Trends in Biological Anthropology 1
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Trends in Biological Anthropology 1 - Oxbow Books for the British Association for Biological Anthropology and Osteoarchaeology
Introduction
This volume brings together some of the papers presented during the British Association for Biological Anthropology and Osteoarchaeology annual meetings, 2011, held at the University of Edinburgh, and 2012, held at Bournemouth University. The Edinburgh conference organisers included Kathleen McSweeney, Elena Kranioti, Marlo Willows and Dawn Gooney and the sessions revolved around palaeopathology, scientific advances in osteology, and forensic anthropology, subject areas that are representative of individual fields of interest in the human osteology team at the University of Edinburgh. Bournemouth University’s Biological Anthropology team – Martin Smith, Karina Gerdau-Radonić, Holger Schutkowski, Elizabeth Craig-Atkins and Amanda Korstjens – organised the 2012 meeting which offered sessions in primatology and human evolution, interpreting and analysing trauma, interpreting and analysing funerary deposits and the regular open session. The range of papers presented at the meetings and those finally included in this volume are representative of the present breadth of research in Biological Anthropology and Osteoarchaeology within Britain and abroad.
We decided to organise the volume according to the themes that emerged from the papers submitted. The volume opens with studies focusing on extant nonhuman primates. Gabriele Macho’s Can Extant Primates Serve as Models to Determine the Dietary Ecology of Hominins? The Case of Paranthropines covers the study of modern baboons (Papio cynocephalus) as proxies to understand extinct hominin species’ diets and hence our own evolutionary history. Diana Mahoney Swales and Pia Nystrom’s Recording Primate Spinal Degenerative Joint Disease Using a Standardised Approach focuses on the use of human standards to analyse and interpret skeletal degenerative joint disease (SDJD) on the skeletal remains of extant primates, in particular within the superfamily Cercopithecoidea. Their study looks at the impact of locomotion and body mass on the development of SDJD.
These chapters on extant primates are followed by two on methods used in the fields of Biological Anthropology and Osteoarchaeology. Brenna Hassett’s Enamel Hypoplasia in Post-Medieval London: A Reassessment of the Evidence for Childhood Health is a study on the methods used to record Linear Enamel Hypoplasia (LEH) and how the choice of method can affect the prevalence recorded in different populations and hence the conclusions drawn from these types of studies. Géraldine Sachau-Carcel, Dominique Castex, and Robert Vergnieux’s Archaeoanthropology: How to Construct a Picture of the Past? focuses on the use of three-dimensional modelling to generate pictures of the content of collective graves. These images can then function as a means to understand the use and history of these structures.
These two papers are followed by three others that focus on Palaeopathology and Trauma. Marlo Willows’ Palaeopathology of the Isle of May presents the palaeopathological analysis of a skeletal collection from the Isle of May, off the coast of Scotland, dating between the 5th and 16th century AD. By comparing this collection to one from medieval Scotland, Willows tries to ascertain whether the palaeopathological data is evidence that the Isle of May benefitted from a healing tradition during the medieval period, as historical records and legends would have it. Malcolm Lillie, Inna Potekhina, Alexey G. Nikitin and Mykhailo P. Sokhatsky’s First Evidence for Interpersonal Violence in Ukraine’s Trypillian Farming Culture: Individual 3 from Verteba Cave, Bilche Zolote is a case study of a cranium found at Verteba Cave, western Ukraine, as a means to understand inter-personal interactions and burial ritual in that part of Ukraine during the Trypillian culture. This section is closed by Nataša Miladinović-Radmilović and Vesna Bikić’s Beheading at the Dawn of the Modern Age: The Execution of Noblemen during Austro-Ottoman Battles for Belgrade in the Late 17th Century, the study of a series of skulls found at a deposit site outside the fortress walls of Belgrade, Serbia, displaying evidence for beheading. Through the use of osteological and archaeological data, this study contributes to the history of Belgrade.
Two papers focus on the History of Medicine and Biological Anthropology. Gaynor Western’s The Remains of a Humanitarian Legacy: Bioarchaeological Reflections of the Anatomized Human Skeletal Assemblage from the Worcester Royal Infirmary presents the results of the excavation and analysis of a deposit containing disarticulated human remains at the Worcester Royal Infirmary. Western’s paper, though presenting osteological and archaeological evidence, is a contribution to our understanding of the History of Medicine and how the study of human anatomy progressed and developed. Stefanie Vincent and Simon Mays’ Thomas Henry Huxley (AD 1825–1895): Pioneer of Forensic Anthropology revisits Huxley’s analysis and report on the skeletal remains of a member of Sir John Franklin’s 1845 expedition to the Arctic and highlights one of the earliest attempts at identifying a recently deceased individual through the analysis of his or her skeletal remains as do forensic anthropologists today.
Finally, we close the volume with two papers that illustrate how the study of human remains whether modern or past can contribute to the modern world. Douglas Ubelaker’s The Concept of Perimortem in Forensic Science defines ‘perimortem’, particularly within a forensic anthropology context. He emphasises the importance of this definition because though a forensic anthropologist will not determine the cause and manner of death, he or she will interpret the timing of the injury, which may in turn contribute to the forensic pathologist’s determination of cause and manner of death. Jo Buckberry, Alan Ogden, Vicky Shearman and Iona McCleery’s You Are What You Ate: Using Bioarchaeology to Promote Healthy Eating presents a collaborative effort between historians, archaeologists, museum officers, medieval re-enactors and food scientists to encourage healthy eating among present day Britons by presenting the ill effects of certain dietary habits on the human skeleton.
To conclude, we thank our colleagues Martin Smith, Holger Schutkowski, and Amanda Korstjens for their editorial input and contributions, the team of reviewers, Laszlo Bartosiewicz, Laura Bassell, Sean Beer, Anthea Boylston, Elizabeth Craig-Atkins, Roxana Ferllini, Louise Loe, Piers Mitchell, Robert Paine, Catriona Pickard, Katherine Robson-Brown, Todd Rae, Norman Sauer, Rick Schulting, and John Stewart, the British Association for Biological Anthropology and Osteoarchaeology’s committee, Tina Jakob, the series editor, and last but not least, the contributors for their patience and hard work.
Commemoration
Given the subsequent sad death of our friend and colleague, Professor Donald Ortner, in 2013, we were extremely privileged that he was able to open the 2011 Edinburgh conference with one of his ever-stimulating keynote speeches. He will be sincerely missed.
Karina Gerdau-Radonić
(Bournemouth University)
Kathleen McSweeney
(University of Edinburgh)
1. Can Extant Primates Serve as Models to Determine the Dietary Ecology of Hominins? The Case of Paranthropines
Gabriele A. Macho
The dietary ecology of early hominins, particularly East and South African Paranthropus, remains poorly understood. Here I argue that an integrative approach that combines current knowledge on isotope composition, microwear textures, dental morphology and comparative studies on the extant baboon Papio cynocephalus has the potential to shed light on the possible diet(s) of Paranthropus boisei and P. robustus.
Baboons eat a variety of C4 foods, which differ considerably in nutritional value and material properties. East and South African paranthropines apparently spent longer periods of time feeding on similar C4 foods; their morphology suggests that they exploited opposite ends of the C4 plant food niche spectrum that is utilised by baboons. Paranthropus boisei consumed predominantly hard brittle foods, while P. robustus fed on hard tough resources. Because of the high nutrional value of some C4 foods, a shift in dietary preferences from C3 to C4 sources need not have been accompanied by an extension of total feeding time. To what extent differences in food selection and time spent feeding on C4 foods between P. boisei and P. robustus were due to habitat differences between East and South Africa, or constitute true species preferences, needs to be investigated further.
Keywords: Paranthropus boisei; Paranthropus robustus; Hominin dietary ecology; C4 plant niche; Papio cynocephalus
1. Introduction
The dietary adaptations of extinct hominins remain the topic of intense research. This is unsurprising as diet underpins all aspects of an animal’s biology and a shift in diet facilitated the marked life history changes seen in our lineage, including the 3-fold increase in brain size (Leonard and Robertson, 1997). Determining the dietary niche(s) of extinct hominins is not trivial however and is hampered by a number of factors. The hominin masticatory apparatus differs greatly from that of extant primates and may be phylogenetically constrained, while the fragmentary nature of the hominin fossil record makes it impossible to carry out in-depth functional analyses. Therefore, palaeoanthropological studies have tended to focus on information that can be gleaned from dental remains, particularly enamel thickness (e.g. Rabenold and Pearson, 2011), as well as microwear textures and isotope composition. The latter two approaches are regarded particularly useful in deciphering the dietary ecologies of hominins, as microwear and isotope composition directly reflect what an animal ate during life (Grine et al., 2012). Despite considerable research efforts in these areas however, the diets of hominins remain poorly understood. As a case in point, Paranthropus boisei from East Africa is assumed to have subsisted almost exclusively on a low-quality diet of grasses and sedges (up to 91%), as inferred from the isotope composition of their hard tissue (Lee-Thorp, 2011; Cerling et al., 2013). Yet, such interpretations are inconsistent with P. boisei morphology and its energetic requirements predicted from body mass and brain size; this interpretation is also in conflict with the species´microwear textures, which resemble those of a soft fruit consumer (Ungar et al., 2008). Paranthropus robustus from South Africa, in contrast, is similar to gracile australopith with regard to isotope composition, while overall morphological and cladistic considerations predict its feeding ecology to have been comparable to that of P. boisei. Clearly, not all predictions can be equally valid.
Of course, hominins may have been truly unique and their ecologies never be known. While this is possible, it is improbable. Food sources do not vary so dramatically across Africa, nor between now and the past. I therefore propose a bottom-up approach that (a) explores the variety of foods available to primates with similar physiologies, specifically baboons, and (b) assesses the capabilities of the hominin masticatory apparatus to break down these various food types. It is imperative to identify what an animal would not have been able to eat on the basis of its morphology before exploring its potential niche, i.e., what it could have eaten (availability). Another important factor for determining the diet of an animal is energetics: Could the inferred diet have provided the hominin with sufficient energy and nutrients while, at the same time, being low in toxins (Altmann, 2009)? Could the animal have harvested the proposed foods within its time budget constraints? To answer these questions a multi-faceted approach is necessary that combines information derived from morphology, behavioural ecology of extant primates and modelling. Here I outline the fundamentals of such an approach and explore whether the results obtained from each strand could be brought together to arrive at a coherent inference about the dietary niche(s) of P. boisei and P. robustus. Papionins serve as a modern template.
Papio and Theropithecus have long been considered good analogs for an appraisal of the dietary radiation of hominins vis-à-vis the ecological drivers underlying it (Jolly, 1970, 2001; Elton, 2006). Together with suids, hominins and baboons have the same basic physiology and share(d) the same ecological and, presumably, dietary niche (Hatley and Kappelman, 1980), i.e., they exploit(ed) Underground Storage Organs (USOs). Baboons, modern humans and pigs are the only large-bodied mammals that can, and habitually do, extract below-surface foods. Together with many sedges and grasses USOs mostly follow the C4 photosynthetic pathway. Rather than being of low nutritional value however, USOs tend to be nutrientrich and could therefore have constituted a valuable source for large-bodied large-brained hominins. In fact, it has been suggested that USOs may have played the key role in the evolution of modern human life histories and sociality, including allocare (O’Connell et al., 1999, 2002). Comprehensive nutrional analyses of C4 foods are unfortunately still wanting, in part because C4 foods are generally considered nutritionally unimportant and/or, as in the case of USOs, because they require substantial extraoral preparation, i.e., pounding or cooking, before they are suitable for human (hominin?) consumption (Carmody et al., 2011) and have therefore been thought to have played a minor role in the earliest stages of human evolution (but see Dominy et al., 2008). Fortunately, empirical data on the feeding ecology of yearling baboons from the Amboseli National Park, Kenya, are available and are sufficiently detailed (Altmann, 1998) to inform which C4 foods are commonly eaten by baboons and their nutritional value. This allows to assess (a) whether early hominins could have subsisted on a predominantly C4 diet, (b) whether they could have obtained these foods within their daily time budget, and (c) whether such a diet is consistent with hominin dento-cranial morphologies.
2. Background
2.1. The Palaeontological Background
With its hyper-masticatory apparatus and thick-enamelled teeth P. boisei has originally been interpreted as a hard object feeder (Tobias, 1967), but microwear texture analyses seem to indicate that it fed on soft foods (Ungar et al., 2008). Comparative isotope analyses, in contrast, identified P. boisei as a grass-eater like the gelada baboon, Theropithecus gelada (Cerling et al., 2011a). Overall dento-cranial morphology and the lack of shearing crests would have made it difficult for P. boisei to break down grasses however, save for some soft fresh shoots (Kay, 1975). Grasses are broken down by a scissor-like action of opposing molars. Teeth of P. boisei are low-crown and relatively flat when worn, which would have made it nearly impossible for them to break down tough grasses. An even stronger argument against grass-eating comes from broader biological considerations, specifically the species’ relatively large brain and its associated life history (Robson and Wood, 2008). Brains are expensive to grow and to maintain, and a diet consisting of mainly grasses is unlikely to fulfil the energetic requirements of a largebrained primate (Navarrete et al., 2011). Unsurprisingly, the specialised grass-eating Theropithecus gelada is characterised by relatively and absolutely smaller brains compared to other baboons (Isler et al., 2008). South African P. robustus is even more encephalised than P. boisei (Robson and Wood, 2008), which implies that its energy requirements may have even been higher than those of P. boisei.
Paranthropus robustus from South Africa is commonly considered to form a clade with East African P. boisei or, alternatively, to have evolved its derived morphology in response to similar ecological pressures, i.e., through homoplasy (Wood and Constantino, 2007). Either way, both P. robustus and P. boisei would therefore be expected to exhibit similar feeding habits. Apparently they do not. Isotope analyses imply that P. robustus consumed greater amounts of C3 sources than P. boisei: it overlaps entirely in its isotope composition with Australopithecus africanus (Sponheimer et al., 2005; Lee-Thorp et al., 2010), but not in microwear texture (Scott et al., 2005). Inspection of microwear textures provided by Grine et al. (2012) reveals P. robustus to be unique amongst extant and extinct primates, i.e., it does not unequivocally cluster with any other extant primate analysed thus far. This is intriguing, as is the observation that there is no overlap in microwear textures between P. robustus and P. boisei at all (Figure 1.1a).
Figure 1.1. (a) The microwear texture data ep Lsar (anisotropy) and Asfe (complexity) were derived from Grine and colleagues (2012), whereby the data for papionins were originally presented in El-Zaatari et al. (2005). (b) High resolution SEM picture of a naturally broken P. boisei tooth OH30. (c) SEM image of P. robustus SK55b. In P. boisei (b) enamel prisms are mostly straight and are organised nearly parallel. This renders the material stiff when loaded in the direction of the prisms, but weak when loaded perpendicular to it (see Figure 1.2). Consequently, P. boisei are poorly adapted to multi-directional loading. In contrast, prisms of P. robustus enamel undulate in a complex manner in 3D. Because of the different orientation of bundles of prisms, cracks would not propagate easily through the tissue. As a result, P. robustus teeth can be inferred to have been strong and well adapted to multi-directional loading. Information obtained from microwear textures, which do not overlap between the species (a), further highlight the distinctiveness in dietary ecology between paranthropines. Yet, each of these exinct hominin exhibits some similarities with baboons.
2.2. Biomechanics and Teeth
Enamel thickness continues to feature prominently in paleaoanthropological studies, not least because all hominins, particularly paranthropines, are characterised by hyperthick enamel. It is unclear however whether the thick enamel of these primates is an adaptation to wear resistance or to hard object feeding. To shed light on this question researchers commonly take a comparative approach whereby the correlation between diet in extant taxa and the enamel thickness of their teeth is used to make inferences about the dietary niche(s) of hominins (e.g. Kay, 1981; Dumont, 1995; Rabenold and Pearson, 2011). Such research designs are problematic, as extinct taxa do not (normally) have modern analogs. An assessment of the micro- and macrostructural detail of enamel may be more informative, as the microanatomy determines whether the structure was adapted to resist abrasion, high bite forces and/or multi-directional loading.
Figure 1.2. The accumulation of tensile stresses underneath the wear surfaces obtained in a finite element study, for the leading and trailing edge respectively (Shimizu et al., 2005). When the prisms are oriented parallel to the force vector (i.e., 0°–30°) wear resistance is high, but the dental material is soft and weak (i.e., tensile stresses building up between the prisms would push the tissue apart). At higher angles of prism orientation the tooth is stiff, but wear resistance is low. These opposite mechanical behaviours are schematically shown in (b). The schematic enamel blocks are positioned underneath the respective values shown in (a).
Enamel is a composite hierarchically-organised material that is made up of a complex arrangement of hydroxyapatite crystals, both within and between prisms. Within prisms, i.e., the prism head, the crystal orientation is parallel with the prism long axis (c-axis), whereas in the prism tail/interprismatic matrix crystals are aligned nearly perpendicular to those of the prism head (Osborn, 1981); the change in crystal orientation from prism head to tail (interprismatic matrix) is gradual however. The diameter of a prism varies and is generally between 3–6μm (Figure 1.1b, c). Hydroxyapatite crystals are held together by an inorganic matrix and each prism is partly surrounded by a protein-rich prism sheath, which bonds the prisms and confers strength to the tissue (Ge et al., 2005). The situation is further complicated by the fact that prisms are not (normally) parallel. Rather, prisms follow an undulating path from the dentino-enamel junction to the outer enamel surface, which varies in amplitude and frequency between taxa, and each prism is slightly offset with regard to its neighbour (Macho et al., 2003). This results in bundles of prisms apparently crossing over, i.e., decussating (Figure 1.1c), when viewed in histological cross-sections (even though the transition is, in fact, gradual). Decussation acts as a crack-stopping mechanism (Rensberger, 1995, 2000). It is this complex hierarchical 3D arrangement of crystals within prisms, together with differences of prism orientations, that determines the biomechanical behaviour of the tissue (An et al., 2012).
As crystals are considerably stiffer than the matrix, loads applied along the direction of the crystals will in large part be carried by the crystals: enamel will be stiff (Figure 1.2b). In contrast, when loads are applied across the direction of crystals, most of the internal stresses will be carried by the inorganic matrix and