Chapter 17
Humans are the product of the ape lineage that launched out into expanding savannas. Several adaptive challenges needed to be overcome. Increased competence in bipedal locomotion was required to traverse the widening gaps between trees. Then there was the problem of what to eat during intensifying dry seasons when trees were mostly leafless, while the leaves that did remain were tough to digest and fruits were few and far between. However, savanna plants must store carbohydrates in roots, bulbs and tubers to regenerate foliage at the start of each wet season. To extract them from underground, the evolving ape-men needed to dig and to chew, like porcupines do. Above ground, there remained another potential source of food in the bodies of the herbivores that were adapted to digest the leaves of expanding grasslands as well as those on trees. Scraps of their flesh and bones became available on the carcass remains of animals killed by carnivores, particularly during the dry season when plant resources were sparsest. Exploiting bits of meat and bone marrow required stone tools to be deployed to scrape off flesh and break open bones. Further adaptations in locomotion, dentition, thermal tolerance and stone tool technologies led evolving humans to become hunters in their own right, exploiting time windows to reduce competition from hunting and scavenging carnivores. Of course, they also needed to avoid becoming food themselves for the carnivores.
In this chapter, I consider first the evolutionary transitions that took place in physical features preserved in fossilised bones, skulls and teeth. Four major adaptive shifts can be recognised. The first entailed the development of bipedal locomotion, during the late Miocene. This was followed by trends in dentition towards greater chewing capacity during the Pliocene. The dental trend then became reversed as humans evolved longer legs and larger brains, with a surge in cranial capacity associated with the climatic transition into the Pleistocene. Lastly, following amplified climatic oscillations defining the start of the Middle Pleistocene, brain volume surged to modern levels and facial features converged on those of modern humans. My focus in this chapter is on the ecological processes driving adaptive changes in physical forms. Supporting changes in cultural artefacts in the form of stone tools and, increasingly, other technologies will be covered in the following chapter.
The fragmentary nature of the fossil record in time and space must be acknowledged. Sites providing hominin fossils in eastern Africa are located mostly alongside rivers or lakes within or adjacent to the Eastern Rift Valley. Those in southern Africa are located mostly within cavities formed in dolomitic limestone in the high central interior. Figure 17.1 shows timelines linking named species representing the various hominin forms distinguished, indicating advances in adaptive grades.
Figure 17.1
Timeline of hominin species recognised with colours indicating adaptive grades from early ape-men to modern humans.
(supplied by Bernard Wood, updated from Wood & Boyle (2016) American Journal of Physical Anthropology 159:37–78)
Emergence of Ape-men
The connections between the earliest hominins and the common ancestor shared with chimpanzees have yet to be revealed and may never be. The crucial period between 12 and 6 Ma, from mid to late Miocene, has yielded few fossil deposits. So far, only two enigmatic fossil finds from this time interval have been linked with hominin divergence.1 The ‘Toumai’ skull, scientifically named Sahelanthropus tchadensis, was discovered on the land surface in Chad in north-central Africa and dated approximately to around 7 Ma. Its foramen magnum connecting the brain to the spinal cord had shifted anteriorly, consistent with an upright posture, while its dental features appear intermediate between those of chimpanzees and later australopiths (which I will colloquially label ‘ape-men’, while recognising that there were women as well). However, its cranial volume remained no bigger than that of a chimpanzee. The second set of fossils, given the name Orrorin tugenensis, consists of a mandible plus limb and foot bones extracted from sediments in the Tugen Hills situated in west-central Kenya, dated to ~6 Ma. These limb bones show greater support for upright balancing than is typical of apes.
The earliest more firmly hominin fossils come from Ethiopia, dated to the period between 5.7 and 4.4 Ma and assigned to the genus Ardipithecus (Figure 17.2A).1 They show features of leg and foot bones that would facilitate upright walking, but retain grasping big toes that would help with tree climbing. The oldest fossils placed in the genus Australopithecus, named Australopithecus anamensis, come from deposits dated between 4.2 and 4.0 Ma found from north-eastern Ethiopia into the Turkana region of northern Kenya, but no further south.1,2 They show further advances in hind-limb and ankle bones for bipedal walking, but no change in cranial capacity. Dentally, these ape-men deviated from modern apes by having smaller incisor and canine teeth coupled with larger molars bearing thicker enamel, supportive of a dietary shift from soft fruits towards tougher plant parts. Au. anamensis is abundantly represented in fossil assemblages through this northern region of Africa, contributing as much as 5 percent of fossil specimens, similar to early baboons. The lakeshore or riparian vegetation present around the fossil sites during that period took the form of a varying mosaic of quite dense woodland and quite open grassland.3,4 Other animals present included numerous proboscideans along with frugivorous monkeys, while among the ungulates browsers were more common than grazers. The diet of these early australopiths was restricted entirely to C3 plants.5
Figure 17.2
Competence in bipedal locomotion. (A) Ardipithecus depicted walking among trees in a wooded environment (artwork: Jay Matternes); (B) Australopithecus afarensis family depicted walking bipedally across a volcanic ash surface at Laetoli, where their footprints are preserved.
(artwork: Marco Anson)
Following on chronologically, Au. afarensis was distributed more widely throughout eastern Africa in deposits dated to the period between 3.85 and 2.95 Ma.6 A nearly complete skeleton discovered in Ethiopia was labelled ‘Lucy’, from the Beatles’ song about diamonds in the sky played during the celebration following its finding. The bipedal walking capabilities of this species are documented by footprints of three individuals etched on volcanic tuff at Laetoli in Tanzania, dated to 3.6 Ma (Figure 17.2B). A cranium dated to 3.4 Ma found west of Lake Turkana with a flattened face and somewhat smaller molars was named Kenyanthropus platyops; but the generic distinction is questionable given the range of variation among specimens assigned to Australopithecus. Nevertheless, it might represent an initial stage of the shift towards the more ‘gracile’ features shown by early Homo. After 2.9 Ma, two hominin lineages diverged. Fossils with massive jaws and especially large cheek teeth, colloquially named ‘nutcracker man’, appear earliest in the Omo valley of south-western Ethiopia, dated to 2.7 Ma, and shortly thereafter in the Turkana basin in adjoining Kenya.7 They are generally assigned to a distinct genus, Paranthropus. These robust ape-men were far rarer in local faunas than Au. anamensis had been, contributing less than 1 percent of fossils. Paranthropus boisei persisted in eastern African fossil deposits with little morphological change until around 1.3 Ma.
Within South Africa, an almost complete skeleton named ‘Little Foot’, from the bones that were first exposed in the enclosing breccia at Sterkfontein, was given the name Au. prometheus and dated to 3.67 Ma,8,9 although this early time has been contested.10 The physical features of its skull and dentition resemble those of Au. anamensis from Ethiopia dated around 4 Ma. Au. africanus, its likely descendant, is abundantly represented in various cave sites in the Cradle region from 2.8 Ma until around 2.3 Ma. Its type specimen is the Taung skull of a child, apparently killed by an eagle. A nearly complete skull found in Sterkfontein Cave was named ‘Mrs Ples’ (Figure 17.3; but ‘she’ might have been a male). Au. africanus persisted somewhat later in South Africa than its eastern African counterpart Au. afarensis, overlapping in time with the transition to early Homo in the north. Fossils dated more recently to 1.98 Ma, found in a single cave in South Africa, were given the name Au. sediba.11 They show human-like molar teeth and pelvic girdle, but brain size and facial shape similar to chimpanzees.12 Their long thumbs coupled with short fingers could have facilitated the precision grip needed for manipulating stone tools, while bone structures in the hands and wrist would have aided arboreal climbing. It has been suggested that they are closely linked to the ancestry of Homo,11 but I wonder whether they might be ancestral to the strange Homo naledi found likewise in a single cave and dated to 260 ka (see below). The local robust ape-man, Paranthropus robustus, made its appearance in South African cave sites around 2 Ma and became the most abundant hominin represented there until around 1.0 Ma. Its limbs and hand bones suggest that it was less effectively bipedal than coexisting forms of Homo, but somewhat better at tree-climbing.
Figure 17.3
Skulls of robust ape-man (Paranthropus robustus) (left) and more gracile ape-man (Australopithecus africanus) (right) from cave deposits in the Cradle of Humankind, South Africa.
Becoming Human
The earliest fossils placed in the genus Homo come from Ledi-Geraru in the Afar region of north-eastern Ethiopia, in the form of a mandible with teeth dated to almost 2.8 Ma.13 They exhibit features transitional between Au. afarensis and later specimens from Ethiopia assigned more firmly to early Homo, dated to around 2.4 Ma. Vertebrate fossils suggest that the habitat had become prevalently more open with a mixture of grassland and riparian forest and expanded C4 component around that time.14,15 Around one-third of the bovid taxa identified at the site made their first appearance then, including the earliest wildebeest (Connochaetes sp.).
The Ledi-Geraru mandible is followed after an interval of 400 kyr by fossils assigned to early Homo recorded not only in Ethiopia, but also further south in Kenya and even Malawi.7 This gap in time happens to span the climatic transition into the start of the recurrent ice ages typifying the Pleistocene. Further specimens assigned more firmly to H. habilis, including a nearly complete skull, come from both the Omo–Turkana Basin and Olduvai Gorge, dated ~1.9 Ma. This name, meaning ‘handy man’, was given because the fossils were associated with stone tools defining the Oldowan culture at Olduvai. Features distinguishing this species from earlier australopiths include a larger body size and cranial capacity, less-protruding face, longer legs, smaller jaws, and smaller molar teeth with thinner enamel. Hominins somewhat larger in size discovered to the west of Lake Turkana, likewise dated to ~2.0 Ma, were named H. rudolfensis, but may not be sufficiently distinct from H. habilis (or H. ergaster) to justify the species distinction. Fossils from the South African cave sites allied with early Homo are generally too fragmented to be assigned reliably to any particular species. These very early humans were rare components of local faunas, making up less than 0.1 percent of all large mammal fossils, which is less than contributed by Paranthropus spp. and similar to that formed by large carnivores. The scarcity of fossils representing early Homo in South African cave sites suggests that early humans were either rare in this Highveld plateau region, or much less susceptible to falling (or being dragged) into cavities than Paranthropus.
The earliest fossils assigned to H. ergaster come from the Omo–Turkana Basin, dated to ~1.9 Ma, but became common elsewhere only after 1.7 Ma. H. ergaster is commonly merged with H. erectus, named from fossils found in Java and elsewhere in south-east Asia. It made its appearance during the time when glacial oscillations defining the Pleistocene, coupled with local earth movements, further accentuated aridity in eastern Africa. These proto-humans exhibited a cranial volume a little larger than that of H. habilis, stood as tall as modern humans, and walked as competently.16,17 Their molar teeth were relatively smaller than those of the gracile australopiths, and incisors somewhat larger, thereby reverting towards dental features of the great apes. Cranially, they retained a sloping forehead and prominent brow ridges. Surprisingly, a juvenile cranium recently recovered in Drimolen Cave in the Cradle region of South Africa, ascribed to H. ergaster, has been dated as early as 2.0 Ma, preceding the first appearance of this species in eastern Africa.18 The next earliest record of H. ergaster in the Cradle region is a specimen from Swartkrans dated shortly after 1.8 Ma.12
Specimens allied with H. habilis apparently persisted alongside H. ergaster until ~1.4 Ma. Whether these two forms segregated ecologically or represent a single polytypic species remains debatable. Distinctions between them are based mainly on skull shape.17 H. ergaster showed a slow expansion in brain size and progressive reduction in molar surface area through time, although rather poorly documented. It was replaced by H. heidelbergensis, clearly a descendent, around 800 ka, both in Europe and in Africa.19,20 This was around the time when the period between glacial extremes lengthened to around 100 kyr, defining the transition from early to middle Pleistocene when seasonal extremes of aridity intensified in Africa. By that stage the cranial volume of these early humans was almost equal to that of modern humans. H. heidelbergensis was clearly ancestral to the European Neanderthals (H. neanderthalensis), but how it connected with early humans inhabiting Africa remains obscure. Genetic evidence suggests that the Neanderthals separated from the human lineage in Africa around 500 ka.21 They differed from modern humans in their stocky build, prominent brow ridges, and sloping rather than domed foreheads.
The earliest fossils sufficiently similar to modern humans to be assigned to the species Homo sapiens come from a cave in Morocco dated to between 300 and 350 ka.22 These craniums show a reduction in face size, like later humans, but retain fairly prominent brow ridges and lack the globular shape of the braincase characteristic of modern humans. The Kabwe skull, found in a limestone cave in Zambia, has also been dated to ~300 ka.23 It has been affiliated with H. heidelbergensis due to its lack of more modern features. A partial cranium from the Lake Ndutu region near Olduvai also represents this time period.24 Slightly more recent is the Florisbad skull from interior South Africa, dated approximately to ~260 ka and regarded as representing early H. sapiens. Partial human skulls from Herto and Omo in Ethiopia and Turkana in Kenya, dated to between 160 and 195 ka, are more firmly accepted as modern humans.
Strangely out on an evolutionary limb are the remains of diminutive humans with small but complexly shaped brains named Homo naledi, which were found deep in a cave system in South Africa. Although their features resemble those of early humans living around 2 Ma, their hardly fossilised bones date from as recently as ~280 ka.25 While their leg and foot bones were adapted for efficient walking, their hands retained long fingers, which would have facilitated climbing trees. They had smaller but higher-crowned molars with greater wear-resistance than the dentition of the australopiths, suggesting that abrasive particles were prominent in their diet.26 They apparently coexisted alongside H. ergaster for well over a million years without showing up elsewhere in fossil deposits.
Around 130 ka, humans with modern features appeared in the Levant region of the Middle East, but did not persist there for very long. This was around the beginning of the relatively moist interglacial period that defines the transition into the late Pleistocene. The major dispersal of modern humans beyond Africa through the Middle East and onwards occurred ~60 ka. These people evidently followed a coastal route through tropical Asia, arriving in Australia ~55 ka. By 47 ka they had spread westward into Europe, displacing the Neanderthals within a few thousand years.
The Locomotor Transition: From Brachiating Arms to Legs for Walking
During the late Miocene, the space between trees occupied by grassland widened as temperatures cooled and precipitation became more seasonal, promoting the radiation of browsing and grazing ruminants. For the stem hominins, the conversion of forest or woodland into savanna meant more time spent in terrestrial travel and less time foraging in tree canopies. If the tree canopy cover thinned from over 90 percent, representing a forest, to under 30 percent as is typical of savanna, this would approximately triple the home range needed by chimpanzees to encompass sufficient fruit-bearing trees, towards ~50 km2. Covering such a large area could not readily be accomplished by waddling clumsily on two legs, or by knuckle-walking. More likely, fruit-dependent apes became confined to localities where the tree cover remained closer to 50 percent, or where forest strips traversed savanna vegetation formations, as found where chimpanzees occupy moist savanna in Senegal.
Whichever situation prevailed, selective pressures would favour hind-limb adaptations facilitating bipedal walking, while forelimbs retained their capabilities for ascending trees to access fruits and to escape from ground-based carnivores at night. Bipedal locomotion also provides an elevated perspective for detecting predators lurking in the grass and frees arms for carrying food or other things to safer sites.
Food supplies for herbivores diminish drastically during the dry season when trees shed their leaves and herbaceous plants whither and become dormant. This is illustrated by the foraging ecology of kudus, which consume a foliage diet augmented by fruits and flowers when available (Chapter 10). Towards the end of the wet season while trees retained abundant foliage, kudus needed only 8 steps to be taken for each minute of feeding time; but by the late dry season their movement rate became tripled to 24 steps per minute of feeding, i.e. only a third as much food gained per step taken, despite concentrating where most food remained.27,28 Kudus restrict their dry season foraging to localities near rivers or around the bases of hills where most evergreen foliage remains. Fruits contribute rather little to their diets during the dry season, after fallen acacia pods had been depleted (Figure 10.5).29 Kudus are absent from savanna regions where trees retain insufficient leaves, for example from the open umbrella thorn savanna prevalent in Serengeti NP.
Adaptations for bipedal locomotion were apparent in Ardipithecus, the earliest unquestionably hominin fossils, after the start of the Pliocene ~5 Ma. They include lengthened legs, shifts in how the hind-limbs articulated with the pelvis, and stiffened rather than dextrous ankle joints. Furthermore, the skull opening connecting the brain to the spine (‘foramen magnum’) had shifted centrally to support an upright head posture. By 3.6 Ma in the mid-Pliocene, australopiths had become competent bipedal walkers, as shown by the footprints preserved at Laetoli, despite retaining offset big toes (Figure 17.2B). By 1.7 Ma in the early Pleistocene, long-legged H. ergaster was as effectively equipped for bipedal walking, and perhaps also for running, as modern humans are.
Dietary Shifts: From Fleshy Fruits to Tough Tubers
As aridity intensified during the Pliocene, trees potentially providing fruits became more widely spaced, and the herbaceous layer between became dominated by grasses. Grass leaves may be sufficiently nutritious while young, even for primates with simple stomachs like geladas, but become more fibrous and resistant to digestion after they mature and turn brown during the dry season. Hence Pliocene hominins needed to look for food below the soil surface, especially during the dry season.
Many of the plants grouped as forbs store carbohydrates underground in the form of bulbs (compacted stem bases) or tubers (swollen roots). Grasses and sedges relocate nutrients in corms (swollen stems) and rhizomes (connecting roots) during the dry season. Underground plant parts form the staple food resource for mole-rats, which forage in tunnels beneath the soil surface, and for porcupines, which dig up bulbs and tubers. Warthogs root for grass rhizomes during the dry season and baboons scratch for corms. Mole-rats first appeared in the fossil record during the Miocene, while porcupines are first recorded late in the Miocene. This indicates that underground storage organs of plants had become sufficiently abundant for the needs of these large rodents by the late Miocene, along with the expansion of grasses. Omnivorous pigs, which use their snouts to dig, diversified a little later during the early Pliocene. The australopiths needed to join this ‘rhizophage’ guild.30
Fossils document the dental trend that australopiths showed towards enlarged molars of low relief with thickened enamel, enabling them to chew and chew, while their canine teeth became reduced so as not to obstruct grinding.19 Au. anamensis had initiated this trend by 4 Ma and it became accentuated in later australopiths. Molar enlargement reached its epitome in the Paranthropus forms, which possessed massive jaws with huge molars. These dental features seem adapted especially for processing the ‘fallback’ foods providing subsistence through the dry season, rather than the staples forming the bulk of the diet during the wet season, which were probably still fruits, seeds and leaves. Nevertheless, greater chewing capabilities might also have been helpful for breaking open fruits with hard shells, like monkey oranges and baobab pods.
Plants with large underground tubers are particularly abundant in sandy savanna regions and less common on volcanic soils.31 Sedges are especially abundant in wetlands, although dryland forms do exist. Sandy soils intermingled by wetlands are typical of broad-leaved miombo woodlands and coupled there with seasonally abundant fruits. It has been suggested that this dietary mix could best have been obtained within Zambia in south-central Africa, rather than in the rift valley regions of eastern Africa,32 but quite possibly miombo-type woodlands extended as far north as Ethiopia during the late Miocene and Pliocene while rift valley troughs were still forming.
Besides the form of the teeth, information about the diets consumed by extinct hominins can be gleaned from (1) the form of scratches, pits and other micro-wear on tooth surfaces33,34 and (2) stable carbon isotope ratios in tooth enamel.35 From micro-wear abrasions, it can be deduced that Paranthropus consumed hard-brittle corms, tubers and seeds. Paranthropus fossils are frequently associated with wetland grasslands, which contain abundant sedges, in eastern Africa.36 The comparatively gracile australopiths, which were around earlier than the robust-jawed ape-men, evidently ate tough but less-hard bulbs mixed with some animal matter.37,38
The difference between the heavy and light carbon isotopes 13C and 12C in body tissues indicates the relative portion of the diet derived from C4 grasses, or from animals eating these grasses (like some rodents, grasshoppers and termites), versus fruits or other plant parts obtained from trees and non-grassy herbs (see Chapter 10). Stable carbon isotope ratios in the teeth of Au. africanus indicate that food derived directly or indirectly from C4 grasses constituted 30–40 percent of its diet on average, very similar to that shown subsequently by Paranthropus robustus despite their dental differences.5,39 More remarkable is the wide individual variation in the C4 contribution to the diets of both species of ape-man in southern Africa.5,40 There is also a surprising divergence in the C4 component between the robust ape-men inhabiting eastern African and those in southern Africa, with a maximum of 80 percent recorded for P. boisei at Olduvai.5,36 The dental micro-wear shown by Paranthropus in eastern Africa is also less complex than shown by the robust ape-men from South Africa’s Cradle region, suggesting a more leafy diet. The two Au. sediba skeletons from around 2 Ma had both consumed solely C3 plants, although large mammals associated with them had eaten large amounts of C4 grasses at that time.41 A reversal of the trend towards robust dentition from the australopiths to Paranthropus is a distinguishing feature of the lineage that become Homo. Following the emergence of H. ergaster there is a dietary shift towards increased consumption of C4 resources around 1.65 Ma.42
Robust-jawed Paranthropus spp. persisted alongside forms of early Homo for around a million years, fading out after 1.3 Ma in eastern Africa but only by ~1 Ma in southern Africa.43 It seems that progressive dryness eventually made the ‘nutcracker’ lifestyle no longer tenable. Nevertheless, porcupines survived into modern times consuming a mix of fruits and underground plant parts in savanna regions; but being smaller they require less food per day than would a hominin.
Homo naledi retained morphological features typical of hominins dated around 2 Ma, and hence must have coexisted alongside the robust australopiths and H. ergaster since that time. How might it have differed in its diet? Perhaps it exploited the forb component in Highveld grasslands, supplemented by grass seeds plus grassland insects and rodents as a protein supplement. Large mammals are less abundant in high-altitude grasslands, so making a living as a hunter or scavenger in this savanna variant does not seem a viable proposition. Further insights are needed to resolve its mysterious niche.
Scavenging for Marrow or Meat
Life in savanna became increasingly tough as global cooling intensified dry season aridity. Another opportunity was there to be exploited: gaining from the energy and nutrients contained in the bodies of the large herbivores that were able to eat and digest tough plant parts. Helpfully, these herbivores are most likely to die in the dry season when food and water run short, especially in drought years.
While digging for bulbs and tubers, the early australopiths would have encountered burrows of mole-rats, mice and other rodents, and likely extracted the inhabitants using wooden or bone tools like modern San people do for springhares. Reptiles like tortoises and lizards would also have been found, perhaps singed by the passage of dry season fires, and added to the protein larder. Thus ‘faunivory’ in some form probably contributed protein to the diet of the australopiths, like it does for chimpanzees and baboons.
While nutritious plant parts became scarcer and harder to process for a primate with the passage of the Pliocene, grazing ruminants became more abundant and diverse. These animals might have seemed tantalisingly out of reach to a primate not much more robust physically than a chimp. However, as noted in Chapter 10, all animals die eventually, either through the agency of a predator or simply from old age or starvation. While searching for food through dry-season landscapes bereft of much vegetation cover, the ape-men would have encountered the carcass remains of large herbivores that had been killed by carnivores, or had starved to death during droughts.44,45 Large carnivores were especially diverse during the late Pliocene, including 2–3 species of sabretooth cat along with several species of hyenas, some adapted for bone-crushing and others for pursuing prey (Chapter 11). Lions appeared late in the Pliocene, but did not become common until after the sabretooth cats had faded out in the early Pleistocene. Leopards and cheetahs were, however, represented during the Pliocene. The danger for ape-men from encountering such large carnivores during daylight is not as great as is commonly feared. As ambush predators, the sabretooth cats probably hunted mainly nocturnally as also would have the cursorial hyenas. As long as the ape-men retained capabilities for ascending trees following encounters, they should have been sufficiently secure, especially if they moved in groups.
Modern lions leave little flesh behind on the carcasses of the medium–large ungulates that they preferentially kill, and what is left gets rapidly removed by vultures (Figure 17.4A,B), but limb bones containing fat-rich marrow remain, while skulls enclose fatty brain tissues. Sabretooth cats probably used their enormous canine daggers to kill and dismember thick-skinned animals (‘pachyderms’), not only young elephants, rhinos and hippos, but also short- and long-necked giraffes and giant long-horned buffalos, etc. Leopard kills stashed up in trees could also be stolen while the owners were absent. Hyenas can crush limb bones, but would be active mainly nocturnally. Modern spotted hyenas seem not to hunt much in woodlands, perhaps because of the difficulty of prolonged chases there, and the extinct hyenas may also have shown this pattern. Thus, more bones along with some bits of flesh might have remained particularly on carcasses in wooded areas, with climbable trees nearby, and be less readily detected by vultures under tree canopies.46
Figure 17.4
Carcass remains. (A) Lion feeding on the remains of a zebra, Kruger NP; (B) carcass left behind from lion kill of a buffalo, Luangwa Valley, Zambia; (C) early humans depicted scavenging for meat and bone marrow from a buffalo carcass – although it is unlikely that females and young would have been present at a kill site while hyenas would be in their dens during daylight.
(© O-M. Nadel 2020)
Securing bone marrow, brain tissue, and perhaps meat fragments from carcasses need not entail ‘confrontational’ scavenging, i.e. driving carnivores from their kills.44 Left-overs could be gathered towards midday while big cats rested nearby (Figure 17.4C). Hyenas would be long gone back into their dens. Hominins could thus have exploited this temporal window around midday without incurring much risk. Marrow contained within bones would not be putrid, so there was no requirement for meat-eating primates to cope with bacterial toxins. Large herbivores are most readily killed by carnivores during the dry season when plant resources run short, facilitated by concentrations of water-dependent animals around remaining water sources. During extreme droughts when ape-men most desperately needed something else to eat because of the scarcity of plant foods, more carcasses would become available from animals dying of starvation.
How ample would the supply of carcasses have been for the food needs of hominin scavengers getting only what was left behind by large carnivores? Scavenging typically entails long distance travel to find sufficient remains of animals47 (see Chapter 11). Only birds able to fly far, like vultures, are obligate scavengers. Mammalian scavengers like brown and striped hyenas traverse distances averaging 20–30 km nightly, and they kill mostly small animals encountered opportunistically.48 Jackals supplement meat obtained from carcasses or from their own kills of small mammals and birds with various fruits.
Based on ungulate population totals in the Serengeti ecosystem and their annual mortality rates estimated during the 1970s, the annual production of large herbivore carcasses was then around 2000 kg/km2.47 Medium–large wildebeest and zebra contributed 60 percent of this, of which 30 percent were juveniles. Large carnivores killed 30 percent and scavenged 6 percent of the animals that died. The remaining two-thirds of animal deaths resulted from either starvation or illegal hunting within the national park. Over half of the mortality took place during the three months of the late dry season from August to October. During this time of the year, migratory ungulates were concentrated in the north within about a quarter of the ecosystem. Hence the rate of carcass production during the late dry season would amount to around 5000 kg/km2 locally, equivalent to 3 wildebeest-sized carcasses per km2 per week within the dry season range. A practical exploration of the carcass remains available to hominin scavengers that was undertaken in the northern Serengeti woodlands during the mid-dry season yielded five carcasses of animals killed by lions or found dead within a travel distance effectively representing about 10 days of searching, i.e. about one every second day.49 Two injured or sick animals were also encountered and could have been dispatched. Based on these projections, it seems that the production of large herbivore carcasses could indeed constitute an economically exploitable resource for hominins through the critical dry-season months in parts of the Serengeti ecosystem. Back in the Pliocene, the larger herbivore fauna would have been different, with a greater contribution from very large herbivores and less from smaller ones. This implies that the total herbivore biomass at that time would have been greater than at present, but with less relative turnover of this biomass through mortality. Comparable seasonal concentrations of ungulates also occurred in parts of the Eastern Rift Valley historically.50 Water limitations would have drawn local concentrations of ungulates more widely through Africa.
Kruger NP in South Africa supports only about half of the herbivore biomass found in Serengeti (Figure 13.1), most of this in the form of elephants and other megaherbivores rarely killed by lions. From herbivore population totals and mortality rates recorded in Kruger NP, potential food for lions, represented by carcasses of potential prey animals dying annually, amounts to 100–150 kg/km2, equivalent to one wildebeest-sized carcass per km2 per year.51 However, most of this mortality is incurred during the dry season when mobile grazers are confined to the proximity of perennial water sources. This raises the local rate of carcass production at least 10-fold, to 10 or more wildebeest equivalents through the last 3 months of the dry season, or one carcass per week within each square kilometre.
Scavenging for marrow and meat would initially have been a fallback response to enable survival through the critical dry-season months when little plant food remains and what remains is mostly of low nutritional value. It was viable because of the locally high biomass of large herbivores sustained by fertile volcanic soils and the seasonal concentrations of grazers near water during the dry season. Furthermore, the bones of the large ungulates that predominated in the Pliocene would have contained more marrow than those of the smaller antelope found today. Scavenging opportunities during the wet season would have been meagre, because carnivore kills during that time of the year are mostly of young animals that get consumed completely. Hominins would have been dependent largely on plant food during this time of the year.
Scavenging for marrow and flesh from carcasses would have had ramifying consequences. The broad, flat-crowned molars of the australopiths had become adapted for chewing tough plants, not macerating raw meat. Early Homo initially retained quite large mandibles, but showed a progressive reduction in surface area of its molar teeth and in the thickness of the dental enamel through time. Its dental features became adapted to handle food with a wide range of fracture properties, potentially including bone marrow and flesh.34,52 No specially worked tools were needed to break open bones to get at the marrow, merely large hammerstones.53 The fatty tissue obtained from within long bones and inside skulls would have been especially valuable as an energy source to balance the protein provided by the scraps of meat that remained on carcasses.54 The dental needs for chewing marrow and fragments of meat were less demanding than those required to macerate plant storage organs, reversing the trends towards larger jaws and molar teeth that produced the robust-jawed ape-men.
A further adaptation, not preserved in fossils, was crucial to make scavenging a viable niche for these ape-men. To enable foraging excursions to be carried out during the heat of midday, when hyenas were back in their dens and the big cats were sleepy, a reduction in body hair was necessary to allow sweating to counteract body heat build-up.
Upright walking frees hands to carry bones and other carcass pickings back to secure sites, plus of course also fruits and tubers, but the location of carcass remains would have differed from the places where plant products were most readily gathered. This situation would have promoted a division of labour between males, taking on the danger of confronting carnivores still lurking near carcasses, and females plus their offspring, choosing less-risky places to gather fruits, seeds and roots. Males would need to be in groups to detect carnivores and deter attacks, while females would need to move in groups to be secure. A shared home base would be required to exchange fruits, bones and meat obtained. This central base would need to be located in woodland patches providing trees for shade and for nocturnal sleeping platforms. It would also need to be within walking distance of year-round surface water, and therefore amid dry-season concentrations of water-dependent ungulates.
This is the ecologically consilient scenario that I propose for the trophic divergence of the lineage leading to Homo from that ending in Paranthropus, taking place during the Pliocene/Pleistocene transition. Making a living as a facultative scavenger was crucially dependent on a sufficiency of large herbivore carcasses to provide sustenance through intensifying dry seasons.
Becoming a Hunter
The amount of food obtained by scavenging is somewhat meagre for the energy invested, although essential as a supplement enabling ancestral humans to survive through the dry seasons. Could not animals be dispatched before they died from whatever cause? There would surely have been opportunities to do so during severe droughts, when starving herbivores may exceed the consumption capacity of large carnivores.55 Sharp sticks and big rocks might be sufficient to kill these weakened animals. But how could animal flesh be obtained more reliably over a wider portion of the year? How could ungulates able to outrun hyenas and wild dogs be captured?
The pre-adaptations facilitating the transition from scavenging to hunting were those enabling endurance running capabilities.56 Lengthened legs and bared skin allowed scavenging excursions to take place during the heat of midday when big cats were lethargic and hyenas had not yet arrived to clean up bones and remaining flesh. With a bit of coordination among group companions, early humans equipped with these features could succeed in chasing down living ungulates by persistently running after them until the targeted animal reached potentially lethal levels of over heating, particularly during midday heat that sparsely hairy hominins could better tolerate (Figure 17.5). Soils bared of much grass during the dry season would permit them to follow the tracks of selected animals until these herbivores came to a standstill. Anatomical adaptations in the shoulder region of early Homo became evident around 2.0 Ma, which would assist in the launching of projectiles, probably made from wood, at high speed.57 At close quarters, these primitive spears could be driven through ribs into vital tissues to dispatch animals that could run no more. If females lacking horns were chosen to chase, there would be little risk of injury to the hunters at this final stage. Hunting in this fashion would have been productive particularly under dry-season conditions when herbivores become weakened and grazers concentrate near remaining water sources. This does not preclude ambushing ungulates from the cover provided by termite mounds or tree clumps alongside trails.58 These conditions enabled relatively puny upright primates, lacking the teeth, claws and muscle power of true carnivores, to become effective cursorial hunters.
Figure 17.5
The transition to hunting by Homo ergaster. (A) Chasing after an antelope around midday, enabled by bare skin facilitating cooling by sweating; (B) thrusting spears to bring about the death of the antelope once it can run no further due to overheating.
(original artwork by Marco Anson)
The composition of H. habilis diets in eastern Africa estimated from stable carbon isotope ratios in tooth enamel indicated 25–50 percent to be of C4 plant origin.34,36 Because grass seeds and leaves would not provide adequate food for these large omnivores, most of this isotopic signal probably came from tissues of large grazers they had scavenged or, at a later stage, killed.42,59 A diet consisting almost solely of plant resources eventually failed to suffice for the robust-jawed ape-men, which dropped out of the fossil record after ~1.4 Ma in eastern Africa. The capacity of early Homo to exploit animal flesh as a dry-season fallback surely contributed crucially to their persistence.
Whether early humans hunted or scavenged is revealed by whether cut marks on bones overlay tooth marks from carnivores, or vice versa, as well as the kinds of bones assembled and the age profiles of the ungulates represented.60,61 Butchery marks on bones associated with Oldowan tools at Olduvai dated 1.84 Ma suggest that smaller ungulates had primarily been hunted, whereas larger species were either hunted or scavenged.62,63 Subsequent bone assemblages show a high frequency of cut marks and other signs indicating prior access by early humans rather than carnivores, and thus that the animals had mostly been hunted.59,64,65 In addition, marrow had apparently been extracted from the large limb bones of elephants, rhinos and hippos unlikely to have been killed by the early humans.66 Further evidence of the butchery of large vertebrates comes from Swartkrans Cave in South Africa’s Cradle of Humankind dated ~2.0 Ma.67,68 Where the ungulate species were identified, they mostly showed a predominance of mainly medium to large grazers.69,70,71 A site at Olduvai where ungulates as large as giant buffalo and short-necked giraffe had been butchered evidently represented circumstances where these animals had been trapped in mud.72
Sites in the Afar region of Ethiopia dated 2.6–2.1 Ma have yielded limb bones showing cut marks interpreted as signs of butchery by humans, although whether these were products of scavenging or hunting could not be firmly established.73,74 Cut and percussion marks from Dikika in Ethiopia dated much earlier at 3.4 Ma75 are controversial because these marks could have been imposed by crocodiles.76 No fossil sites exist spanning the period between 2.8 Ma, when the first humans appeared, and 1.9 Ma, when H. ergaster emerged, retain adequate bone preservation to indicate whether human rather than carnivore damage was primary.
Increased dependence on hunting would have accentuated the division in food procurement between hunting by males and foraging for plant products primarily by females plus young. Food gathered by each sex would need to be carried back to the home base to be shared at least within families. Signs of a central gathering place where worked bones and stone artefacts accumulated are evident at Olduvai in layers dated ~1.8 Ma.77 More effective communication would be needed to plan foraging excursions, based on recent or longer experience. The extra social competence required must have contributed to the expansion in cranial capacity from H. habilis to H. ergaster. However, fossils continued to be assigned to H. habilis contemporaneous with H. ergaster, until ~1.4 Ma.7,78 Whether the morphological distinctions between them indicate ecological segregation or a polytypic species will be addressed in Chapter 19.
Evading Predation
The australopiths retained arboreal competence in climbing, as shown by hand and foot bones, coupled with more effective terrestrial locomotion. This meant that they could readily ascend trees at night to gain sufficient security from predation by large cats and hyenas. Both chimpanzees and gorillas routinely spend time constructing new nests in trees around sunset each night. Only mature male gorillas, but neither females nor young, dare to doze at ground level during darkness. All other primates, apart from modern humans, restrict their vulnerability to predation by ascending trees or cliff faces at night.
Arboreal capabilities became compromised with the emergence of H. ergaster, generally bigger in height and weight and with relatively longer legs than its predecessor, H. habilis. Although modern humans can still climb trees when confronted by lions, we do not ascend very adeptly compared with other primates. During my white rhino study, I experienced the discomfort of being perched in a tree beside a waterhole to observe what animals came down to drink during the night. After squirming there for a few hours, I abandoned this quest and walked back to camp through the darkness despite the danger. Of course, the early hominins would have constructed some form of platform upon which to sleep, whether nightly or permanently can only be guessed. But an essential requirement was trees sufficiently tall, yet still climbable, to elevate them beyond the reach of lions and leopards. This would have restricted their habitat occupation to river margins where such big trees grow.
The metabolic resources needed to grow larger brains delay reproductive maturity and perhaps restrict how much energy is available for digestive processes.79,80 Dental eruption patterns plus cementum lines show how the life-history stages of hominins became prolonged as brain size expanded.81 The age when females first gave birth was retarded from 14 years among chimpanzees to between 18 and 20 years, as shown by women living as modern hunter-gatherers.82 In compensation, humans extend their reproductive period by living much longer than any other primate, and even than elephants. Furthermore, human females cease reproducing at menopause around 40–45 years of age, two or more decades before they die. Other large mammals keep reproducing until the end of their life.
To counteract their reduced reproductive period, women in modern hunter-gatherer societies exhibit a 2–3-year inter-birth interval, shorter than that shown by both chimpanzees and gorillas. The survival of human females beyond the age at which they cease contributing offspring has been ascribed to the substantial benefits provided by grandmothers.83,84 Rather than raising their own offspring, older females shift their nurturing contributions towards the progeny of their daughters, alleviating the costs incurred by younger females arising from the briefer inter-birth interval.
The age at which reproductive maturity is attained, coupled with maximum longevity, determine the minimal mortality loss that can be sustained by the adult segment of the population. For human hunter-gatherers maturing at 20 years and living beyond 60 years of age, this minimal adult mortality is 2 percent annually. Their relatively short inter-birth interval allows human mothers to produce potentially 8–10 offspring between 20 and 40 years of age, exceeding the seven offspring that chimpanzee mothers contribute during a reproductive lifespan enduring nearly twice as long. This means that human populations can support greater mortality among offspring prior to their incorporation into the adult segment than chimpanzees can.
The population growth rate that could be achieved is restricted by mortality taking place during the adult stage. Annual mortality rates recorded for modern human hunter-gatherers82 prevent population growth from much exceeding 3 percent per year (Table 17.1). In order for populations to be maintained, predation rates on adult hominins must be half as great as the mortality losses incurred by chimpanzees living in forested regions, despite occupying savanna environments thronged with large ungulates and associated carnivores.85
Table 17.1Life-history parameters for growing and stable populations of humans, chimpanzees, elephants and white rhinos. For human hunter-gatherers,82 elephants and white rhinos, values from near-maximally growing populations were adjusted to obtain a likely combination generating zero population growth. For chimpanzees, values derived from a stable population in Kibale Forest, Uganda were adjusted to generate near-maximum population growth. Kudu data are mine. For humans, reproduction terminates at the age of senescence, while for other species reproduction continues at a reduced rate until maximum longevity is reached.
Large ungulates spending every night exposed to predation on the ground, but with sharp senses and honed running capabilities, incur annual mortality rates among prime-aged females amounting to 8 percent or more annually (Chapter 12).86 How might early humans too big to be secure perched in trees have restricted their adult mortality rate to less than a third of this?
Early humans would have been especially vulnerable to predation in two circumstances: (1) while foraging for left-overs from carcasses not yet abandoned by large carnivores, or when protecting carcasses of their own kills, and (2) while sleeping during the night, once their competence in tree climbing had become compromised in favour of walking. Risks of predation during daylight are not that great. The most threatening carnivores, i.e. lions and leopards, are most active nocturnally, and so probably were sabretooth cats and hunting hyenas. During the 3.5 years I spent wandering on foot after rhinos in the Mfolozi GR, I was never directly threatened by a carnivore on any of the occasions when I met one. Scientists studying baboons spend countless days on foot among troops, without any of them being injured or killed by a predator, so far as I know. Modern hunter-gatherers like the San and Hadza seldom fall prey to lions, leopards or hyenas, despite commonly sleeping outside the protection of huts at night (see Chapter 18).
Risks are greatly elevated at night. Human refugees from Mozambique traversing Kruger NP to enter South Africa, and forced to sleep out overnight during the journey, were all too frequently eaten by lions. When other prey runs short, lions may switch their hunting to humans.87 How did members of H. ergaster bands avoid being killed by lions or leopards during the hours of darkness? Did they construct durable sleeping platforms in trees at each temporarily occupied home base? Or were they able instead to build impenetrable barriers of thorny branches around overnight abodes at ground level each night? Notably, fossils ascribed to Au. sediba retained long curved fingers and wrist bones that would aid arboreal climbing. Specimens assigned to H. habilis also had long arms that would facilitate climbing. The robust-jawed Paranthropus also retained greater adaptive competence for tree-climbing than that shown by H. ergaster.
Carnivores sneaking up at night could be deterred by throwing rocks at them; but it would help to know where to aim. Could these earliest humans have had the benefit of campfires to illuminate the darkness? The contentious issue I am raising is whether the active deployment of fire to light the darkness, render meat and tough plant parts chewable, and keep sufficiently warm in the absence of much fur, helped foster the emergence of Homo ergaster after 1.8 Ma, despite the lack of much evidence for the use of fire until thousands of years later.88,89,90
The earliest evidence claimed to show the deployment of fire comes from burnt bones found in Swartkrans Cave in South Africa91 and from baked surfaces of volcanic soils associated with stone tools in northern Kenya,92 both dated ~1.6 Ma.93 Burnt bones have also been recorded at Koobi Fora near Lake Turkana dated around 1.5 Ma. The earliest evidence of fire used for cooking in hearths is in Wonderwerk Cave in the Northern Cape of South Africa, dated to ~1 Ma,94 and from numerous sites in Eurasia from around the same time.93 Most likely, debris from open-air fires would be indistinct from that left by the grassland fires that recur within savannas. Lightning-ignited fires would have presented opportunities to transport smouldering logs back to home bases. Over time, humans should have learnt how to ignite fires by rotating sticks within cavities drilled in soft wood, even during the wet season when wood is mostly wet.
Overview
The ecologically compatible narrative covering the transition from frugivorous forest-dwelling ape to partially meat-eating, savanna-inhabiting human takes this form. The initial adaptive changes shown by evolving hominins in response to expanding savanna vegetation during the late Miocene were towards bipedal locomotion. Primates occupying savannas needed to walk further to cope with the widened spacing between trees and seasonally restricted production of fruits and young leaves on these trees. This also freed hands for carrying resistant plant parts to secure places where they could be processed for consumption.
Following closely in time were dental adaptations for coping with tough plant parts sought underground between the trees once fruits were no longer available year-round. Molar teeth for chewing expanded in surface area while incisor teeth used for biting into fruits became reduced. This adaptive trend, initiated during the Pliocene, ultimately culminated in the robust-jawed ape-men around the start of the Pleistocene. They continued to exist for well over a million years, disappearing later in southern Africa than recorded in eastern Africa. Hence falling back on tough plant parts for bridging dry-season shortages eventually faded as a viable niche, except among baboons and rodents able to get by on lesser amounts of food.
Around the commencement of the Pleistocene ice ages, a diverging lineage reversed the trend towards greater dental robustness by adding marrow-containing bones scavenged from carnivore kills to its diet, promoting greater dietary versatility. While leaves contract in edibility and fruits in availability during the dry season, carcasses of herbivores killed or dying of starvation are concentrated during this lean period. Furthermore, a temporal window could be exploited around midday when heat inhibited predator activity. Hyenas had gone to dens and the big cats had ceased feeding, or at least defending what remained of their kills. Consequently, emerging humans incurred a reduction in hair cover over most of the body except on top of the head, facilitating evaporative cooling. Enlarging brains and lengthening legs supported the transition from ape-men to earliest humans. Multi-mode foraging favoured the expansion in brain size to cope with the organisational complexity. When and how these adaptive shifts took place during the period between 2.9 and 1.8 Ma, spanning the climatic transition into the early Pleistocene, remains obscure.
These adaptations for scavenging opened a new window of opportunity, leading early humans to become superior to any ungulate in endurance running capabilities. The latter remained handicapped by their fur cover and resultant over heating. Scavenging became augmented by active hunting of increasingly large prey, enabling greater reliability in food procurement through the dry season. However, lengthened legs and larger body size handicapped tree-climbing capabilities and thereby safety from predators. It seems that the deployment of fire became necessary around this time to deter predators, as well as providing warmth and tenderising meat and plant tubers.
The ecological circumstances that enabled hominins to become scavengers on animal tissues and later function as hunters were (1) high abundance of large mammalian herbivores, found especially in dry/eutrophic savannas in semi-arid regions adjoining the African rift valleys where volcanic influences are pervasive; (2) predominance of medium to large grazers in these faunal assemblages, providing bones of manageable size for carrying back from kills; (3) restricted surface water sources, generating concentrations of water-dependent grazers during the dry season when plant foods are most deficient in their availability; (4) thermal tolerance, enabling temporal partitioning from scavenging hyenas; and (5) endurance running capabilities, enabling humans to chase more densely furry ungulates to a standstill. Still unresolved is the stage at which fire became deployed, crucially not only for cooking but also to illuminate lurking carnivores. The fossil dating and ecological contexts seem consistent with the evolutionary divergence of the lineage leading to Homo taking place earliest in eastern Africa and dispersing southward from there to form sister-species in South Africa.
This transition from obligate rhizophage to facultative meat-eater was both necessary and opportunistic: necessary for survival through dry seasons, without specialised chewing and digestive adaptations; and opportunistic, exploiting the concentrations of large grazing ungulates that developed around remaining water sources during the late dry season. This lifestyle enabled H. ergaster to persist with only minor changes in adaptive morphology for around a million years, from 1.9 to 0.9 Ma, before the surge in brain capacity into our immediate human predecessors took place. While features of bones and teeth changed little, important adaptive changes were taking place in the artefacts supporting this hunting and gathering lifestyle. This cultural evolution will be the subject of the chapter that follows.
SUGGESTED FURTHER READING
Klein, RG. (2009) The Human Career: Human Biological and Cultural Origins, 3rd ed. University of Chicago Press, Chicago.
Thompson, JC, et al. (2019) Origins of the human predatory pattern: the transition to large-animal exploitation by early humans. Current Anthropology 60:1–23.
Wood, B; Leakey, M. (2011) The Omo–Turkana basin fossil hominins and their contribution to our understanding of human evolution in Africa. Evolutionary Anthropology 20:264–292.
REFERENCES
1.MacLatchy, LM. (2010) Hominini. In Werdelin, L; Sanders, WJ (eds) Cenozoic Mammals of Africa. University of California Press, Berkeley, pp. 471–540.
2.Bobe, R, et al. (2020) The ecology of Australopithecus anamensis in the early Pliocene of Kanapoi, Kenya. Journal of Human Evolution 140:102717.
3.Wynn, JG. (2000) Paleosols, stable carbon isotopes, and paleoenvironmental interpretation of Kanapoi, Northern Kenya. Journal of Human Evolution 39:411–432.
4.Reed, KE. (2008) Paleoecological patterns at the Hadar hominin site, Afar regional state, Ethiopia. Journal of Human Evolution 54:743–768.
5.Sponheimer, M, et al. (2013) Isotopic evidence of early hominin diets. Proceedings of the National Academy of Sciences of the United States of America 110:10513–10518.
6.Wood, B; Leakey, M. (2011) The Omo–Turkana Basin fossil hominins and their contribution to our understanding of human evolution in Africa. Evolutionary Anthropology: Issues, News, and Reviews 20:264–292.
7.Bobe, R; Carvalho, S. (2019) Hominin diversity and high environmental variability in the Okote Member, Koobi Fora Formation, Kenya. Journal of Human Evolution 126:91–105.
8.Clarke, RJ; Kuman, K. (2019) The skull of StW 573, a 3.67 Ma Australopithecus prometheus skeleton from Sterkfontein caves, South Africa. Journal of Human Evolution 134:102634.
9.Crompton, RH, et al. (2018) Functional anatomy, biomechanical performance capabilities and potential niche of StW 573: an Australopithecus skeleton (circa 3.67 Ma) from Sterkfontein Member 2, and its significance for the last common ancestor of the African apes and for Hominin origins. bioRxiv:481556.
10.Pickering, R, et al. (2019) U–Pb-dated flowstones restrict South African early hominin record to dry climate phases. Nature 565:226–229.
11.Berger, LR, et al. (2010) Australopithecus sediba: a new species of Homo-like australopith from South Africa. Science 328:195–204.
12.de Ruiter, DJ, et al. (2017) Late australopiths and the emergence of Homo. Annual Review of Anthropology 46:99–115.
13.Villmoare, B, et al. (2015) Early Homo at 2.8 Ma from Ledi-Geraru, Afar, Ethiopia. Science 347:1352–1355.
14.DiMaggio, EN, et al. (2015) Late Pliocene fossiliferous sedimentary record and the environmental context of early Homo from Afar, Ethiopia. Science 347:1355–1359.
15.Robinson, JR; Rowan, J. (2017) Holocene paleoenvironmental change in southeastern Africa (Makwe Rockshelter, Zambia): implications for the spread of pastoralism. Quaternary Science Reviews 156:57–68.
16.Bennett, MR, et al. (2009) Early hominin foot morphology based on 1.5-million-year-old footprints from Ileret, Kenya. Science 323:1197–1201.
17.Antón, SC, et al. (2014) Evolution of early Homo: an integrated biological perspective. Science 345:1236828.
18.Herries, AIR, et al. (2020) Contemporaneity of Australopithecus, Paranthropus, and early Homo erectus in South Africa. Science 368:eaaw7293.
19.Teaford, MF; Ungar, PS. (2000) Diet and the evolution of the earliest human ancestors. Proceedings of the National Academy of Sciences of the United States of America 97:13506–13511.
20.Maslin, M. (2016) The Cradle of Humanity: How the Changing Landscape of Africa Made Us So Smart. Oxford University Press, Oxford.
21.Stringer, C. (2016) The origin and evolution of Homo sapiens. Philosophical Transactions of the Royal Society B: Biological Sciences 371:20150237.
22.Hublin, J-J, et al. (2017) New fossils from Jebel Irhoud, Morocco and the pan-African origin of Homo sapiens. Nature 546:289–292.
23.Grün, R, et al. (2020) Dating the skull from Broken Hill, Zambia, and its position in human evolution. Nature 580:372–375.
24.Rightmire, GP. (1983) The Lake Ndutu cranium and early Homo sapiens in Africa. American Journal of Physical Anthropology 61:245–254.
25.Dirks, PHGM, et al. (2017) The age of Homo naledi and associated sediments in the Rising Star Cave, South Africa. Elife 6:e24231.
26.Berthaume, MA, et al. (2018) Dental topography and the diet of Homo naledi. Journal of Human Evolution 118:14–26.
27.Owen-Smith, N. (1979) Assessing the foraging efficiency of a large herbivore, the kudu. South African Journal of Wildlife Research 9:102–110.
28.Owen-Smith, RN. (2002) Adaptive Herbivore Ecology: From Resources to Populations in Variable Environments. Cambridge University Press, Cambridge.
29.Owen‐Smith, N; Cooper, SM. (1989) Nutritional ecology of a browsing ruminant, the kudu (Tragelaphus strepsiceros), through the seasonal cycle. Journal of Zoology 219:29–43.
30.Laden, G; Wrangham, R. (2005) The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. Journal of Human Evolution 49:482–498.
31.Marean, CW. (1997) Hunter–gatherer foraging strategies in tropical grasslands: model building and testing in the East African Middle and Later Stone Age. Journal of Anthropological Archaeology 16:189–225.
32.O’Brien, EM; Peters, CR. (1999) Landforms, climate, ecogeographic mosaics, and the potential for hominid diversity in Pliocene Africa. In Bromage, TG; Schrenk, F (eds) African Biogeography, Climate Change and Human Evolution. Oxford University Press, Oxford, pp. 115–137.
33.Ungar, PS; Sponheimer, M. (2011) The diets of early hominins. Science 334:190–193.
34.Ungar, PS. (2012) Dental evidence for the reconstruction of diet in African early Homo. Current Anthropology 53:S318–S329.
35.Sponheimer, M; Lee-Thorp, JA. (2003) Differential resource utilization by extant great apes and australopithecines: towards solving the C4 conundrum. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 136:27–34.
36.Van der Merwe, NJ, et al. (2008) Isotopic evidence for contrasting diets of early hominins Homo habilis and Australopithecus boisei of Tanzania. South African Journal of Science 104:153–155.
37.Scott, RS, et al. (2005) Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436:693–695.
38.Dominy, NJ, et al. (2008) Mechanical properties of plant underground storage organs and implications for dietary models of early hominins. Evolutionary Biology 35:159–175.
39.Sponheimer, M; Lee-Thorp, JA. (1999) Oxygen isotopes in enamel carbonate and their ecological significance. Journal of Archaeological Science 26:723–728.
40.Sponheimer, M, et al. (2006) Isotopic evidence for dietary variability in the early hominin Paranthropus robustus. Science 314:980–982.
41.Henry, AG, et al. (2012) The diet of Australopithecus sediba. Nature 487:90–93.
42.Patterson, DB, et al. (2019) Comparative isotopic evidence from East Turkana supports a dietary shift within the genus Homo. Nature Ecology & Evolution 3:1048–1056.
43.Gibbon, RJ, et al. (2014) Cosmogenic nuclide burial dating of hominin-bearing Pleistocene cave deposits at Swartkrans, South Africa. Quaternary Geochronology 24:10–15.
44.Blumenschine, RJ, et al. (1987) Characteristics of an early hominid scavenging niche [and comments and reply]. Current Anthropology 28:383–407.
45.Blumenschine, RJ; Cavallo, JA. (1992) Scavenging and human evolution. Scientific American 267:90–97.
46.Domínguez-Rodrigo, M. (2001) A study of carnivore competition in riparian and open habitats of modern savannas and its implications for hominid behavioral modelling. Journal of Human Evolution 40:77–98.
47.Houston, DC. (1979) The adaptations of scavengers. In Sinclair, ARE; Norton-Griffiths, M (eds) Serengeti: Dynamics of an Ecosystem. University of Chicago Press, Chicago, pp. 263–286.
48.Mills, MGL. (1990) Kalahari Hyaenas. Unwin Hyman, London.
49.Schaller, GB; Lowther, GR. (1969) The relevance of carnivore behavior to the study of early hominids. Southwestern Journal of Anthropology 25:307–341.
50.Ogutu, JO, et al. (2012) Dynamics of ungulates in relation to climatic and land use changes in an insularized African savanna ecosystem. Biodiversity and Conservation 21:1033–1053.
51.Owen-Smith, N; Mills, MGL. (2006) Manifold interactive influences on the population dynamics of a multispecies ungulate assemblage. Ecological Monographs 76:73–92.
52.Teaford, MF, et al. (2002) Paleontological evidence for the diets of African Plio-Pleistocene hominins with special reference to early Homo. In Ungar, PS; Teaford, MF (eds) Human Diet: Its Origin and Evolution. Bergin & Garvey, Westport, pp. 143–166.
53.Thompson, JC, et al. (2019) Origins of the human predatory pattern: the transition to large-animal exploitation by early hominins. Current Anthropology 60:1–23.
54.Pobiner, BL. (2020) The zooarchaeology and paleoecology of early hominin scavenging. Evolutionary Anthropology: Issues, News, and Reviews 29:68–82.
55.Cooper, SM, et al. (1999) A seasonal feast: long‐term analysis of feeding behaviour in the spotted hyaena (Crocuta crocuta). African Journal of Ecology 37:149–160.
56.Bramble, DM; Lieberman, DE. (2004) Endurance running and the evolution of Homo. Nature 432:345–352.
57.Roach, NT, et al. (2013) Elastic energy storage in the shoulder and the evolution of high-speed throwing in Homo. Nature 498:483–486.
58.Bunn, HT; Gurtov, AN. (2014) Prey mortality profiles indicate that Early Pleistocene Homo at Olduvai was an ambush predator. Quaternary International 322:44–53.
59.Domínguez-Rodrigo, M, et al. (2014) On meat eating and human evolution: a taphonomic analysis of BK4b (Upper Bed II, Olduvai Gorge, Tanzania), and its bearing on hominin megafaunal consumption. Quaternary International 322:129–152.
60.Domínguez-Rodrigo, M. (2002) Hunting and scavenging by early humans: the state of the debate. Journal of World Prehistory 16:1–54.
61.Domínguez‐Rodrigo, M; Pickering, TR. (2003) Early hominid hunting and scavenging: a zooarcheological review. Evolutionary Anthropology: Issues, News, and Reviews 12:275–282.
62.Parkinson, JA. (2018) Revisiting the hunting-versus-scavenging debate at FLK Zinj: a GIS spatial analysis of bone surface modifications produced by hominins and carnivores in the FLK 22 assemblage, Olduvai Gorge, Tanzania. Palaeogeography, Palaeoclimatology, Palaeoecology 511:29–51.
63.Pante, MC, et al. (2018) The carnivorous feeding behavior of early Homo at HWK EE, Bed II, Olduvai Gorge, Tanzania. Journal of Human Evolution 120:215–235.
64.Pobiner, BL, et al. (2008) New evidence for hominin carcass processing strategies at 1.5 Ma, Koobi Fora, Kenya. Journal of Human Evolution 55:103–130.
65.Oliver, JS, et al. (2019) Bovid mortality patterns from Kanjera South, Homa Peninsula, Kenya and FLK-Zinj, Olduvai Gorge, Tanzania: evidence for habitat mediated variability in Oldowan hominin hunting and scavenging behavior. Journal of Human Evolution 131:61–75.
66.Organista, E, et al. (2019) Taphonomic analysis of the level 3b fauna at BK, Olduvai Gorge. Quaternary International 526:116–128.
67.Pickering, TR, et al. (2008) Testing the ‘shift in the balance of power’ hypothesis at Swartkrans, South Africa: hominid cave use and subsistence behavior in the Early Pleistocene. Journal of Anthropological Archaeology 27:30–45.
68.Kuman, K, et al. (2018) The Oldowan industry from Swartkrans cave, South Africa, and its relevance for the African Oldowan. Journal of Human Evolution 123:52–69.
69.Ferraro, JV, et al. (2013) Earliest archeological evidence of persistent hominin carnivory. PLoS One 8:e62174.
70.Patterson, DB, et al. (2017) Ecosystem evolution and hominin paleobiology at East Turkana, northern Kenya between 2.0 and 1.4 Ma. Palaeogeography, Palaeoclimatology, Palaeoecology 481:1–13.
71.Van Pletzen-Vos, L, et al. (2019) Revisiting Klasies River: a report on the large mammal remains from the Deacon excavations of Klasies River main site, South Africa. South African Archaeological Bulletin 74:127–137.
72.Organista, E, et al. (2016) Did Homo erectus kill a Pelorovis herd at BK (Olduvai Gorge)? A taphonomic study of BK5. Archaeological and Anthropological Sciences 8:601–624.
73.De Heinzelin, J, et al. (1999) Environment and behavior of 2.5-million-year-old Bouri hominids. Science 284:625–629.
74.Domínguez-Rodrigo, M, et al. (2005) Cutmarked bones from Pliocene archaeological sites at Gona, Afar, Ethiopia: implications for the function of the world’s oldest stone tools. Journal of Human Evolution 48:109–121.
75.McPherron, SP, et al. (2010) Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia. Nature 466:857–860.
76.Sahle, Y, et al. (2017) Hominid butchers and biting crocodiles in the African Plio–Pleistocene. Proceedings of the National Academy of Sciences of the United States of America 114:13164–13169.
77.Dominguez-Rodrigo, M. (2009) Are all Oldowan sites palimpsests? If so, what can they tell us about hominin carnivory? In Hovers, E; Braun, DR (eds) Interdisciplinary Approaches to the Oldowan. Springer, Berlin, pp. 129–147.
78.Antón, SC; Snodgrass, J. (2012) Origins and evolution of genus Homo: new perspectives. Current Anthropology 53:S479–S496.
79.Aiello, LC; Wheeler, P. (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Current Anthropology 36:199–221.
80.Isler, K; van Schaik, CP. (2009) The expensive brain: a framework for explaining evolutionary changes in brain size. Journal of Human Evolution 57:392–400.
81.Schwartz, GT. (2012) Growth, development, and life history throughout the evolution of Homo. Current Anthropology 53:S395–S408.
82.Kaplan, H, et al. (2000) A theory of human life history evolution: diet, intelligence, and longevity. Evolutionary Anthropology: Issues, News, and Reviews 9:156–185.
83.Hawkes, K, et al. (1998) Grandmothering, menopause, and the evolution of human life histories. Proceedings of the National Academy of Sciences of the United States of America 95:1336–1339.
84.Hawkes, K, et al. (2003) Human life histories: primate tradeoffs, grandmothering socioecology, and the fossil record. In Kappela, P; Pereira, ME (eds) Primate Life Histories and Socioecology. University of Chicago Press, Chicago, pp. 204–227.
85.Meindl, RS, et al. (2018) Early hominids may have been weed species. Proceedings of the National Academy of Sciences of the United States of America 115:1244–1249.
86.Owen‐Smith, N, et al. (2005) Correlates of survival rates for 10 African ungulate populations: density, rainfall and predation. Journal of Animal Ecology 74:774–788.
87.Packer, C, et al. (2011) Fear of darkness, the full moon and the nocturnal ecology of African lions. PLoS One 6:e22285.
88.Wrangham, RW, et al. (1999) The raw and the stolen: cooking and the ecology of human origins. Current Anthropology 40:567–594.
89.Wrangham, R. (2017) Control of fire in the Paleolithic: evaluating the cooking hypothesis. Current Anthropology 58:S303–S313.
90.Hlubik, S, et al. (2019) Hominin fire use in the Okote member at Koobi Fora, Kenya: new evidence for the old debate. Journal of Human Evolution 133:214–229.
91.Brain, CK; Sillent, A. (1988) Evidence from the Swartkrans cave for the earliest use of fire. Nature 336:464–466.
92.Bellomo, RV. (1994) Methods of determining early hominid behavioral activities associated with the controlled use of fire at FxJj 20 Main, Koobi Fora, Kenva. Journal of Human Evolution 27:173–195.
93.Gowlett, JAJ. (2016) The discovery of fire by humans: a long and convoluted process. Philosophical Transactions of the Royal Society B: Biological Sciences 371:20150164.
94.Berna, F, et al. (2012) Microstratigraphic evidence of in situ fire in the Acheulean strata of Wonderwerk Cave, Northern Cape province, South Africa. Proceedings of the National Academy of Sciences of the United States of America 109:E1215–E1220.