sense of smell than tailed lemur showing its haplorrhines, their visual adaptations are more ancestral. Strepsirrhines grooming claw on the second have less convergent eyes than haplorrhines and therefore all have digit. Credit: Lemur catta toilet postorbital bars, whereas haplorrhines have full postorbital closure (see claw by Alex Dunkel (Maky) is under a CC BY 3.0 License. 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. 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 Figure 5.17: The lower front teeth of a lorises, pottos, and galagos of Africa and Asia. By molecular ring-tailed lemur showing the six teeth of the tooth comb: four incisors and two estimates, these two groups split about 65 million years ago canines. The teeth that superficially look (Pozzi et al. 2014). like canines are premolars. Credit: Lemur catta toothcomb by Alex Dunkel (Maky) is under a CC BY 3.0 license. 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). 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 Figure 5.19: Indris, the largest of the lemurs. highly seasonal breeders, often mating only during a short These folivorous lemurs are vertical clingers window once a year (Wright 1999). Female ring-tailed lemurs, and leapers and live in pairs. Credit: Indri indri for example, come into estrus one day a year for a mere six 0003 by Christophe Germain is under a CC hours. Unlike most primates, where males are typically large BY-SA 4.0 License. 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 5.20) and pottos are known for being slow, Figure 5.20: This slow loris, quadrupedal climbers, moving quietly through the forests to avoid being like all others in this detected by predators. These strepsirrhines have developed additional taxonomic group, is solitary defenses against predators. Lorises, for example, eat a lot of caterpillars, and nocturnal, with a diet which makes their saliva slightly toxic. Loris mothers bathe their young in heavy in insects and fruit. Credit: Nycticebus coucang this toxic saliva, making the babies unappealing to predators. In comparison 002 by David Haring / Duke to the slow-moving lorises and pottos, galagos are active quadrupedal Lemur Center is under a CC runners and leapers that scurry about the forests at night. Galagos make BY-SA 3.0 License. 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. Lemurs Lorises, Pottos, and Galagos South and Southeast Asia Geographic Madagascar range Central Africa Activity Diurnal, nocturnal, or Nocturnal patterns cathemeral Insectivore, frugivore, Dietary types Insectivore, frugivore or folivore Social Solitary, pairs, or small Solitary groupings to large groups Forms of Vertical clinger leapers, Slow quadrupedal climbers and locomotion quadrupedal active quadrupedal runners 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.] 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. Suborder Strepsirrhini Suborder Haplorrhini No rhinarium Rhinarium Short snout Longer snout Eyes more convergent Eyes less convergent Sensory Postorbital plate adaptations Postorbital bar No tapetum lucidum Tapetum lucidum Many are trichromatic Mobile ears Fovea Mostly insectivores and Dietary Few insectivores, mostly frugivores, few differences frugivores and folivores folivores Mostly nocturnal, few Only two are nocturnal, rest are diurnal or cathemeral diurnal Activity patterns and Ecology Almost entirely Many arboreal taxa, also many arboreal terrestrial taxa Mostly solitary, some Only two are solitary, all others Social groupings pairs, small to large live in pairs, small to very large groups groups Few taxa have little/none, many Sexual Minimal to none taxa show moderate to high dimorphism dimorphism 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 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 5.23). Tarsiers are small-bodied primates that live in Southeast Asian forests (Figure 5.24) and Figure 5.23: Tarsiers are possess an unusual collection the only living of traits that have led to some representatives of this debate about their position in Infraorder. Credit: Tarsier the primate taxonomy. They Sanctuary, Corella, Bohol are widely considered (2052878890) by Figure 5.24: Tarsiiformes are found in the tropical yeowatzup is under a CCmembers of the haplorrhine forests of multiple islands in Southeast Asia BY 2.0 License. group because they share including Sumatra, Borneo, Celebes, and the several derived traits with Philippines. Credit: Infraorder Tarsiiformes of Asia monkeys, apes, and humans, including dry noses, a map (Figure 5.22) original to Explorations: An Open fovea, not having a tapetum lucidum, and eyes that are Invitation to Biological Anthropology by Elyssa more convergent. Tarsiers also have some traits that are Ebding at GeoPlace, California State University, Chico is under a CC BY-NC 4.0 License. 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 tr