P r i m a t e s Nocturnal or Madagascar or both S.E. Asia S. America “Old World”

Origins and Relations?

Evolution Primate adaptive themes: “…exploitation of arboreal herbivory, arboreal locomotion, manual dexterity, stereoscopic vision, and complex social behavior and communication.” (Vaughan et al., 2000) Increased manual dexterity (next 2 slides) may be correlated with increase in brain size. Mostly animals of the humid tropics, primates are an ancient (Cretaceous) Order, probably evolving in N. Am. (soon extinct) (Europe )Asia & Africa S.America It is useful to consider the Primates as 2 Suborders: The Strepsirhini (“prosimian” lemurs, bush babies, galagos, etc.). The Haplorhini (anthropoids: monkeys, apes, people). The tarsier does not fit well with the anthropoids, but it is not a strepsirhine.

“Prosimians” (For each pair, hand is on left.)

“Anthropoid” primates (hands on left)

Taxonomic generalization (“suborders”) Strepsirhini (prosimians) Probably somewhat like earliest primates. Either Madagascar, or nocturnal, or both (all are tropical). Apparently do not compete effectively w/monkeys, etc. In contrast w/anthropoids: More smell-oriented Less obviously social Seasonal breeders Haplorhini (anthropoids) Platyrrhini (New World) Catarrhini (Old World) Tarsiars are placed in this group largely because of molecular evidence. People are worldwide; most other species are tropical. A commonly noted trend is toward behavioral (often social) adaptation rather than anatomical-physiological adaptation.

Ecological generalizations (regardless of taxonomic position) Smaller primates: For S/V reasons, must exploit high-energy foods. All eat arthropods plus occasional small vertebrates, which are difficult to collect in quantity. (Think protein.) Therefore most have other, reliable, sources of calories: Fruit (very seasonal) Seeds (somewhat seasonal) Resins & saps (less seasonal) Larger primates: Most are either leaf specialists or fruit specialists: “Leaf eaters”: Energy-conserving second-rate fermenters that usually supplement calories with fruit. (These get plenty of protein if they make their calories.) “Fruit eaters”: Plenty of energy; must supplement protein with selected leaves or seeds or animal matter.

Tarsius: Anthropoid life in the dark Formerly called a prosimian, now classed w/anthropoids, mostly on molecular evidence. The Family Tarsiidae includes 5 species in one genus. H-b of T. bancanus is 8.5-16cm; mass is 100-150g. Nocturnal S.E. Asian primates eating only animal matter. Solitary/social  an important concept Reputedly has largest eyes (per body size) of any animal; even gives up eye-mobility for size. (Why is size important?) Other night-vision adaptations….

Uh, why do they call it a tarsiar? Diagram compares right feet of tarsier and brown lemur. Note extreme elongation of the calcaneum and navicular (tarsal bones) in the tarsier. The tarsier also has a radically different mechanism of foot-rotation so that it can grasp vertical stems with inverted foot.

Family Galagonidae (4g/11sp) All are restricted to Africa. All are nocturnal. All have long tails, large, mobile ears, and strong hind limbs (all are great leapers). All are highly vocal. Diets vary, but galagos eat lots of arthropods (from which they derive some calories & all necessary protein). Most usually supplement this diet with fruit or with gums and resins. All are seasonal reproducers.

Galago sp. Lesser bush baby These African primates are slightly larger than tarsiars, and they have long tails. Primary habitat is woodlands. Mature more rapidly than other primates (XX sexually mature < 1 yr). Except for mother with offspring, most galagos are solitary, but community is defined by scent marks. In some areas, > 1 Galago species live sympatrically; partitioning should be studied.

Otolemur crassicaudatus, greater bush baby Woodlands of southern Africa, including suburbs. Mass 1-1.5kg (XX slightly larger). > 50% of calories from gums & resins (especially in winter). Social structure poorly known: XY said to be solitary; XX said to move in groups? XX territories overlap, but not much; XY territories encompass XX territories but don’t overlap other XY territories? How do you resolve the contradictions?

Family Lorisidae (lorises & potto) These are slow-moving nocturnal animals relying in part on gliding motion to avoid detection by predators. Unlike galagos, they do not jump. Wrists & ankles specialized: Great range of motion. Hands & feet are zygodactylus. “Special blood vessel storage channels in their hands and feet enable lorises to contract their muscles and hold tightly to a branch for hours, seemingly without fatigue or pain.” Socially, these primates live in a world of smells.

Loris tardigradus (slender loris) Range is s. 2/3 of India plus Sri Lanka. Mass is 200-450g. Diet is mostly arthropods. Solitary but social (!): Foraging usually solo, sleeping often not; XY mark territories by fecal sign posts; XX leave urine trails w/social information.

Nycticebus coucang, slow loris Deep-forest animal of S.E. Asia. H-b 25-35cm, mass 1.5kg. Diet 50% fruit w/ protein hits from small animals. Social structure & ecological relationships to other loris sps are poorly known in wild.

Perodicticus potto, the potto Nocturnal animal of W. African rainforest canopy. H-b 25-35cm; mass 1kg. Basis of diet is fruits, plus gums and small animals for protein hits. Young learn to eat by foraging with mother. Defensive behavior….

The Lemuriform primates All of these are restricted to Madagascar (see next slide). Here are some Family sketches: Cheirogaleidae: 4 genera of nocturnal primates ecologically more similar to African prosimians than to other Madagascar lemurs. Megaladapidae: Has only 1 living species, a leaf-fermenter, but formerly included huge terrestrial types filling artiodactyl niches. Lemuridae: 4g/10s. Most species are diurnal. Often partition habitat finely; mostly monkey-convergents. Indridae: 3g/5s. Large leaf-eaters, mostly diurnal. Some extinct members were large, terrestrial browsers. Daubentoniidae: The aye-aye is a strange nocturnal insect-eater, a woodpecker-convergent.

Alternative Evolution: Madagascar invaded by only 6 mammal Orders: Insectivores, carnivores, rodents, bats, artiodactyls & primates.

Patterns of Malagasy Extinctions

Aye-aye Daubentoniidae Originally classified as a rodent, this nocturnal primate occupies woodpecker niche on Madagascar. Note chisel teeth, long middle finger, and use of the finger in feeding. Like much other Malagasy fauna, aye-ayes are endangered by habitat destruction.

Brown & ringtail lemurs (Lemuridae; 5 genera, about 25 species) Eulemur fulvus: Mostly arboreal. Leaves & fruit. Flexible, multi-XY groups that can fracture into subgroups. Lemur catta: Mostly terrestrial. Dietary generalists. Group structure is organized around XX residents which are entirely dominant over transient XY.

Behavioral adaptability in the Lemuridae

Fat-tail & mouse lemurs (Cheirogaleidae; 4 genera; 17 species) Cheirogaleus medius (left): 200g (medium rat). Eat fruit + protein hits. Only hibernating primate. Microcebus murinus (right): 30g (medium mouse) Rainforest-edge species Foraging (for anything) mostly solitary, but XX day-nest together. Heavy depredation pressures; rapid maturity & twice-annual litters of 2-4.

Anthropoid primates: Phylogeny & general trends Increased body-mass Increased brain-mass/body-mass Longer life Increased manual dexterity Specialization of eyes: Binocular vision (at expense of olfaction) Increased density of cones Emphasis of visual acuity over light-gathering

Notes on sociality in “higher” primates: Primatologists are abundant and specialized; often they use a vocabulary of their own, naming many types of social structures. Most general mammalogists agree that: Primate groups vary among and within species. Most social organizations seen in primates have also been documented in other mammal species. Intraspecific variation is often correlated w/habitat. Territorial XY primates appear more attached to XX’s than to land. XX among primates are more likely (than XX among other mammals) to leave natal groups (but remember equids?). Human social organization varies & is almost unique.

Ancestor rafted from Africa. Groupings: New World Monkeys Ancestor rafted from Africa. Groupings: M&T: small, fruit & exudate eaters. C&S: Highly adaptable fruit eaters. N&T: Unripe fruit, leaves, insects. U&S: Seed eaters. H: Leaf eaters. S&W: Large, brachiating fruit eaters.

Callitrichidae (marmosets; our first anthropoid Family) 4 genera/26species of small monkeys confined almost entirely to South American forests. Evolutionary origins controversial: Small size is primitive condition? Small size is specialization for insect & resin diet? Little sexual dimorphism…. Group nucleus is one breeding pair (often monogamous) that is often assisted by stay-at-home older kids. Litter size is typically 2 (dizygotic twins; shared placenta…); offspring receive extensive family care.

Marmosets & tamarins (Callitrichidae) Golden-chested marmoset: Mass < 500g; squirrel-like in activity. Most calories from resins. Sociality & reproduction…. Golden lion tamarin: Mass c. 500-750g. Most calories from fruits.

New World Monkeys: Cebidae 11 genera, 58 species, small to medium size. Vast majority South American w/ some species extending into Central America and a few crossing into North America (in s. Mexico). Evolutionary origins unclear, but emerging consensus holds with rafting from Africa? All species but one are diurnal. Tail typically long, often prehensile. Major ecological differences are between fruit-eaters and leaf-eaters.

Squirrel monkeys (Saimiri) Not much larger than marmosets (0.7-1.2kg). Social and arboreal omnivores. Large groups, poorly studied: XX: maturity @ 2 yrs; sisterhood, “aunting.” XY: Loose dominance hierarchy mediated by physiological changes.

Cebus monkeys Cebus has the largest brain/body ratio of any New World primate. Most diverse diet of any New World primate. One of few mammals in which XX’s often outlive repro. years. Members of this genus are highly adaptable: In the wild: home range, occasional tool-use, social organization. In captivity, general “train-ability.” C. albiniforns (left) C. capucinus (right)

Dusky Titi Monkey (Callicebus moloch) Diet is mostly leaves and green fruit, supplemented by ripe fruit and insects. Titis are basically monogamous, bearing young early in rainy season. Although they do well in zoos, these monkeys are not well known in the wild.

Night Monkey (Aotus trivirgatus) Sometimes called owl monkeys, these are the most nocturnal anthropoid primates. Diet is fruit, leaves, & insects (+ small verts). Basically monogamous. The taxonomy of this monkey is confusing; some authorities name up to 9 species. This species is of considerable medical interest because owl monkeys are immune to malaria.

Uakaris (Cacajao calvus) These are poorly known monkeys with short tails, shaggy bodies, & naked heads. Mass is 3-4kg w/XY slightly heavier than XX. Habitat makes study of uakaris almost impossible Multi-XX, multi-XY groups w/XY dominance. Food may be primarily seeds.

Sakis (Pithecia sps.) Sakis are medium-small monkeys (1.5-2kg). Diet includes fruit but is probably dominated by seeds and nuts (see teeth). Social structure is not well known but involves breeding pairs. (Sakis are sexually dichromatic.) These are great leapers in mature forests.

Howlers (Alouatta sps.) The most common monkeys in most Neotropical systems. XX mass 4-5kg; XY 6.5kg. Cautious, “lazy” leaf-eaters marking territory by vocalizations. Group size reflects resource density. Groups are 1-XY harems within which XX rankings are age-inverted.

Wooly & Spider Monkeys These are the largest New World monkeys; h-b length to 60cm & mass to 12kg. Diet is mainly fruit, supplemented for protein. Group structure is highly flexible, varying with habitat and season. Sexual dimorphism is minimal; though males do have dominance hierarchies, they are loose & generally age-structured.

“Old World” Primates

Family Cercopithecidae The most successful primate Family (18g/81s) Africa; East, South, & Southeast Asia. Extending beyond tropics in southern Africa, China, Tibet, and Japan. Mass ranges from 1.5 to > 50kg. Most are diurnal; all are highly social. Ecologically divisible into 2 groups: Colubinae, the Old World leaf eaters Cercopithecinae, the Old World generalists.

African leaf-eaters (e.g., Colobus guereza) Mass XX 8kg; XY 12kg. Central Africa; habitat is rainforest, gallery forest, well-structured secondary forest. The most capable fermenters among African primates (all primates?). Multi-XY groups (8-15) w/dominance hierarchies. Small (c. 18ha) ranges defended against other groups.

Asian leaf-eaters (e.g., Semnopithecus entellus) Hanuman langurs are south-Asian. XX 12kg; XY 18kg. Diet 35% leaves, 25% fruit; 40% misc. Social structure changes as function of monkey/ resource density: Low: multi-XY groups. High: 1-XY harems plus bachelor groups that take over harems (“lion” pattern).

Cercopithecus [Chlorocebus] aethiops Found in southern African open woodlands. XX 3kg; XY 4kg. Group size ecologically flexible (usually 15-25) with multiple XY and dominance hierarchies. XX stay in natal group; XY out-migrate. CIV’s: Each species of Cercopithecus (sensu lato) may have its own. About 50% are non-symptomatic carriers.

Baboons (Papio hamadryas) Baboons are large, pan-African monkeys living in large, intricately-structured social groups evolved in part for collective defense. Sexual dimorphism is extreme: XX 15kg; XY to 50kg. Diet includes anything that provides good nutrition.

Further baboon notes Group structures and subspecies/habitat differences: Effectiveness of group defense where needed…. Southern African savannas: 20-50 animals; group defense in a predator-rich environment. Ethiopia: Few big, safe sleeping areas (& thus groups of several hundred baboons); sparse resources (& thus foraging groups of 1-2XY + XX), residual “typical” groups…. Life within a group: XY hierarchy obvious & important; XX hierarchy subtle and more important for eventual status of offspring. Until mature, (c. 4 years) XY remain subordinate to XX. “Godfather” relationships rare but potentially important. “Political” behavior, troop shake-ups, and XX behavior.

Other baboon-like monkeys Mandril (Mandrilus spinx): This is a large monkey with brightly-colored face & hindquarters, poorly known in the wild, that fills a baboon-type niche in African rainforests. Groups are smaller than among baboons. Gelada (Thercopithecus gelada): This is a big monkey of the Amhara Plateau. Sociality looks at first like that of baboons– but XX are socially more important. Perhaps this reflects the fact that gelada XX stay with their natal groups while baboon XX out-migrate.

Macaques (Asian generalists) Macaques include one genus (Macaca) & 16 sps. Diets, social structures, and habits vary by habitat, but all are adaptable. All include multi-XY groups w/ XY & XX dominance hierarchies. Long-term studies on Japanese macaques indicate group innovations are brought in by young XX’s. Example is “crab-eating” macaque, Macaca fascicularis. Group size is 10-50; food mostly fruit.

Macaca nemestrina sociality, #1 Adult XX with offspring. As with baboons, macaque babies inherit to some degree the status of their mothers. Also, the status of a XX with infant is temporarily raised. And XX’s who are consistently successful mothers often have higher status.

Macaca nemestrina sociality, #2 Adult XY, pucker-threat. Note the crouch, the extended lips, and the forward-directed posture, which are diagnostic for several types of threat. The pucker-threat is an assertion of dominance that typically elicits either submission or a reciprocal challenge (and then possibly a fight).

Macaca nemestrina sociality, #3 Adult XX, pucker-threat. XX almost always respond submissively to XY threats, but macaques are also individuals. This XX (you’ve seen her before) is able to reciprocate the XY threat because (1) he’s low-ranking, (2) she’s usually high-ranking, and (3) she has an infant with her.

Macaca nemestrina sociality, #4 Male-male mount. In primate societies things that appear to be about sex are often about power. To appease a higher-ranking XY, a lower-ranking XY acts submissively, “presenting” sexually (an XX gesture). The higher-ranking XY accepts, with a symbolic mount. Note the young animal looking on– and becoming socialized.

Macaca nemestrina sociality, #5 Low-status adult XY, fear-yawn. The lowered eyes, raised brows, & retracted head indicate fear, as does the yawn itself. The exposed canines indicate that attack would nevertheless risk injury. Note that some facial gestures have been conserved for MY in primates.

Macaca nemestrina sociality, #6 Coalition of brothers. As with other social animals (e.g., lions), displacement of group leaders is often accomplished by coalitions. In macaques, coalitions almost always involve (half-) brothers because most lasting social connections are established through mothers.

The Ape Grade A general evolutionary trend among anthropoid primates is increasing reliance on vision at the expense of smell. The trend culminates in apes and is associated w/increased hand-eye coordination & enlargement of the brain. Ape-grade primates lack external tails. In all except people, arms are longer than legs. Apes have long inter-birth intervals & extended parental care (both anthropoid trends). All ape-grade primates (except people) are pan-tropical and endangered– by direct exploitation and/or habitat destruction.

Family Hylobatidae This Family includes gibbons & siamangs (1 genus, 11 species); picture example is Symphalagus syndactylus. These are small (10-12kg), tailless, fruit-eating apes of S.E. Asian rainforests. Monogamous fidelity is extreme. Inter-birth intervals are c. 3 years. 2-parent care is extensive (6-7 years). First birth is at about 9 years. Pairs “mark” territory by brachiating displays & duets.

Orangutans (2 similar species) Pongo pygmaeus, from Kalimantan, is illustrated; another sp. on Sumatra. XX ave. 40kg; wild XY twice as heavy. Adult XY avoid other XY & use roars to maintain territories overlapping ranges of > 1 XX. XX are at first repro is about 12-15yrs. Only cohesive social unit is mother + offspring.

Common chimp (Pan troglodytes) Chimps are forest animals of Central & West Africa. XX 35kg; XY 45kg. Diet varies but is usually dominated by fruit. (Hunting traditions in some groups….) XX sexually mature @ 14; inter-birth interval c. 5 years. Unique because XY-XY bonds form backbone of social groups (XX out-migrate). Chimps share c. 98% of genes with people.

Bonobo (Pan paniscus) The bonobo, or pygmy chimp, inhabits central rainforest along the Congo basin. Anatomically and genetically similar to common chimp… …but radically different socially: Sex seems to be the glue that holds bonobo society together. XX’s are migratory gender, but relationships among them are strong. Even adult XY’s appear to take status partly from mothers.

Gorillas (Gorilla gorilla; 3ssp.) Gorillas are, on ave., the largest primates: XX 85-95kg; XY c. 165kg. Habitat is dense forests, swamps, etc. 2 lowland ssps eat fruit; mountain ssp eats leaves & shoots. Group size typically 5-20; most include 1 (2) large XY plus XX’s & young. Inter-birth interval 3-5 years. XX & XY out-migrate.

People (Homo sapiens) The most abundant primate species. Large African primate most closely related to chimps– but radically divergent in anatomy & behavior. People are world-building (as opposed to world-accepting) animals relying on artificially constructed ecosystems for almost all material needs.