Do Larger Molars and Robust Jaws in Early Hominins Represent Dietary Adaptation?’ a New Study in Tooth Wear

Clement, A and Hillson, S 2013 ‘Do larger molars and robust jaws in early hominins represent dietary adaptation?’ A New Study in Tooth Wear. Archaeology International, No. 16 (2012-2013): 59-71, DOI: http://dx.doi.org/10.5334/ai.1605

ARTICLE ‘Do larger molars and robust jaws in early hominins represent dietary adaptation?’ A New Study in Tooth Wear Anna Clement* and Simon Hillson*

Diet imposes significant constraints on the biology and behaviour of animals. - Thefos sil record suggests that key changes in diet have taken place throughout the course of human evolution. Defining these changes enables us to understand the behaviour of our extinct fossil ancestors. Several lines of evidence are available for studying the diet of early hominins, including craniodental morphology, palaeoecology, dental microwear and stable isotopes. They do, however, often provide conflicting results. Using dental macrowear analysis, this new UCL Institute of Archaeology project will provide an alternative source of information on early hominin diet. Dental macrowear has often been used to analyse diet in archaeological populations, but this will be the first time that this type of detailed study has been applied to the early hominin fossil record.

Studies of living primates have shown how dence. Instead research into the early homi- their diet determines many aspects of their nin diet has had to rely on alternative sources lives, such as geographic range, body size, of evidence, including the size and shape of locomotor behaviour (how they moved) and the skull and teeth (craniodental morphol- breeding strategy. Diet must have occupied ogy); palaeoecology; dental microwear; and a similarly important place in the biology of stable isotopes. While each of these differ- extinct primates and therefore, if we are to ent lines of evidence has given us important understand the evolution of hominins (the insights into past diets, they often provide grouping that includes our own species and conflicting results. In 2012, a new project extinct fossil ancestors), it important to try began at the UCL Institute of Archaeology and uncover evidence for this past diet. The examining tooth wear patterns in low magni- sources of information available for this vary fication images of early fossil hominins. This between different parts of the fossil record. type of study is known as dental macrowear For later hominins, archaeological materials analysis and is often used to examine diet in such as stone tools and butchered animal archaeological populations, but this is the bones provide a key form of evidence with first time a detailed study has been applied which to reconstruct their diet. Early hominin to the early hominin fossil record. fossils (4.4 to 1.8 million years ago), however, are rarely associated with these types of evi- The fossil record The early hominin fossil record is dominated by two main genera – Australopithecus and * UCL Institute of Archaeology, Paranthropus. These two groups are dated London WC1H 0PY, United Kingdom [email protected], [email protected] to a geological time period between the end 60 Clement and Hillson: A New Study in Tooth Wear

2007). These features have been interpreted as adaptations for masticating a mechanically resistant diet that demanded the gen- eration of a powerful bite force over a broad grinding area of teeth (Kay, 1981; Walker, 1981; Demes and Creel, 1988; Hylander, 1988; Daegling and Grine, 1991; Teaford and Ungar, 2000; Strait et al., 2009). This diet is thought to have included hard, brittle foods such as nuts, fruits with hard shells, skins and stones, and possibly some soft foods such as flowers and buds (Kay, 1981; 1985; Lucas and Peters, 2000; Teaford and Ungar, 2000; Wood and Richmond 2000; Strait, et al., 2009). It has also been suggested that these early hominins would have had difficulty breaking down tough and more pliant food items like seed pods and meat (Lucas and Peters, 2000). Fig. 1: Map of the major fossil sites where Australopithecus and Paranthropus have specimens of Australopithecus and Paran- small anterior teeth (incisors and canines) thropus have been found. relative to their cheek teeth (premolars and molars) in comparison with later hominins of the Pliocene and beginning of the Pleis- such as modern humans (Jolly, 1970; Kay, tocene, known as the Plio-Pleistocene. Like 1985; Ungar and Grine, 1991; Teaford and most mammal fossils, they are especially well Ungar, 2000). This is interpreted as the result represented by jaws and teeth because the of less emphasis being placed on foods that dental tissues are much more resistant than required substantial incisor use, such as bone to most forms of physical and chemi- those with large thick husks and hard seeds cal attack during fossilization. Four different surrounded by a thick layer of flesh (Teaford taxa (a group of related organisms) within and Ungar, 2000). these two main genera are particularly well Whilst these early hominins share com- known within the fossil record – Australo- mon features in their craniodental mor- pithecus afarensis and Paranthropus boisei phologies, there are clear contrasts between from sites in East Africa and Paranthropus them which suggest that their diets might robustus and Australopithecus africanus from have differed (Figs 2 and 3). Paranthro- sites in South Africa (Fig. 1). pus specimens, in particular, have greatly enlarged molars and premolars relative to Craniodental evidence their tiny incisors and canines with exceed- Compared with most primates, both living ingly thick enamel crowns and massively and extinct, Australopithecus and Paranthro- proportioned jaws (Grine, 1981; Kay, 1981; pus had relatively large, flat, thick enamelled 1985; Walker, 1981; Ungar, 2004). This sug- cheek teeth held within robust jaws with gests that they represented an even more large muscle attachments (Robinson, 1956; specialised adaptation to hard foods, with Wolpoff, 1973; Rak, 1983; Wood and Abbot, increased grinding surfaces, greater abra- 1983; Kay, 1985; Martin, 1985; Benyon and sion resistance and stronger tooth support- Wood, 1986; Macho and Thackery, 1992; Tea- ing structures and musculature (Robinson, ford and Ungar, 2000; Ungar, 2004; Lucas, 1954; Grine, 1981; Rak, 1983; Kay, 1985; Clement and Hillson: A New Study in Tooth Wear 61

afarensis and P. boisei challenges this simple dichotomy in diet between Australopithecus and Paranthropus, which suggests that, although A. afarensis may have been mor- phologically equipped to process hard brittle foods, it did not necessarily do so (Grine et al., 2006; Ungar et al., 2010). Similarly, P. boisei is characterised by the largest cheek teeth of any known hominin, backed by the most robust jaws, supporting structures and large areas of muscle attachment which imply an ability to consume mechanically challeng- ing foods on a regular basis (Jolly, 1970; Kay, 1985; Teaford and Ungar, 2000). The results of recent microwear analysis, however, have shown no evidence that they consumed particularly hard or tough foods (Ungar et al., 2008). Scott et al.’s (2005) study found that Fig. 2: Australopithecus africanus. P. robustus was also unlikely to have been a specialised hard object feeder and that it is Hylander, 1988). As Paranthropus is found more likely, that hard, brittle foods were only later in the Plio-Pleistocene fossil record than an occasional part of their diet. Australopithecus, which had smaller and less The original microwear studies of early heavily built cheek teeth, this has been taken hominins were hindered by the difficulty to suggest that hard, abrasive foods became of making repeatable observations with the increasingly important during this epoch of methods of the time (Grine et al., 2002). Now geological time. This is supported by pal- more objective and repeatable approaches aeoenvironmental data which suggest that are available for studying these features, such Australopithecus occupied relatively wooded as high resolution scanning of the worn sur- habitats, while Paranthropus inhabited more faces and three-dimensional surface texture open environments requiring increased die- analysis (see Scott et al., 2005). However, tary flexibility and the ability to process dif- some limitations still apply. Microwear is con- ferent types of food, including harder items fined to little worn teeth of younger individu- (Vrba, 1975; Reed, 1997; Avery, 2001). als who still possess substantial amounts of occlusal enamel. The number of specimens Dental microwear studies that preserve good ante-mortem microwear Microscopic examination of wear pits and features in fossils of this age is greatly lim- scratches on dental enamel (dental micro- ited, reducing the sample size suitable for wear) provides direct evidence of what a fos- further analysis. Microwear features also sil taxon ate, by making comparisons with only represent food eaten during the period living primates. The first microwear studies immediately before death and this had of early hominins suggested that P. robus- become known as the ‘Last Supper Effect’ tus consumed harder more brittle foods (Grine, 1986). In addition, microwear studies that required more variable chewing forces tend to compare a single tooth type between than A. africanus who consumed tougher, taxa – for example, either a first molar or inci- but softer fruits and/or leaves (Grine, 1981; sor – rather than examining the relationship 1986; 1987; Grine and Kay, 1988). More between different teeth in the dentitions of recent work on microwear patterns in A. the fossils which are being compared. 62 Clement and Hillson: A New Study in Tooth Wear

Fig. 3: Paranthropus robustus.

Stable isotope studies et al., 2006). P. boisei specimens give values In contrast to many of the microwear stud- that suggest consumption of more C4 rich ies, the results from stable carbon isotope foods, such as tropical grasses and sedges, analysis suggest greater similarities between than all other early hominins, which indicate early hominins in their diets. A. africanus, for that, rather than processing hard objects, example, appears to have eaten a highly vari- their robust craniodental anatomy was an able diet mostly consisting of C3 foods (such adaptation for processing large quantities as fruits and leaves from trees, bushes and of low-quality vegetation (van der Merwe et shrubs or animals which consumed them), al., 2008; Cerling et al., 2011). While stable but also exploited C4 resources (such as carbon isotope research has provided some tropical grasses and some sedges or again the interesting results it does have some limita- animals feeding on them) (Sponheimer and tions. One of the biggest problems is that it Lee-Thorp, 1999; van der Merwe et al., 2003). is currently unable to distinguish between This is surprising because the palaeoenvi- diets as different as folivory, frugivory and ronmental evidence suggests C3 resources carnivory because they are all based on C3 were more abundant than C4 in their habitat plants in forested ecosystems. (Vrba, 1975; Reed, 1997; Avery, 2001). The In order to understand as much as we can results for P. robustus showed similar values about early hominin diets all available sources to A. africanus (Lee-Thorp et al., 1994) despite of information need to be used. One area evidence that C4 plants were more abundant which has currently been under-researched in their habitats (Vrba, 1995; Reed, 1997). is dental macrowear. Whilst observations of It also appears that the P. robustus values the dental macrowear in early fossil hominins changed between seasons and years, suggest- have been made (Robinson, 1956; Wolpoff, ing that, rather than being dietary specialist, 1973; Wallace, 1973; Grine, 1981), a system- they ate a very variable diet (Sponheimer atic study has never been carried out. Clement and Hillson: A New Study in Tooth Wear 63

Dental macrowear stantiate archaeologically because there is no Tooth wear is a complex process resulting directly associated evidence of tools or even from contact either between teeth or with food remains. foreign bodies in the mouth, such as food, materials, artefacts and grit (Molnar, 1972). Research Questions Two main types of tooth wear can take place This research project aims to address three between teeth: occlusal and approximal. main questions about the pattern of dental Occlusal wear occurs between the occlusal macrowear in early fossil hominins: (grinding and cutting) surfaces of oppos- ing teeth in the upper and lower dentition, • How variable is the wear pattern whereas approximal wear occurs between amongst members of the same taxo- neighbouring teeth in the same jaw, at their nomic group of early hominins; does contact points. Most dental macrowear stud- this change with increasing overall tooth ies have focused on the difference in occlusal wear; does it show differences between wear patterns in modern humans and males and females in those fossil groups between agriculturalists and hunter-gath- where sexual dimorphism is suggested? erers (Molnar, 1971; Smith, 1972; Turner, • Taking this variation into account, are 1979; Hinton, 1981; Smith, 1984; Kaifu, there consistent differences between 1999; Eshed et al., 2006; Deter, 2009). Smith taxa? In particular, is there a relation- (1984), for example, found that while hunter- ship between such differences and the gatherers maintained relatively flat occlusal robustness and size of molars/premolars wear, agriculturalists exhibited more oblique and the jaws? wear patterns. These differences were attrib- • How does the variation seen in early uted to a reduction in the toughness of food hominins compare with that of living consumed by the agricultural groups. Work chimpanzees, gorillas and orang-utans, with recent hunter-gatherers has also sug- as well as modern humans; are there gested that diet played a strong role in the consistent differences between species? balance of tooth wear through the dentition, Much more is known about the diet of although this is overlain by their strikingly extant primates, which will therefore heavy use of teeth as tools (Clement et al., provide an important comparison. 2009; Clement and Hillson, 2012). The diets of modern humans would, how- Methods ever, have greatly differed from those of early Our project uses a dental macrowear method. hominins. A better comparison therefore The method works on the progressive expo- might be the living chimpanzees, gorillas sure of underlying dentine as the enamel of and orang-utans, which show marked con- a tooth crown is worn away. Almost all living trasts in diet matched by variation in tooth humans are exceptional amongst primates morphology (Kay, 1985; M’kirera and Ungar, in having very slow rates of tooth wear. This 2003; Lucas, 2004), but little is known about is in contrast to recent hunter-gatherers, the their pattern of tooth wear. Chimpanzees people who made the Upper Palaeolithic also, to some extent, use their teeth as tools cultures and early farmers, all of whom in preparing foods, for example in modifying showed a rapid rate of tooth wear, as does sticks for food gathering (Boesch and Boesch, every other living and extinct primate (e.g. 1990), but this is nothing compared to the Smith, 1984; Dean et al., 1992; Clement et heavy and sustained use in human hunter- al., 2009, 2012; Clement and Hillson, 2012). gatherers. It is a reasonable assumption that Under these conditions, dentine is exposed early hominins also used their teeth as tools very rapidly after the teeth erupt into the to some extent, but this is impossible to sub- mouth. We use image analysis software to 64 Clement and Hillson: A New Study in Tooth Wear

Fig. 4: An image of the occlusal (biting) surface of a molar with the occlusal outline highlighted in blue and the area of dentine highlighted in red. measure both occlusal and approximal wear als whose age at death is not independently from digital images of the occlusal (biting) known. To remove age as a factor, we present surfaces of teeth, prepared from photo- the dentine proportion of each tooth as a graphs of original specimens where possible, ratio of the dentine proportion of another or from casts or scans of good quality pub- tooth from the same jaw (usually the perma- lished photographs. nent first molar is the reference tooth as this ImageJ image analysis software is used to is the first to emerge and therefore the most measure the area of the occlusal surface and worn, but this varies with preservation and the area of exposed dentine (Fig. 4). A den- with the question being asked). The resulting tine proportion is then calculated by divid- figure for each tooth is known as the wear ing the area of exposed dentine by the area ratio and this allows heavily worn dentitions of the occlusal surface. As wear progresses, to be compared directly with lightly worn this dentine proportion increases steadily. because it represents the wear pattern rather ImageJ is also used to measure the circum- than the amount of wear. This maximises the ference of the occlusal surface and then the number of individuals that can be included part of this circumference which is taken up in the study. by approximal attrition facets. An approxi- The fundamental principle of interpreta- mal proportion is then calculated by dividing tion of these wear ratios is that the dental this facet length by the circumference of the eruption sequence – the order in which occlusal surface. different teeth in the dentition appear in Overall tooth wear naturally increases with the mouth – dictates the amount of time age and this makes it difficult to compare the each tooth is exposed to wear. In modern state of wear in younger and older individu- humans the first molar is normally the first Clement and Hillson: A New Study in Tooth Wear 65 permanent tooth to erupt, around 6 years of incisors in early hominins are indeed adap- age, whereas the third molar erupts signifi- tations to the requirements for processing cantly later in an individual’s life, during the diets of differing texture, then it is reason- late teens and early twenties. Thus, the first able to suggest that the balance of wear molar is exposed to considerably more wear between these tooth types would also be (10–16 years) than the third molar. If we different. It is also important to consider the assume a constant rate of wear for all teeth timing and pattern of dental development then, at any age, it follows that earlier erupt- in different taxa, as the ages at which differing teeth will exhibit the most advanced ent teeth erupt into the mouth will have a wear. If the rate of tooth wear is not constant considerable effect on the balance of wear for all teeth, then the degree of wear will not between them. Living chimpanzees, gorillas reflect the expected eruption sequence and and orang-utans show a number of key dif- this tells us that some other factor affected ferences from ourselves in eruption timing the evenness of the wear through the denti- and sequence of their teeth. The chimpanzee tion. Our studies with dental casts of recent permanent dentition, for example, is com- high wear rate hunter-gatherers for whom plete by 11–12 years of age and their first age was known at the time impressions were molars erupt between 3 and 4 years (Nissen taken have shown that, although occlusal and Riesen, 1964). Their first incisors erupt tooth wear increased with age, the balance around two years after the first molars, at between different tooth types in the denti- about the age their second molars erupt, tion remained relatively constant (Clement whereas in humans the first incisors erupt and Hillson, 2012). almost at the same age as the first molars. Our previous research has shown that this This needs to be taken into account when method can be applied to dentitions at all considering tooth wear patterns. Histological states of wear in original specimens, casts, examination of enamel and dentine of fossil photographs or scans of published images teeth has suggested that both Paranthropus (Clement et al., 2009; 2012; Clement and and Australopithecus had short dental devel- Hillson, 2012) and therefore, unlike micro- opment sequences more similar to chimpan- wear and stable isotope studies, it is not zees and gorillas than to ourselves, but dif- limited by access to original specimens. This fered from each other in the formation times allows us to include the majority of tooth fos- of their incisors and canine (Bromage and sils so far recovered for the taxa of interest. In Dean, 1985; Dean, 1985; 2010; Dean et al., addition, this method is less time consuming 2001; Dean and Lucas, 2009). Remarkably than microwear methods and can therefore rapid formation of incisors and canines has be applied to much larger assemblages of fos- been reported for Paranthropus (Bromage sils. It can be applied equally to teeth of dif- and Dean, 1985; Benyon and Dean, 1988). ferent morphology from different taxa. Our All these differences in dental development study of recent hunter-gatherer people has timing, and thus eruption, should also be made it clear that the balance of this wear reflected in wear patterns. measure between molars, premolars, the canine and incisors shows subtle differences Current and future research due to diet and use of teeth as tools (Clement objectives et al., 2012; Clement and Hillson, 2012). We 1. Catalogue digital images of A. afri- believe that a similar approach is appropri- canus and P. robustus teeth. Digital ate to the very different question of diet and images were taken of all original spec- adaptation in extinct early hominins. imens of A. africanus and P. robustus If differences in the relative size and mor- that were available for study during phology of molars, premolars, canines and data collection trips to the University 66 Clement and Hillson: A New Study in Tooth Wear

Fig. 5: Data collection at the Ditsong Museum of Natural History, South Africa.

of Witswatersrand in Johannesburg las from the collections at the Powell and the Ditsong Museum of Natural Cotton Museum, UK. A future data History, South Africa (Fig. 5). These collection trip to the Natural His- included specimens from the sites of tory Museum, London is planned to Kromdraii, Makapansgat, Sterkfon- photograph a comparative sample of tein, Swartkrans and Taung (Fig. 1). orang-utans. Published images of specimens una- 4. Analysis of early hominin tooth wear vailable for study were also compiled. patterns. Tooth wear has been meas- 2. Catalogue digital images of A. afa- ured from all digital images of early rensis and P. boisei teeth. A data col- hominins within the project’s cata- lection trip was undertaken to the logue and the aim is to measure all University of Arizona, USA, where a images of the extant primates by the catalogue of digital images of origi- end of July 2013. The next step in this nal specimens and dental casts of A. research project will be to compare afarensis and P. boisei were compiled. tooth wear patterns in A. afarensis and These images included specimens A. africanus with those of the more from the sites of Hadar and Omo, in robust early hominins, P. boisei and P. Ethiopia, Laetoli, Olduvai Gorge and robustus. The wear patterns of these Peninj, in Tanzania, and Koobi Fora, four taxa of early hominins will then in Kenya (Fig. 1). Scans of published be compared to the wear patterns images were also included in the cata- of gorillas, chimpanzees and orang- logue for any further specimens of A. utans, taking into account the dif- afarensis and P. boisei. ferences and similarities in eruption 3. Catalogue digital images of chimpan- sequence and dental morphology. In zees, gorilla and orang-utans. Digital addition, early hominin and extant images were taken of a large sample primate wear patterns will be com- of wild shot chimpanzees and goril- pared with the database of high wear Clement and Hillson: A New Study in Tooth Wear 67

rate modern humans already held at Acknowledgements the UCL Institute of Archaeology, tak- The authors wish to thank Professor Bill Kim- ing into account differences between bel, Arizona State University, for supplying age groups, sexes and diet. the images of A. afarensis from Hadar, Ethio- 5. Context of early hominin dental mac- pia, as well as access to casts of other early rowear patterns. The final part of this hominin fossils. We are also grateful to Dr project will be to analyse the patterns of Bernhard Zipfel from the University of Wit- tooth wear in the early fossil hominins watersrand and Ms Stephany Potze from the within the context of the published lit- Ditsong National Museum of Natural History erature on stable isotope studies, den- for granting access to the South Africa fos- tal microwear analysis, craniodental sils, and to Ms Angela Gill for allowing us to morphology and palaeoecology. study the collections at the Powell Cotton Museum, UK. This research is funded by the Conclusion Leverhulme Trust. The fossil record suggests that hominin dietary capabilities changed greatly during the References Plio-Pleistocene. Developing a better under- Avery, D M 2001 The Plio-Pleistocene veg- standing of these changes is vital in order etation and climate of Sterkfontein and to further our knowledge of the behaviour Swartkrans, South Africa, based on mi- of our early hominin ancestors. The concept cro-mammals. Journal of Human Evolu- of using tooth wear, in association with the tion 41(2): 113–132, DOI: http://dx.doi. morphology of the teeth, to reconstruct the org/10.1006/jhev.2001.0483. diet of extinct mammals has a long history in Beynon, A D and Dean, M C 1988 Distinct palaeontology. It continues to be an impor- dental development patterns in early fossil tant focus of discussions on the diet of fossil hominids. Nature 335(6190): 509–514, DOI: hominins, but attention has focused on den- http://dx.doi.org/10.1038/335509a0. tal microwear; a systematic study of dental Benyon, A D and Wood, B A 1986 Varia- macrowear has never previously been made. tion in enamel thickness and structure This project will contribute in new ways to in East African Hominids. American Jour- our understanding of the early hominin diet nal of Physical Anthropology 70(2): 177– through the simplicity of its methods, as it 193, DOI: http://dx.doi.org/10.1002/ can be applied to most of the fossils so far ajpa.1330700205. discovered for the taxa of interest as well Boesch, C and Boesch, H 1990 Tool use as comparative material from chimpanzees, and tool making in wild chimpanzees. gorillas and orang-utans. The concentration Folia Primatologica 54(1–2): 86–99, DOI: on balance of tooth wear between different http://dx.doi.org/10.1159/000156428. teeth in the dentition enables a direct com- Bromage, T G and Dean, M C 1985 Re-evalua- parison to be made between younger and tion of the age at death of immature fossil older individuals with greatly differing over- hominids. Nature 317(6037): 525–527, DOI: all extents of wear. This is a central difficulty http://dx.doi.org/10.1038/317525a0. for other investigations of tooth wear which Cerling, T E, Mbua, E, Kirera, F M, Manthi, limits the comparisons they can make. It also F K, Grine, F E, Leakey, M G, Sponhe- limits their ability to consider variation in imer, M and Uno, K T 2011 Diet of Par- wear within taxa. The significance of our con- anthropus boisei in the early Pleistocene tribution therefore comes from our ability to of East Africa. Proceedings of the National consider differences between taxa within the Academy of Sciences 108(23): 9337– context of variation across the largest possi- 9341, DOI: http://dx.doi.org/10.1073/ ble groups of fossils and recent primates. pnas.1105808108. 68 Clement and Hillson: A New Study in Tooth Wear

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How to cite this article: Clement, A and Hillson, S 2013 ‘Do larger molars and robust jaws in early hominins represent dietary adaptation?’ A New Study in Tooth Wear. Archaeology International, No. 16 (2011-2013): 59-71, DOI: http://dx.doi.org/10.5334/ai.1605

Published: 24 October 2013

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