Scavenging by chimpanzees at Ngogo and the relevance of chimpanzee scavenging to early hominin behavioral ecology

Chimpanzees regularly hunt a variety of prey species. However, they rarely scavenge, which distinguishes chimpanzee carnivory from that of some modern hunter-gatherers and, presumably, at least some Plio-Pleistocene hominins. I use observations made over an 11-year period to document all known opportunities for scavenging encountered by chimpanzees at Ngogo, Kibale National Park, Uganda, and describe all cases of scavenging. I also review data on scavenging from other chimpanzee research sites. Chimpanzees at Ngogo encountered scavenging opportunities only about once per 100 days and ate meat from scavenged carcasses only four times. Scavenging opportunities are also rare at other sites, even where leopards are present (Mahale, Ta?, Gombe), and scavenging of leopard kills is known only from Mahale. Feeding on prey that chimpanzees had hunted but then abandoned is the most common form of scavenging reported across study sites. For example, several individuals at Ngogo ate meat from a partially consumed red colobus carcass abandoned after a hunt the previous day. Such behavior probably was not common among Oldowan hominins. Ngogo data and those from other sites also show that chimpanzees sometimes eat meat from carcasses of prey that they did not see killed and that were not killed by chimpanzees, and that scavenging allows access to carcasses larger than those of any prey items. However, chimpanzees ignore relatively many opportunities to obtain meat from such carcasses. Scavenging may be rare because fresh carcasses are rare, because the risk of bacterial infections and zoonoses is high, and because chimpanzees may not recognize certain species as potential prey or certain size classes of prey species as food sources. Its minimal nutritional importance, along with the absence of technology to facilitate confrontational scavenging and rapid carcass processing, apparently distinguishes chimpanzee foraging strategies from those of at least some Oldowan hominins.     

The evolution of culture: New perspectives and evidence

This and the next issue of Evolutionary Anthropology are devoted to presenting the most recent advances in our understanding of the evolution of culture in non‐human primates and humans. This effort was stimulated in part by the recent explosion of comparative evidence for extensive communicative and material culture in two great apes, chimpanzees 1 and orangutans. 2 Before this evidence accumulated, it was easy for anthropologists to maintain that examples of non‐human primate culture were little more impressive than those put forward for many other non‐human species, and thus they could leave intact the seemingly huge gap between animal and human culture. The overall purpose of this special pair of issues of Evolutionary Anthropology is to ask how and why culture has changed over evolutionary time from non‐primates to non‐human primates to early hominins to modern humans.     

On the ecological scenario of the first hominin dispersal out of Africa

The archaeopaleontological site of Dmanisi in Georgia, dated to ～1.8 Ma, provides evidence on the first hominin dispersal out of Africa, while the sites of Barranco León and Fuente Nueva-3 in Spain, dated to ～1.4 Ma, record the earliest hominin settlements in Europe. However, a number of issues related to the dispersal route, the climatic conditions and the ecological scenario of this dispersal event are subject to debate. In a recent paper in L’anthropologie, Agustí and Lordkipanidze (2019) proposed an alternative scenario for the arrival of hominins in the Caucasus, which they conceived as a forest refugium area during the Early Pleistocene, and discarded that their dispersal coincided with that of other members of the Ethiopian and Asian faunas, like the sabertooth Megantereon whitei or the giant hyena Pachycrocuta brevirostris. Our review of these issues suggests that: (i) the elongated sabers and reduced postcanine teeth of African M. whitei limited the ability of this predator to process the prey carcass, which resulted in scavengeable resources for the Dmanisi hominins; (ii) the mass estimate in excess of 100 kg obtained for the trochlear perimeter of the distal humerus of the hyena from Dmanisi shows that it can be confidently ascribed to the genus Pachycrocuta; (iii) the postcranial anatomy of the Dmanisi hominins was not advantageous for scavenging tree-stored prey; (iv) the laterally flattened upper canines of M. whitei could not withstand the loads that would result from climbing a prey carcass into a tree; (v) paleobotanical analyses suggest a temperate grassland ecosystem in Dmanisi, not dominant forest conditions, with enhanced aridity in the level of hominin occupation; (vi) similarly, the low frequency of arboreal pollen in the Levantine Corridor at ～1.8 Ma points to more arid conditions than today in this area; (vii) many archaeopaleontological sites of the Rift Valley and its extension towards the Red Sea, the Levant and the Caucasus show evidence of tectonic, volcanic and/or hydrothermal events; and (viii) the delay of 400 ka in the arrival of hominins in Western Europe did not result from a lower availability of scavengeable resources.     

卡氏尖在中国古人类化石中出现及其演化意义

欧洲与亚洲古人类之间的关系一直是人类演化研究的关注点。基于对化石形态的研究,一些学者认为中国与欧洲古人类之间在更新世中、晚期存在一定程度的基因交流,并提供了支持基因交流的系列形态证据,但古人类学界对其中一些形态特征的人群属性、功能意义及形成机制存在不同认识。本文采用釉质外表观察和CT扫描方法对卡氏尖在98枚中国古人类上颌臼齿化石的出现和表现情况进行了数据统计和分析,并与非洲和欧洲古人类进行了对比。本研究发现卡氏尖在中国古人类具有较高的出现率(27.6%-62.5%)和多种形态表现。此外,在多枚中国古人类上颌臼齿发现两个通常只出现在在黑猩猩和非洲早期人类的原始卡氏尖表现:齿带-原尖脊和齿冠舌侧横行沟及屋檐状结构。基于这些发现,作者支持卡氏尖是从猿类,经过不同演化阶段的古人类,一直延续到现代人的一个古老特征的观点。卡氏尖在中国古人类的表现特点提示出现在中国古人类的卡氏尖更有可能是古老原始特征的残余。本研究显示,卡氏尖在中国与欧洲古人类都具有较高出现率,而卡氏尖在中国古人类的表现程度较同时期欧洲古人类更为显著。因此目前还没有足够的可信证据支持卡氏尖是中国与欧洲古人类之间基因交流的造成化石形态特征。     

Locomotor anatomy and biomechanics of the Dmanisi hominins

The Dmanisi hominins inhabited a northern temperate habitat in the southern Caucasus, approximately 1.8 million years ago. This is the oldest population of hominins known outside of Africa. Understanding the set of anatomical and behavioral traits that equipped this population to exploit their seasonal habitat successfully may shed light on the selection pressures shaping early members of the genus Homo and the ecological strategies that permitted the expansion of their range outside of the African subtropics. The abundant stone tools at the site, as well as taphonomic evidence for butchery, suggest that the Dmanisi hominins were active hunters or scavengers. In this study, we examine the locomotor mechanics of the Dmanisi hind limb to test the hypothesis that the inclusion of meat in the diet is associated with an increase in walking and running economy and endurance. Using comparative data from modern humans, chimpanzees, and gorillas, as well as other fossil hominins, we show that the Dmanisi hind limb was functionally similar to modern humans, with a longitudinal plantar arch, increased limb length, and human-like ankle morphology. Other aspects of the foot, specifically metatarsal morphology and tibial torsion, are less derived and similar to earlier hominins. These results are consistent with hypotheses linking hunting and scavenging to improved walking and running performance in early Homo. Primitive retentions in the Dmanisi foot suggest that locomotor evolution continued through the early Pleistocene.     

Tropical forests and the genus Homo

Tropical forests constitute some of the most diverse and complex terrestrial ecosystems on the planet. From the Miocene onward, they have acted as a backdrop to the ongoing evolution of our closest living relatives, the great apes, and provided the cradle for the emergence of early hominins, who retained arboreal physiological adaptations at least into the Late Pliocene. There also now exists growing evidence, from the Late Pleistocene onward, for tool‐assisted intensification of tropical forest occupation and resource extraction by our own species, Homo sapiens. However, between the Late Pliocene and Late Pleistocene there is an apparent gap in clear and convincing evidence for the use of tropical forests by hominins, including early members of our own genus. In discussions of Late Pliocene and Early Pleistocene hominin evolution, including the emergence and later expansion of Homo species across the globe, tropical forest adaptations tend to be eclipsed by open, savanna environments. Thus far, it is not clear whether this Early‐Middle Pleistocene lacuna in Homo‐rainforest interaction is real and representative of an adaptive shift with the emergence of our species or if it is simply reflective of preservation bias.     

Skeletal biology,functional asymmetry and the origins of "Handedness"

The past decade has witnessed the (re)emergence of a debate as to whether handedness is apomorphic within hominins. There are both qualitative and quantitative arguments, some which draw non-human primates into the handed sphere and others which exclude them. Ultimate questions concern origins of structural asymmetry of both brain and body and lateralized behaviours with implications for tool use and language. Lateralization is thus an important realm of phylogenetic study, and archaeologists and psychologists alike have sought to identify handedness within material culture. However, hand preference for tool manufacture and use among extant non-human primates, such as Cebus and Pan, suggests that the archaeological record may well be mute regarding the origins of laterality. In this paper, an argument is put forward positioning skeletal biology as a viable approach to the handedness origins issue. Behaviour is a mediator of the complementary processes of geometric modelling (change in size and shape) and histological remodelling (disuse osteopenia; microfracture repair); therefore, directional asymmetry in the pattern of skeletal modelling and remodelling is a putative signal of lateralized activity.     

Hominins do not share a common postnatal facial ontogenetic shape trajectory

This paper examines the hypothesis raised by recent studies that postnatal trajectories of shape change in the facial skeleton are parallel between, at least, chimpanzees, modern humans and also fossil hominins, specifically australopithecines and possibly Neanderthals. In contrast, other studies point to divergences in postnatal shape trajectories within diverse groups of primates. As such there is some debate regarding the relative contributions of pre and postnatal ontogeny to adult morphological differences. This paper presents a series of geometric morphometric studies of the ontogeny of facial shape in hominins with the specific aim of resolving these issues. The results indicate that many differences in facial shape between hominins are established prenatally, however highly significant divergences of postnatal facial ontogeny are found among living hominins. Our studies point to possible differences between the shape ontogeny of the Australopithecus africanus face and that of African apes on the one hand and humans on the other. However, sampling experiments indicate that the small sample size of available specimens of A. africanus does not permit any conclusions to be drawn regarding comparative shape ontogeny of the face.     

Hybridization in human evolution: Insights from other organisms

During the late Pleistocene, isolated lineages of hominins exchanged genes thus influencing genomic variation in humans in both the past and present. However, the dynamics of this genetic exchange and associated phenotypic consequences through time remain poorly understood. Gene exchange across divergent lineages can result in myriad outcomes arising from these dynamics and the environmental conditions under which it occurs. Here we draw from our collective research across various organisms, illustrating some of the ways in which gene exchange can structure genomic/phenotypic diversity within/among species. We present a range of examples relevant to questions about the evolution of hominins. These examples are not meant to be exhaustive, but rather illustrative of the diverse evolutionary causes/consequences of hybridization, highlighting potential drivers of human evolution in the context of hybridization including: influences on adaptive evolution, climate change, developmental systems, sex‐differences in behavior, Haldane's rule and the large X‐effect, and transgressive phenotypic variation.     

Validation of bone surface modification models for inferring fossil hominin and carnivore feeding interactions, with reapplication to FLK 22, Olduvai Gorge, Tanzania

Resolving the issue of how Early Stone Age hominins acquired large mammal carcasses requires information on their feeding interactions with large carnivores. This ecological information and its behavioral and evolutionary implications are revealed most directly from the tooth, cut, and percussion marks on bone surfaces generated by hominin and carnivore feeding activities. This paper employs a bootstrap method, a form of random resampling with replacement, to refine published neotaphonomic models that use the assemblage-wide proportions of long bones bearing feeding traces to infer the sequences in which Plio-Pleistocene hominins and carnivores accessed flesh, marrow, and/or grease from carcasses. Results validate the sensitivity of the models for inferring hominin feeding ecology, which have been questioned on grounds shown here to be unfounded. The bootstrapped feeding trace models are applied to the late Pliocene larger mammal fossil assemblage from FLK 22 (Zinjanthropus site), Olduvai Gorge, Tanzania. High frequencies of tooth and percussion marking on long bone midshaft fragments from FLK 22 are most consistent with those feeding trace models that simulate hominin scavenging from carcasses defleshed by carnivores, while cut mark data indicate that hominins more often had access to upper forelimb flesh than upper hind limb flesh. Together, the bone surface modification data indicate that hominins typically gained secondary access to partially defleshed carnivore kills, but they also allow for the possibility of some carcasses being processed only by carnivores and only by hominins.     

The Laetoli footprints and early hominin locomotor kinematics

A critical question in human evolution is whether the earliest bipeds walked with a bent-hip, bent-knee gait or on more extended hindlimbs. The differences between these gaits are not trivial, because the adoption of either has important implications for the evolution of bipedalism. In this study, we re-examined the Laetoli footprints to determine whether they can provide information on the locomotor posture of early hominins. Previous researchers have suggested that the stride lengths of Laetoli hominins fall within the range of modern human stride lengths and therefore, Laetoli hominins walked with modern-human-like kinematics. Using a dynamic-similarity analysis, we compared Laetoli hominin stride lengths with those of both modern humans and chimpanzees. Our results indicate that Laetoli hominins could have used either a bent-hip, bent-knee gait, similar to a chimpanzee, or an extended-hindlimb gait, similar to a human. In fact, our data suggest that the Laetoli hominins could have walked near their preferred speeds using either limb posture. This result contrasts with most previous studies, which suggest relatively slow walking speeds for these early bipeds. Despite the many attempts to discern limb-joint kinematics from Laetoli stride lengths, our study concludes that stride lengths alone do not resolve the debate over early hominin locomotor postures.     

The mammalian fauna associated with an archaic hominin skullcap and later Acheulean artifacts at Elandsfontein, Western Cape Province, South Africa

The Elandsfontein site, Western Cape Province, South Africa, is well known for an archaic hominin skullcap associated with later Acheulean artifacts. The site has also provided nearly 13,000 mammalian bones that can be identified to skeletal part and taxon. The assemblage derives from 49 species, 15 of which have no historic descendants. Comparisons to radiometrically dated faunas in eastern Africa indicate an age between 1 million and 600 thousand years ago. Unique features of the fauna, including the late occurrence of a dirk-toothed cat and a sivathere, may reflect its geographic origin in a region that was notable historically for its distinctive climate and high degree of biotic endemism. Together, taxonomic composition, geomorphic setting, and pollen extracted from coprolites indicate the proximity of a large marsh or pond, maintained by a higher water table. The small average size of the black-backed jackals implies relatively mild temperatures. The sum of the evidence places bone accumulation during one of the mid-Pleistocene interglacials that were longer and cooler than later ones, including the Holocene. The geomorphic context of the fauna presents no evidence for catastrophe, and most deaths probably resulted from attritional factors that disproportionately killed the young and old. However, only the dental-age profile of long-horned buffalo supports this directly. Field collection methods biased skeletal-part representation, but originally, it probably resembled the pattern in the younger, marsh-edge Acheulean occurrence at Duinefontein 2, 45 km to the south. Excavation there exposed multiple vertebral spreads, which probably mark carcasses from which hominins or large carnivores removed the meatier elements. Bone damage at both sites suggests that, despite abundant artifacts, hominins were much less important than carnivores in the bone accumulation. Together with limited observations from other sites, Elandsfontein and Duinefontein provisionally suggest that Acheulean-age hominins obtained few large mammals, whether by hunting or scavenging.     

Neanderthal genomics suggests a pleistocene time frame for the first epidemiologic transition

High quality Altai Neanderthal and Denisovan genomes are revealing which regions of archaic hominin DNA have persisted in the modern human genome. A number of these regions are associated with response to infection and immunity, with a suggestion that derived Neanderthal alleles found in modern Europeans and East Asians may be associated with autoimmunity. As such Neanderthal genomes are an independent line of evidence of which infectious diseases Neanderthals were genetically adapted to. Sympathetically, human genome adaptive introgression is an independent line of evidence of which infectious diseases were important for AMH coming in to Eurasia and interacting with Neanderthals. The Neanderthals and Denisovans present interesting cases of hominin hunter‐gatherers adapted to a Eurasian rather than African infectious disease package. Independent sources of DNA‐based evidence allow a re‐evaluation of the first epidemiologic transition and how infectious disease affected Pleistocene hominins. By combining skeletal, archaeological and genetic evidence from modern humans and extinct Eurasian hominins, we question whether the first epidemiologic transition in Eurasia featured a new package of infectious diseases or a change in the impact of existing pathogens. Coupled with pathogen genomics, this approach supports the view that many infectious diseases are pre‐Neolithic, and the list continues to expand. The transfer of pathogens between hominin populations, including the expansion of pathogens from Africa, may also have played a role in the extinction of the Neanderthals and offers an important mechanism to understand hominin–hominin interactions well back beyond the current limits for aDNA extraction from fossils alone. Am J Phys Anthropol 160:379–388, 2016. © 2016 Wiley Periodicals, Inc.     

A guide to the genomics of ecological speciation in natural animal populations

Interest in ecological speciation is growing, as evidence accumulates showing that natural selection can lead to rapid divergence between subpopulations. However, whether and how ecological divergence can lead to the buildup of reproductive isolation remains under debate. What is the relative importance of natural selection vs. neutral processes? How does adaptation generate reproductive isolation? Can ecological speciation occur despite homogenizing gene flow? These questions can be addressed using genomic approaches, and with the rapid development of genomic technology, will become more answerable in studies of wild populations than ever before. In this article, we identify open questions in ecological speciation theory and suggest useful genomic methods for addressing these questions in natural animal populations. We aim to provide a practical guide for ecologists interested in incorporating genomic methods into their research programs. An increased integration between ecological research and genomics has the potential to shed novel light on the origin of species.     

The possible role of predator–prey dynamics as an influence on early hominin use of burned landscapes

Foraging in burned areas has been suggested to represent the earliest stage in the use and control of fire by early hominins. Recently burned areas offer immediate foraging benefits including increased search efficiency for high‐ranked food items and decreased hunting opportunities for ambush predators. As such, they provide a triple‐bonus (reduced risk from ambush, ease of terrestrial travel and higher foraging returns) for some primates. However, previous studies have not yet accounted for other types of predators e.g., coursing (endurance predators that can pursue prey over long distances) which were sympatric with hominins and may also have exploited these environments. Behavioral ecology studies on the use of burned landscapes by extant carnivores demonstrate that while some ambush predators avoid recently burned areas, coursing predators do take advantage of their immediate hunting opportunities. Research examining habitat selection by animals under the simultaneous threat of multiple predator species with different modes of hunting, and the diversity of Plio‐Pleistocene carnivore guild is suggestive of two possible evolutionary scenarios in which hominins could either have selected or avoided burned areas (3–2 mya), based on whether ambush or coursing predators were perceived as presenting the greatest risk.     

Lower Paleolithic hominin ecology at the fringe of the desert: Faunal remains from Bizat Ruhama and Nahal Hesi, Northern Negev, Israel

The Southern Levant is a pivotal area for the study of hominin paleoecology during the Lower Paleolithic, because of its location on the out-of-Africa dispersal route and its significant ecological diversity. Important information has been gained by archaeofaunal studies, which usually reveal that exploitation of diverse Mediterranean environments with woodlands, marshes and lake margins, represents a dominant subsistence strategy for Lower Paleolithic hominins. Here, we present new taxonomic and taphonomic data from two sites in the southern coastal plain of the Southern Levant, at the fringe of the Negev Desert: Bizat Ruhama (Early Pleistocene) and Nahal Hesi (Middle Pleistocene). The sites preserve anthropogenic faunas, with the former signaling a marrow-exploitation strategy, perhaps related to scavenging from carnivore kills, and the latter showing evidence for primary access to fleshed ungulate carcasses. The species composition of these Northern Negev sites is unique for the Levantine Lower Paleolithic in that these sites lack typical woodland and riparian species, probably indicating an open, relatively uniform environment with patchy water sources and trees, much like this semiarid region today. Bizat Ruhama and Nahal Hesi are among the only Levantine Lower Paleolithic faunas associated with such a setting, thereby widening the known spectrum of environments exploited by hominins in the region. It is suggested that the two sites, coupled with the nearby Late Pleistocene evidence, reflect a largely stable semiarid environment on the northwestern fringe of the Negev Desert throughout much of the Pleistocene.     

Relevance of aquatic environments for hominins: a case study from Trinil (Java, Indonesia)

Knowledge about dietary niche is key to understanding hominin evolution, since diet influences body proportions, brain size, cognition, and habitat preference. In this study we provide ecological context for the current debate on modernity (or not) of aquatic resource exploitation by hominins. We use the Homo erectus site of Trinil as a case study to investigate how research questions on possible dietary relevance of aquatic environments can be addressed. Faunal and geochemical analysis of aquatic fossils from Trinil Hauptknochenschicht (HK) fauna demonstrate that Trinil at ∼1.5 Ma contained near-coastal rivers, lakes, swamp forests, lagoons, and marshes with minor marine influence, laterally grading into grasslands. Trinil HK environments yielded at least eleven edible mollusc species and four edible fish species that could be procured with no or minimal technology. We demonstrate that, from an ecological point of view, the default assumption should be that omnivorous hominins in coastal habitats with catchable aquatic fauna could have consumed aquatic resources. The hypothesis of aquatic exploitation can be tested with taphonomic analysis of aquatic fossils associated with hominin fossils. We show that midden-like characteristics of large bivalve shell assemblages containing Pseudodon and Elongaria from Trinil HK indicate deliberate collection by a selective agent, possibly hominin.     

Unraveling hominin behavior at another anthropogenic site from Olduvai Gorge (Tanzania): new archaeological and taphonomic research at BK, Upper Bed II

New archaeological excavations and research at BK, Upper Bed II (Olduvai Gorge, Tanzania) have yielded a rich and unbiased collection of fossil bones. These new excavations show that BK is a stratified deposit formed in a riverine setting close to an alluvial plain. The present taphonomic study reveals the second-largest collection of hominin-modified bones from Olduvai, with abundant cut marks found on most of the anatomical areas preserved. Meat and marrow exploitation is reconstructed using the taphonomic signatures left on the bones by hominins. Highly cut-marked long limb shafts, especially those of upper limb bones, suggest that hominins at BK were actively engaged in acquiring small and middle-sized animals using strategies other than passive scavenging. The exploitation of large-sized game (Pelorovis) by Lower Pleistocene hominins, as suggested by previous researchers, is supported by the present study.     

Tooth wear, Neanderthal facial morphology and the anterior dental loading hypothesis

The Anterior Dental Loading Hypothesis states that the unique Neanderthal facial and dental anatomy was an adaptive response to the regular application of heavy forces resulting from both the masticatory and cultural use of the anterior teeth. Heavy anterior tooth wear frequently observed in Neanderthal specimens is cited as a main source of evidence for heavy forces being applied to these teeth. From this, it might be predicted that the wear shown on the anterior teeth of Neanderthals would greatly exceed that of the posterior teeth and that this differential would be greater than in other hominins with different facial morphologies.In this paper, a new method of examining tooth wear patterns is used to test these predictions in a large assemblage of Late Pleistocene hominins and a group of recent hunter-gatherers from Igloolik, Canada. The results show that all Late Pleistocene hominins, including Neanderthals, had heavily worn anterior teeth relative to their posterior teeth but, contrary to expectations, this was more pronounced in the modern humans than in the Neanderthals. The Igloolik Inuit showed heavier anterior tooth wear relative to their posterior teeth than any Late Pleistocene hominins. There was, however, a characteristic Neanderthal pattern in which wear was more evenly spread between anterior teeth than in modern humans. Overall, the evidence presented here suggests that all Late Pleistocene hominins habitually applied heavy forces between their anterior teeth and that Neanderthals were not exceptional in this regard. These results therefore does not support the Anterior Dental Loading Hypothesis.     

A Hominin Femur with Archaic Affinities from the Late Pleistocene of Southwest China

The number of Late Pleistocene hominin species and the timing of their extinction are issues receiving renewed attention following genomic evidence for interbreeding between the ancestors of some living humans and archaic taxa. Yet, major gaps in the fossil record and uncertainties surrounding the age of key fossils have meant that these questions remain poorly understood. Here we describe and compare a highly unusual femur from Late Pleistocene sediments at Maludong (Yunnan), Southwest China, recovered along with cranial remains that exhibit a mixture of anatomically modern human and archaic traits. Our studies show that the Maludong femur has affinities to archaic hominins, especially Lower Pleistocene femora. However, the scarcity of later Middle and Late Pleistocene archaic remains in East Asia makes an assessment of systematically relevant character states difficult, warranting caution in assigning the specimen to a species at this time. The Maludong fossil probably samples an archaic population that survived until around 14,000 years ago in the biogeographically complex region of Southwest China.