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Evolutionary Anthropology 17
Dental Microwear and Dental Function MARK F. TEAFORD
investigators have used many techniques to understand diet and tooth use in vestigators could never be sure of i.he prehistoric species. A promising new addition to the analytical arsenal is dental diet of specific individual animals. An microwear analysis-the study of microscopic wear patterns on teeth. On-going animal with lots of occlusal relief on its teeth may have eaten a preponderwork is proceeding on a number of fronts. Studies of modern animals are showing ance of soft h i t during its lifetime, some of the limits of resolution of the technique, while studies of prehistoric animals and we could never tell the difference are answering many new questions and raising still more in the process. Much work through analyses of tooth shape. remains to be done, but one thing is clear: if we proceed cautiously, we can provide new insights into the evolution of diet and tooth use.
TOOTH USE AND TOOTH WEAR
Prehistoric animals are often like least those of nonhumans) were based good mysteries: they leave us many on analyses of tooth shape.'" The clues, but we have to put those clues standard argument was that teeth of together to solve a puzzle. We would certain shapes are either more or less like to tease out of fossils information efficient in processing certain foods. about the diet of the animals in ques- Therefore, animals feeding on certain tion or at least some indication of how foods might be expected to have teeth they used their teeth. If we had such of a certain shape. Taking this a step information, then we could probably further, if you found teeth of a certain say something about other aspects of shape in a fossil, you might then infer their behavior, such as how the ani- what the animal had eaten. In the midmals moved and what kind of social 1970s, this work applied a tremendous organization they had. jolt to paleobiological interpretations, The plethora of teeth in the fossil as investigators rushed to see what record, together with the lure of pos- new insights they could gain into diet sible paleobiological interpretations, and tooth use in prehistoric animals.cs has left us with what, at first glance, This work, however, was not withseems to be an endless supply of litera- out limitations. Specifically,it focused ture on teeth. In reality, however, we on unworn teeth, effectively ignoring know surprisingly little about surpris- large portions of animals' lifetimes ingly much! during which they had worn teeth. What are the functional implications DIET AND TOOTH SHAPE of tooth wear? Only recently have inUntil a few years ago, most infer- vestigators begun to ask that quesences regarding prehistoric diet (at tion.gJ0 More importantly, because differences in tooth shape are ultimately products of evolution over many generations, analyses of tooth Mark F. Teaford is an associate professor of anatomy at the Johns Hopkins University shape have very finite limits of resoluSchool of Medicine. His research interests tion. In otherwords, the differences in include primate evolution and functional morphology. He has done extensive work tooth shape between closely related on primate tooth wear and morphology species, or within single species, using scanning electron microscopy and might be functionally meaningless. three-dimensional measuring microscopy. He has worked with museum collections, For example, if some people have laboratory animals, dental patients, and more occlusal relief on their molars primates in the wild, and he has also done paleontological fieldwork at various sites in than do other people, it probably says Kenya, particularly the Miocene sites on nothing about the amount of leaves Rusinga and Mfangano islands. those people eat. Moreover, since difKey words: teeth, tooth abrasion, SEM, primate, ferences in the shape of unworn teeth mammal are, again, products of evolution, in-
To better understand the intricacies of day-to-dayfunction amid the potentially confounding signals provided by tooth shape, some people have turned to studies of tooth wear. After all, tooth wear occurs during an animal's lifetime yet is preserved in the fossil record. If we can better understand tooth wear, then we might tap into a very useful source of information for paleobiological interpretations, one that does not depend on the assumptions about adaptation inherent in studies of functional morphology.' One way to document differences in tooth use has been through analyses of wear facets on teeth. Starting with the pioneeringwork of Butler and Mills,' 2-14 and continuing through the work of Crompton, Hiiemae, Hershkovitz, Kay, and Maier,6~8,15-17 investigators have mapped the location and orientation of facets on the postcanine dentition, and, through that work, documented variations in chewing and the evolution of chewing in many animals.ls.19Again, wear facet analyses are not without limitations. Of necessity they have focused on slightly worn teeth, those with wear facets still intact. No one really has looked at what happens to wear facets as wear progresses.20t21 By the same token, although the size of facets may be a useful indicator of such things as shearing crest use,22 no one has compared the size or incidence of facets between species. Thus, the presence or absence of molar wear facets may tell us a great deal about chewing movements and occlusion, but the take-home message
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many new questions in paleobiology. As a result, there is certainly excitement about it. But because it is so new, there should also be caution. With that in mind, we need to ask what we know and do not know about DMA.
Once a cast, a peel, or an original specimen is ready for examination, the scanning electron microscope is still the instrument of choice for most microwear analyses, largely because it provides better depthof focus and better resolution of detail than do standard light microscopes. Workers must take care in using the SEM, as subtle differences in contrast, working distance, and tilt of the specimen can translate into significant differences in microwear measurement~.~0,83 Early m icrowear studi e~~3-3639-46 usually involved qualitative assessments of microwear patterns. Teeth of various species were characterized as “pitted,” “scratched,”“polished.”This allowed investigators to note some obvious associations between microwear a n d diet (e.g., the preponderance of scratches on the teeth of grazing hyraxes).39However, it did not allow more subtle differences to be documented. More recently,2i~6s71~s4,s5 investigators have resorted to quantitative studies involving measurements of the size and incidence of microwear features and statistical comparisons of those measurements (Fig. 2). Although this work has allowed investigators to document more subtle dietary distinctions, it has
METHODOLOGY Figure 1. Application of dental impression materiais to a monkey.Photo courtesyandcopyright (1985) of David L. Brill.
is that analyses of molar wear facets have yet to reach their potential. As a different approach to documenting differences in tooth use, some investigators have turned to analyses of the gross amount of wear on teeth. This has proven particularly fruitful in studies of humans, where cultural differences in diet and food preparation techniques have led to interesting contrasts in tooth wear.23-26Studies of nonhuman primates have not been as n u m e r o u ~ ,probably ~ ~ - ~ ~ due to gaps in our knowledge of their diets and difficulties in measuring the amount of wear on three-dimensionally complex tooth surfaces. In either case, when all is said and done, studies of the amount of wear on teeth still leave us with a rather gross “measure” of tooth usethe accumulated effects of months or years of use, rather than a more instantaneous record of daily or monthly preferences.
One of the first questions people ask is, “How do you do it?”(see box). Most studies to-date have involved analyses of high resolution casts of museum specimens.21,48,49,52,63-71 Refinements in casting have provided researchers with remarkably stable materials that can accurately reproduce details down to tenths of a m i c r 0 n . 7 ~However, -~~ because the dental casting process is not some researchers have chosen to use thin varnish peels taken directly from the tooth, thus by-passing the preparation of positive casts.5356,58,59 Most dental impression materials are now “automixed”; that is, they are delivered in a caulking-gun-like syringe that automatically mixes a base and a catalyst together as the material is being put on the teeth. The mixed material only takes a few minutes to set. Thus, it is now relatively easy to make in vivo copies of the teeth of animals (Fig. 1)in addition to copies of the teeth of museum specimens. Cercocebus albigena Cebus apella
DENTAL MICROWEAR AS AN OPTION
Paranthropus Pongo pygrnaeus
+ + +
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Over the past few years, analysis of Pan troglodytes microscopic wear patterns on teeth Alouatta paiiiota has emerged as a method for dietary reconstruction and studies of tooth Australopithecus use. Of course, people have long been aware of scratches on teeth. Early Cebus nigrivittatus analyses of molar wear f a c e t ~ ~ J ~ - ~ ~ J O Colobus badius included information on scratch orientation as support for hypotheses Cebus capucinus about jaw movements. Some investigators even noted that species with difCoiobus guereza ferent diets might have different Gorilla gorilla patterns of scratches on their teeth.3l.Q But it was not until the late 2 4 6 8 10 12 1970s that a series of e ~ p e r i r n e n t a l ~ ~ - ~ ~ MICROWEAR FEATURE WIDTH ( p m ) and comparative studies4046opened people’s eyes to the possibilities of den- Figure2. Quantitative comparison of microweardimensions in a wide range of living pfimaYes and two early hominids, Austru/opithecus and Purunthropus. Puranthropus shows wider microwear tal microwear analysis (DMA). Today, features (i.e.,more pits).resemblinganimals that eat hard objects. Australopithecinedata courtesy this technique seems ready to answer of Frederick E. Grine. 1
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Evolutionary Anthropology 19
Studying microwear patterns in live subjects has greatly expanded our understanding of how dietary strategies and activity patterns are reflected in microwear features, but live subjects introduce a set of their own problems that must be monitored. The micrograph on the left is a baseline in which saliva and organic debris coat the tooth surface; the micrographon the right shows the same surface after that debris has been removed.
Unfortunately,methodologicalstandardizationhas yet to be attained in DMA. Indeed,there are nearly as many methods as there are investigators. Some methods are situation-specific and others are just a matter of taste. Some investigators prefer to work at lower magnification^,^^-^^ others at higher magnification^^^,^^^; some prefer to observe occlusal mi~rowear,~~,~8,~9,66-~~ while others study vestibular or buccal surface While the array of methods used in DMA can be quite daunting to the novice, DMAcan be used on many different types of samples each with its own advantages and disadvantages. Museum collections of modern animals offer the luxury of working with large samples that would be difficult or impossibleto study in the wild. The main drawbacks are that we often know painfully little about the collection dates and locations for museum specimens, and we rarely know anything about the diets of the animals in question. Some museum collections (e.g., the “Asian Primate Expedition” collections at the Museum of Comparative Zoology) are also coated with thick layers of preservative that must first be removed before DMA can proceed.
Museum studies of prehistoric materialface similar problems with the added burden of distinguishing useful premortem wear from useless postmortem wear. To the experienced eye, the latter is surprisingly easy to recogni~e,~l-~9,80 but to the novice, it can be a nightmare, as tremendous amounts of time can be wasted inadvertently “analyzing” artifacts. As might be expected, postmortem wear also varies from paleontological site to site and can drastically reduce sample sizes from some ~ i t e ~ . ~ ~ Studies of live, laboratory animals allow experiments with known diets. However, laboratory diets may be unrealistic models of natural diets at least as far as physical propertiesare concerned. Also DMA of large samples of lab animals (especially primates) is now virtually impossible due to the high costs of maintaining animals in captivity. Laboratory and field studies of live animals share two problems: usingthe appropriate anesthesiaand minimizing the effects of various organic films, such as saliva, on the teeth (see However, some deposits on teeth (e.g., plaque) obscure microwear and cannot be removed without creating new microwear patterns. ~
not been free of problems. Microwear measurements are generally computed through the digitizing of individual scratches a n d pits on micrographs. Thus, the entire process is extremely time-consuming-in some cases taking hours for a single micrograph. Some investigators 71,86,87 have tried to side-step this problem by digitizing only a fraction of the microwear features visible in a micrograph, but how representative are such sampling procedures? It is also difficult to define the boundaries of some microwear features at any mag-
nification,20 and some may be small enough (e.g., widths of fractions of microns) to exceed the limits of resolution of some digitizers. Finally, even with a series of measurements in hand, there is still the nagging question of the objectivity of those measurements. Specifically,if micrographs represent relatively small surfaces on the tooth, as certainly is the case in studies of large teeth at higher magnifications, then how comparable are the features in one area versus another?20.71In an effort to minimize the effects of this problem, most investiga-
tors try to restrict their work to specific wear facets. But, since microwear patterns may show subtle variations between areas on the same facet,*lss7 most workers still need to claim that their micrographs are taken of “representative” areas. Microwear patterns also show frequent variations between individual^.^^,^^^^^ Thus, for interspecific comparisons, samples must be large enough to represent with accuracy the variation of the species in question. At first glance, the easiest solution to many of these problems would
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seem to lie in image analysis. It is tempting to t h n k that we could somehow route the microscopic images into a computer, either by scanning, videotaping, or a direct electronic link between the microscope and the computer, whereupon image analysis could yield a quick, objective “measure” of microwear.88-91 Unfortunately, SEM micrographs of casts or natural teeth are extremely complicated images. Thus far, no method of image analysis has been able to yield the sorts of microwear measurements computed through digitizing. Even “semi-automated procedures90 a r e glorified digitizing procedures where the user still has to identify individual features for the computer. In the face of these difficulties, we may need to ask ourselves if we are taking too narrow a perspective on the methods of DMA. In other words, the key to obtaining objective measures of dental microwear quickly may lie in replacing the SEM with other measures of microtopography9*or abandoning the microwear measurements that have proven useful to-date. In either case, the transition would be difficult but welcome. The most pressing problem facing DMA is the need for efficient methodological standardization so that large samples can be processed quickly and objectively. To keep these methodological cautions in mind, we must remember that DMA is not as easy as we might hope. There certainly is room for further research into its methodological idiosyncracies. However, we must also not lose sight of the fact that DMA has already shed new light on a number of topics. What are some of the questions it has raised and answered? What questions remain to be answered?
EXPERIMENTAL STUDIES Given the potential of DMA in paleobiological studies, it is surprising how little experimental work has been done to establish the causes of specific microwear patterns. Many paleobiol o gi cal interpret a t i on s67,68,70,7 have been based on nothing more than simple correlations between the reported dietary habits of modern species and microwear patterns observed in modern species and fossils. Although such correlations may cersB8
tainly yield useful interpretations of fossils,93they will never set the limits of resolution of DMA. To do so, we need to know exactly how certain microwear patterns are formed. Ironically, the earliest “experimental” work had nothing to do with paleobiological interpretations, but instead was spawned by advances in microscopy, as investigators tried to
on teeth, and even between the shape of microscopic scratches and the direction of movement of abrasives relative to the teeth. However, subsequent work51,81,96-102emphasized the complexity of the entire process of dental microwear formation, and showed that some of the previous work was either oversimplified or, at the very least, in need of better documentation. Recently, however, more sophisticated experimental work has begun to The key to experimental bring investigations full circle. Correlations are once again being estabwork may well lie in the lished between the size of abrasive particles and the size of microwear use of more realistic features,lo3and between the hardness models of the oral of food items and rates and patterns environment. Given of dental m i c r o ~ e a rThat .~~ leaves ~~~~~~ experimental studies of dental mirecent advances in crowear with a great deal of work to dental impression be done. Although many investigators techniques, more talk about the processes that might cause observed microwear patemphasis must certainly terns,2 1,36-38,41,43,69,71, 100,1O4-l06 few of be placed on studies the associations between wear procinvolving live animals, in esses and microwear have been rigorwhich it is not necessary ously tested. We also know little about materials that actually abrade to mimic factors such as the teeth. As LucasIo7has shown, many chewing movement and food items are not hard enough to scratch enamel. That leaves us with salivation. For that either abrasives within foods, such as matter, studies of human phytoliths39J06 or exogenous abrasives volunteers could help to on food, such as dust,I06 as the causes of dental microwear in many species. sort through the causes Some studiesIo8 are trying to docuof specific microwear ment the relative effects of phytoliths and dust on dental microwear patpatterns. terns, but more work is clearly needed in this area. DMA is also raising many other establish the appearance of normal questions that can only be answered tooth surface^.^^,^^ These studies gave by experimental work. For instance, hints of possibilities-for instance, what are the effects of acidic foods on etched surfaces showed a preponder- dental microwear patterns?21JM(See ance of enamel prism detail, whereas Figure 3.) Can large and small microabraded surfaces showed a plethora of scopic pits on teeth be formed in disscratches. Unfortunately, little else tinctly different ~ays?36,69,1~.~O3.~05.~09 was done until a series of studies in the Can experimental studies recreate late 197Os.34-38These studies involved some of the patterns of microwear defairly simple experimental tests in scribed in qualitative st~dies?3~,~~,~3,’05 which teeth were abraded by hand- Only quantitative studies of large samheld materials or simple machines in ples will allow us to tell. The key to an attempt to mimic natural oral con- experimental work may well lie in the ditions. Initial results were encourag- use of more realistic models of the oral ing, as correlations were established environment. Given recent advances between the size of abrasive particles in dental impression techniques, more and the size of microscopic scratches emphasis must certainly be placed on ~~
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Evolutionary Anthropology 21
and Johanson6' also suggested that the orientation of scratches on chimp incisors may be related to the use of these teeth in the preparation of termite probes. But little else has been done, unless one considers leaf-stripping62J06J13to be a form of parafunction. By the same token, studies of toothgrinding have barely begun. One early study114suggested that the wear facets of tooth-grinders were scoured with heavy scratches. However, these conclusions were reached only after the teeth were also abraded with pumice. Thus the conclusions remain suspect. Microwear studies of tooth-sharpening in m a m m a l ~ lshowed ~ ~ , ~ that ~ ~ microwear patterns combining enamel prism relief with many small pits might indicate strict tooth-on-tooth wear. But the greatest area of potential for DMA of tooth-grinding involves the monitoring of clinical cases. In other words, if high resolution impressions can be taken from the same patient a few days apart, changes in dental microwear can be used to document the precise location and rate of tooth-grinding (Fig. 5).76-78Toothgrinding has been implicated, often controversially, as a possible cause of certain clinical syndromes, most notably temporomandibular joint syndrome. DMA may finally be able to document the true intricacies of tooth-grinding, including when and where it occurs and how it correlates with other oral functional symptoms. Figure 3. Micrographsof the same region showing the effects of acidic substances on microwear patterns. Figure 3a is the baseline micrograph; in Figure 3b. the finer microwear feutures are removed by the effects of a 2 to 3 second etching with a solution of 30% phosphoric acid.
studies involving live animals, in which it is not necessary to mimic factors such as chewing movement and salivation. For that matter, studies of human volunteers could help to sort through the causes of specific microwear patterns.
PARAFUNCTlON Dental parafunction is a catch-all term that is generally used to refer to any form of tooth use other than that associated with food processing. In primates, three obvious candidates for this category spring to mind grooming, chewing or gnawing on nonfood items, and tooth-grinding. Probably
the most well-known application of DMA to dental parafunction involves evidence of grooming in certain primates. Rose et a1.Il0noted that the incisors and canines of primates that use their anterior teeth for grooming have characteristic microwear patterns, and that similar patterns can be found on the teeth of fossil primates (Fig. 4). This work has since been extended to other species.111 By contrast, dental microwear studies of chewing or gnawing on nonfood items have barely begun. Ryan112 noted heavy microwear on the incisors of Eskimos who routinely use these teeth to chew tough hides. Ryan
ORAL FOOD PROCESSING, DIET, AND DENTAL MICROWEAR IN MODERN ANIMALS As Hiiemae and Cromptonl16 have noted, oral food processing in mammals involves three steps: ingestion, mastication, and swallowing. The last step may well involve incidental toothtooth contacts, but, thus far, DMA has not been used to study it. Ingestion and mastication, however, are another matter. Indeed, mastication has received far more attention than has ingestion.
Ingestion The introduction of food into the mouth has traditionally been viewed as more difficult than mastication to study by DMA, generally because ani-
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Figure 4. Microwear patterns also reflect nonchewing aspects of teeth, such as the mandibular toothcomb of a modern prosimian (40). The left incisor of a modern galago (Galago crassicaudatus, 4b) shows hair grooves on the median ridge (4c. above) and on the interstitial facet (4c. below). A close-up of the hair grooves on the interstitial facet (4d) can be compared positively to striations on the scanning electron micrograph of a Miocene loris, Nycticeboides(4e. 4f). From Rose et aI.,110 courtesy of K.D. Rose.
mals use their anterior teeth for parafunctional activities more often than they do their posterior teeth. Still, as Ungarlo6 has noted, even though parafunctional activities may make interpretations of incisor microwear difficult, this complicating factor may be cancelled out by the fact that anterior teeth probably undergo fewer tooth-tooth contacts than do posterior teeth. In any case, DMA of anterior teeth is still in its infancy, but has great potential for future research. The earliest studies focused on three microwear measurements of incisors: the orientation of scratches and the size and incidence of microwear features. The orientation of microwear was thought to reflect the movements of food across the teeth in ingestion,6O,ll3.Il7whereas the size and incidence of microwear features were thought to reflect the type of food, and abrasives o n food, being ing e s t e d . 5 2 ~ 6 0 ~ 6 1 ~ ~Specifically, ~ 3 ~ ~ * s ~ ~ 1the 9 incisors of animals that use these teeth extensively in food preparation (e.g., Cercocebus) or that habitually ingest
hard objects or abrasives on food (e.g., Pan o r Papio) showed heavier microwear and a higher incidence of microscopic pitting than did those of other animals (such as Gorilla). More recent work by Ungafl2sIO6has combined behavioral observation of primate feeding with microwear analyses of museum samples, with important results. As might be expected, the relationship between the incidence of incisor microwear and diet is probably more complicated than was originally thought, with both the abrasiveness of the diet and the overall degree of use of the incisors being important factors.Io6Moreover, Ungar has also raised the possibility of using DMA to document differences in feeding height, at least in some ecological zones. Specifically, because opal phytoliths are significantly larger than some soil particles (e.g., clay), arboreal animals may show larger incisor microwear features than will terrestrial animals, again within certain ecological settings.Io6On-going work with Alouatta paIliata77J08is beginning to
check this suggestion by looking at the relationship between exogenous grit and dental microwear. At this point, innumerable questions remain to be answered, including some of the most basic ones-for example, how consistent are these microwear patterns within a n d between species? Of course, given the many ways in which anterior teeth are used, more specific questions also spring to mind. For instance, do animals such as marmosets and sakis, which have large incisors, show characteristic incisor microwear patterns?
Mastication The initial step in the break-down of food is traditionally divided into puncture-crushing and chewing per se.Il6To date, DMA of mastication has focused on two different but obviously related topics: jaw movement and what we might call postcanine tooth use (with few distinctions being made between puncture-crushing and chewing). Although the relationship between
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Figure 5. Microscopicscratches and pits are replaced relativelyquickly.5a is a baselinemicrograph from a humansubject,and 5b is the same region micrographedone week later.Referencefeatures (labeled ‘R�) can be located in each micrograph, but virtually all other microwear features have changed wthin the week
jaw movement and the orientation of portantly, DMA has great potential for dental microwear features has long monitoringchangesin jaw movement in been a topic of d i s c u ~ s i o n , ~ little ~ - ~ ~living animals or dental patients.58J25 dental microwear work has focused Such changes might be the result of exon it, at least in modern pri- perimental or clinical procedures or m a t e ~ . 5 1 , 1In~ some ~ , ~ ~respects, ~ this is changes in jaw movement due to age or not surprising, for all living primates diet. For instance, how do jaw movehave fairly similar jaw move- ments change as the teeth become proments.2Jl6 Thus, DMA stands to show gressively more worn with age? Postcanine tooth use has been the us relatively little that is new in this area, and may reveal only subtle dif- focus of a great deal of work in DMA. ferences between or within species.51 Again, it started with qualitative asHowever, DMA has led to insights in sessments of microwear patterns certain nonprimate species in which showing differences in molar mibasic patterns of jaw movement are crowear in animals having broad diepoorly known.122-’24 Even more im- tary difference^.^^^^^^^ For instance,
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grazers had more microwear, particularly more scratches, than did browsers. Qualitative studies have continued to document microwear differences between animals or cultures with different diets.119,126125 However, qualitative studies have been followed by quantitative studies which have laid the groundwork for still more research. Work by G ~ r d o n ~ ~ - ~ O demonstratedthat biomechanical considerations needed to be kept in mind in all DMA. For example, micrographs needed to be taken of similar facets on the same teeth. Work by Teaford and Walker70 showed that DMA might even detect differences in animals, such as primates, with relatively variable diets. Specifically,they found that the teeth of primate folivores had relatively more scratches and fewer pits than did the teeth of primate frugivores (see Fig. 6). After the initial quantitative studies, DMA of modern animals moved ahead on two fronts: studies of museum material and studies of live, wild-caught animals. The ultimate goal of this work was to determine the limits of resolution of DMA, to see if this technique could detect more subtle differences in diet and tooth use than could be identified by other means. Museum work showed that DMA could reveal differences between molar microwear in animals traditionally grouped together as folivores or Some of these differences could be the result of general differences in diet between species, for example, a higher incidence of hard objects in the diet of Cebus apella than in that of C. capucinus,66or the more variable diet of Colobus badius than that of C. gueveza.I3OOther differences might be produced by seasonal changes in diet or ecological differences between site~.69,108J~~J~~ Surprisingly, there have been no indications of differences in dental microwear related to differences in body size. In primate folivores of a wide range of body sizes, dietary similarities seem to overwhelm any possible size differences.21.68 Correlations be tween dental microwear and underlying dental microstructure have also been hard to d o ~ u m e n t . In ~ ~some ~,~~~ cases, this may be because dietary
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24 EvolutionaryAnthropology
Molar Microwear in Modern Primates 45
-u
Folivores
Frugivores
Figure 6 . This bar chart demonstrates the increased percentage of pits on the tooth surfaces of primate frugivores vs. the homologous surfaces in primate folivores.
abrasives overwhelm microstructural ses of these specimens are ultimately effects. In other cases, it may be that at the mercy of published dietary studour measures of microstructure have ies. Thus, museum studies certainly been too crude for the task at hand. have finite limits of resolution. DeClearly, summary-type statements spite this fact, what we've seen thus far about prism packing patterns for a in the way of DMA of museum mateparticular tooth or species are insuffi- rial is just, so to speak, the tip of the cient. Dental microstructure is an ex- iceberg. Although on-going work conceedingly complex phenomenon, but tinues to reaffirm certain early concluas we better understand its variabil- sions (e.g., that hard foods probably DMA ity,I34-137 we may better understand its cause pitting on teeth),84,85J38-142 relationship to dental microwear. has only been performed on a small Right now, only the usefulness of range of samples from a limited numscratch widths in animals with drasti- ber of areas. Furthermore, there have cally different microstructure has been few studies of modern human pop~lations.47.53.60.61,143,144 Innumerbeen called into q u e ~ t i o n , I 3a~n,d~ ~ ~ the fact remains that DMA of closely able questions remain unanswered. related species, or the same species, For instance, what variations might be has documented intriguing differ- found in the dental microwear of huences in scratch widths that may be man populations from western and related to differences in diet.67,106 The nonwestern cultures? What sort of best ways to avoid the complicating ef- dental microwear variations might be fects of dental microstructure seem to detectable on other teeth, such as the be to use teeth from closely related premolars? Can DMA document difspecies and to restrict DMA to the ferences between closely related spesame location on teeth having similar cies (such as Cercopithecus) that live in amounts of wear. It's not clear what the same habitat or that habitually the effects of deviations from those form polyspecific associations? Can DMA document dietary differences guidelines might be. Obviously, many museum collec- in rare species (e.g., species of Gotions have relatively poor data on the rilla) that are either difficult to study dates and locations of capture speci- in the wild or apt to disappear in the mens. Moreover, we rarely have de- next few generation^?^^^-'^^ Are tailed dietary information regarding there age-related changes in dental individuals represented in museum microwear that accompany age-recollections. For this reason, our analy- lated changes in dental morphol-
0gyY7 Only further work will tell. Clearly, studies of live, wild-caught animals would help to answer some of these questions. Until a few years ago, such studies were routinely unsuccessful. Fortunately, advances in dental impression techniques a n d primate capture techniques have now improved the odds dramatically. Thus far, a study has begun on Alouatta in Costa R i ~ a , ~ ~ J ~ 8 J ~is~focused w h i c hon seasonal and ontogenetic changes in dental microwear. Another study, on Propithecus and Eulemur in Madagascar,"+6is more closely tied to correlations between the physical properties of food items and rates and patterns of dental microwear. Results are just beginning to surface, but already there are some interesting hints of possibilities. The Costa Rica howlers are showing more dental microwear in both the dry season and in certain microhabitats within their dry tropical forest locale. 10*,145 They are also showing more microwear than museum collections of the same species collected from wetter ecological z0nes.7~Results are also confirming what had been previously hypothesized based on gross dental morphology: howlers use their molar shearing facets more than do primates with more bunodont teeth.77 The Madagascar prosimians are showing microwear differences related to observed dietary differences, again with a frugivorous lemur (EuZemur) showing a higher incidence of pitting than a less frugivorous one (Propithecus). However, the frugivorous species is showing no evidence of chemical etching by acidic fruit. 146 As for future work on live, wild primates, there are, again, many possibilities. Probably the most pressing need is for data from different species and different ecological zones, including as much information as possible on exogenous abrasives in the diet and the physical properties of food items. As in studies of jaw movement and parafunction, another area of vast potential involves dental clinical studies. Initial work78,147 has already shown that daily or weekly changes in dental microwear can be used to monitor tooth use in a clinical setting. Pilot work is now underway on a number of fronts-for example, rates of tooth wear are being compared in patients
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from different cultures and in patients with certain eating disorders (such as bulimia). However, much more is possible. For instance, can age-related changes in tooth use, in the very young and very old, be related to changes in diet and/or tooth morphology?
INFERENCES ABOUT DIET AND TOOTH USE BASED ON PALEONTOLOGICAL AND ARCHEOLOGICAL SAMPLES Obviously, much of the impetus for DMA is based on its paleobiological potential. As noted earlier, analyses of paleontological and archeological material are made more difficult by the vagaries of taphonomy, particularly postmortem wear, which can severely limit the number of teeth in a sample. As a result, what we have is a patchwork of studies on such samples. Some topics have been covered in far more detail than others, but many topics remain to be examined. What kind of questions have been asked and answered about tooth use through such analyses? Studies of anterior tooth use have certainly been made more difficult by the range of activities that can involve these teeth. Still, DMA has proceeded on a number of fronts. For instance, it has been used to document early examples of the mammalian tooth~omb.~~OJ~8,149 It has also focused on the use by Homo sapiens of its anterior teeth as tools-tentatively verifying the long-held suspicion that Neandertals used their front teeth as ~ o o ~ sand , ~pointing ~ ~ J to~interesting ~ possibilities of anterior tooth use during the N e o l i t h i ~ . ’ ~However, * J ~ ~ all of this has been based on qualitative analyses of small samples. It would be extremely interesting to see what more detailed analyses might uncover. As for anterior tooth use related to feeding, all that is available is work involving two groups of primates: Miocene hominoids and early hominids. Kelley’s qualitative survey’l 8 showed that, while most Miocene hominoids were probably frugivorous, some, such as Proconsul major, used their incisors either more often or to process more abrasive foods than did others, including Proconsul nyanzae. Early hominid work has involved more detailed, quantitative analyses ulti-
Evolutionary Anthropology 25
mately spawned by the age-old question of whether or not there are differences between the australopithecines. The answer, at least insofar as the anterior teeth are concerned, seems to be yes. Although all australopithecines examined to date have exhibited relatively heavy incisor microwear,6’J 12,154 the combination of more microwear and less enamel prism relief on the incisors ofAustralopithecus afvicanus (as compared with Paranthropus robustus) suggests that the gracile australopithecines were using their incisors more frequently to process abrasive DMA has also reaffirmed previous suspicions about the australopithecine canine premolar complex-that it was put to a number of uses and was not merely a shearing or honing a p p a r a t ~ s . Obviously, ~~,~~ it would be nice to see incisal microwear studies extended to other fossil hominids such as the robust australopithecines from East Africa and early members of the genus Homo. But more importantly, what about other animals? Clearly we could use work on ancestors of modern species with known diet differences, for example, colobines and cercopithecines. However, analyses of species with interesting canine morphology and no modern analogues (e.g., Parapithecus) might also be intriguing. Analyses of the posterior, or postcanine, teeth have focused on three topics, the first being, once again, animals with no obvious, or agreed upon, modem analogues. The fossil record is replete with animals exhibiting unusual combinations of morphological features. Where such combinations of features have never been seen before, DMA has provided at least the first direct evidence of their use.65J55-158 Where a fossil’s dental morphology is not quite so distinct, DMA has helped sort through options proposed for its use,21
,67,70,159
The second topic of interest in postcanine DMA involves closely related species suspected, on the basis of other morphological parameters, of having dietary differences. The most familiar of these studies again involve the early hominids. Unfortunately, much of what has been pulled into the literature from these studies is based on early qualitative assessments of small
samples. Thus, various descriptive terms have been used to characterize the diets of early hominids, including chimp- or baboon-like for the East African robust australopithecines,46 tough and abrasive for Homo erectus ~ ~ ,acidic ~ ~ for H. and A. a f a r e n s i . ~ ,and habilis.59,’m Some or all of these assessments may be true, but until we have detailed statistical comparisons that are based on samples of reasonable size, and take adequate account of postmortem wear, they all must be viewed cautiously, to say the least. Clearly the most thorough study so far has been that of Grine and co-workers on the South African australopithec i n e ~ , @,86,88 ~ ~ ,which ~ has demonstrated that Paranthropus consistently has more molar microwear, especially more pitting, than does Australopithecus (Fig.2). This result is particularly intriguing in light of the previously cited work on incisor microwear,Is4in which Australopithecus showed significantly more microwear than did Paranthropus. How could Paranthropus show more microwear on its molars, but less on its incisors? The most obvious answer would be that it habitually processed foods that required little incisor preparation154in essence, “popped them into its mouth by hand. Given the molar microwear patterns of Paranthropus, something in or on the food was probably hard and abrasive, and the food itself must have required extensive masti~ation.~~.86 Has DMA brought us back to Jolly’s seed-eater hypothesis’lboPerhaps, but only further work on the East African australopithecines will tell. There are many other closely related species for which differences in diet or tooth use are suspected. For instance, several studies have focused on the evolution of jaw movement44Jf”J62 and tooth use6s65 in nonprimate mammals. But again, relatively few prehistoric species have been the subject of DMA. In addition, many studies have yet to be completed. Analyses of African fossil monkeys and apes are still in progres~,68,8~.~~3,’6~ but they are already yielding some surprises. Some of the fossil apes are showing differences that might not have been expected. For example, Proconsul nyanzae has less microwear than (does
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26 Evolutionary Anthropology
Because dental microwear features can appear and disappear quite q u i ~ k l y , ~ ~DMA - ’ ~ has the potential to give the first “Polaroid” snapshots of paleobiology: evidence, from an evolutionary instant, directly from the surface of the fossil. Admittedly,other new paleobiological tools can come close to such claims. Analyses of dental microstr~cture may ~ ~outline ~ the history of dental development for specific individuals and bone isotope or trace element analyses’68 may give a cumulative summary of the diet of individuals. Still, the fact remains that, unlike analyses of dental microstructure, DMA can give us informationfrom any stage in an animal’s lifetime or at least any stage at which the animal has teeth! Moreover, unlike bone isotope or trace element analyses, DMA can give us a picture of diet and tooth use over a very short period of an animal’s lifetime daily, weekly, or monthly (see figure). This is not to say that DMA is somehow “better” than the other approaches. Each has its strengths and weaknesses, and each can answer its own set of questions. The point here is that, unlike analyses of tooth shape, DMA tells us what an animal did, not what it was theoretically or evolutionarily capable of doing. Thus, it has the potential to document subtle differences in diet and tooth use that have previously been undetectable. As far as analyses of closely related
species are concerned, there are age-oldquestionsthat we can now at least try to answer with the help of DMA. For instance, if we could document the variability of prehistoric diets, we might shed light on the relative importance of “critical iterns”5,l69vs. “primary spe~ializations”~~~~0 in the evolution of dental morphology. For that matter, in large, well-dated sequences of fossils, such as the Eocene primates of Wyoming,171we might obtain some of the best evidence yet of the relationship between behavioral and morphologicalchange in the fossil record.
P heseloni.164 On the other hand, some had different diets. The favorite topics of the fossil monkeys, specifically, the here involve dietary changes brought colobines and cercopithecines of the on by the onset of agriculture, cookTurkana Basin, are not showing the ing, o r new contacts between culmolar microwear differences exhib- ~es.57.67,83,104,126,127.1 39-142,172,173 As might ited by their modern counter- be expected, such studies need to have p a r t ~ .This ~ ~may , ~ help ~ ~ sort through adequate indicators of the food prepavarious hypotheses concerning the ration techniques used by the people evolutionary or ecological divergence in question, for some techniques may of Old World monkeys and apes,165s166actually add abrasives t o the 27,172 A s in inters peci f ic but more definite statements must diet.57,67,87,1 await the results of on-going DMA of comparisons, such studies cannot rely other fossil catarrhines, including solely on tiny samples where there has monkeys from other Plio-Pleistocene been no control for postmortem wear. sites in Africa, as well as Victoriapi- When adequate control of these facthecus and the Fayum primates. tors is exercised, however, DMA can The third, and final topic of interest document changes in the hardness or in postcanine DMA of prehistoric sam- abrasiveness of diets. It may even yield ples involves intraspecific comparisons information about weaning practices of humans suspected,on the basis of as- in different prehistoric peoples.56,57J74 sociated archeological remains, to have Possibilities for future work include
better documentation or corroboration of the onset of agriculture in various parts of the world, and even examination of differences in diet between sexes, between individuals of different age or status, and between geographc locales within a particular culture. Such work would be particularly useful if done in conjunction with other analyses, such as bone isotope work, that can also shed light on diet.
CONCLUSIONS In the last 10 to 15 years, a great deal of microwear work has been done on a variety of samples. That work has laid the groundwork for innumerable research opportunities. Such possibilities generate excitement. But there
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should also be caution and concern. Yes, we may be able to answer new questions using these techniques, questions that may, in turn, shed light on many larger issues. But there is also a very real danger that many people won’t even bother to learn the strengths and weaknesses of the technique, and will merely rush into microwear studies of their favorite fossils or archeological samples. One point to emphasize here is that DMA is a relatively new approach that is going through the normal growing pains of any young analytical technique. In short, it often raises more questions than it answers. As it becomes more and more popular, its practitioners must never forget to proceed cautiously For DMA to truly reach its potential, we need to establish its limits of resolution, and that requires careful work on a variety of samples, most notably modern animals with known diets and known patterns of tooth use. We must also remember that DMA is not the ultimate answer to questions of tooth use and dietary reconstruction-ultimate answers to those questions could only be provided by a time machine! Instead, it is merely one of a number of approaches that can be applied to paleobiological interpretations. If we keep these cautions in mind, then DMA probably can help us find answers to questions that have, until now, eluded us, and questions we’ve never even asked before.
ACKNOWLEDGMENTS This work could not have been completed without the help of many people. Special thanks go to Rose Weinstein, Courtney Burnell, Vivian Noble, and Bob Pastor for their technical help. Additional thanks go to Ken Glander, Rich Kay, Meave Leakey, Bob Pastor, Peter Ungar, and Alan Walker for thought-provoking discussions and/or comments on the manuscript. Ken Glander and David Brill kindly allowed access to photographs, and Meave Leakey (National Museum of Kenya) and Richard Thorington and Linda Gordon (Smithsonian Institution) kindly allowed access to specimens in their care. This work was supported by NSF grants 8904327and 9118876,and Biomedical Research Support Grant SO7 RR05378.
Evolutionary Anthropology 27
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9634896-0-7. $10.00 (paper). Gill SD, Sullivan IF (1994) Dictionary of North American Mythology. New York: Oxford University Press. xxx + 425 pp. ISBN 0-19508-602-3. $15.95 (paper). Hall BK (ed) (1994) Homology. The Hierarchical Basis of Comparative Biology. San Diego: Academic Press. 512 pp. ISBN 0-12-318920-9$54.95 (cloth). Iwamoto M (ed) (1994) Morphology of the Japanese Macaque. Anthropological Science V. 102 (Supplement). vi + 205 pp. ISSN 0918-7960. Lyman RL (1994) Vertebrate Taphonomy. Cambridge: Cambridge University Press. 576 pp. ISBN 0521-45215-5 (cloth), 0-521-45840-4 (paper). Owsley DW, Jantz RL (eds) (1994) Skeletal Biology i n the Great Plains. Washington, DC: Smithsonian Institution Press. xii + 408 pp. ISBN 56098-093-1. $45.00 (cloth). Parker ST, Mitchell RW, Boccia ML (eds) (1994) Self-Awareness i n Animals and Humans: DevebDmental Perspectives. New York Cambridge
University Press. ISBN 0-52144108-0. $59.95 (cloth). Plotkin H (1994) Darwin Machines and the Nature of Knowledge. Cambridge: Harvard University Press. xviii + 269 pp. ISBN 0-674-19280-x. $27.95 (cloth). Rackham J (1994) Animal Bones. Interpreting the Past Series. Berkeley: University of California Press. 64 pp. ISBN 0-520-08833-6. $10.OO (paper). Savage-Rumbaugh S, Lewin R (1994) W Z I : The Ape at the Brink of the Human Mind. New York: John Wiley and Sons, Inc. 320 pp. ISBN 0-471-58591-2.$24.95 (cloth). Shipman P (1994) The Evolution of Racism: Human Differences and the Use and Abuse of Science. New York: Simon and Schuster. 3 18 pp. ISBN 0-671-75460-2.$23.00 (cloth). Straus LG (1992) Iberia Before the Iberians: The Stone Age Prehistoty of Cantabrian Spain. Albuquerque: University of New Mexico Press. xiii + 336 pp. ISBN 0-8263-1336-1. $40.00 <cloth).
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Books Received Bruhns KO (1994) Ancient South Americans. Cambridge: Cambridge University Press. ISBN 0-521-25907 (cloth), 0-521-27761-2(paper). Carpenter K, Hirsch KF, Horner JR (eds) (1994) Dinosaur Eggs and Babies. New York Cambridge University Press. xiv + 372 pp. ISBN 0-521-44342-3. Chamberlain A (1994) Human Remains. Interpreting the Past Series. Berkeley: University of California Press. 64 pp. ISBN 0-520-08834-4 $10.00 (paper). Corruccini RS, Ciochon RL (eds) (1994) Integrative Paths to the Past: Paleoanthropological Advances in Honor of E Clark Howell. Engelwood Cliffs, NJ: Prentice Hall. xx + 716 pp. ISBN 0-13-706773-9. Crews DE, Garruto RM (eds) (1994) Biological Anthropology and Aging: Perspectives on H u m a n Evolution over the Life Span. New York: Oxford University Press. mi + 445 pp. ISBN 0-19-506829-7.$75.00 (cloth). Ecker RL (1993) The Evolutionary Tales. Pelatke, FL: North Bridge Books. xii + 212 pp. ISBN 0 -
Articles in Forthcoming l ~ 5 u e s Multiple Dispersals and Modern Human Origins Marta Mirazon Lahr and Robert Foley
Locomotor Energetics and Hominid Evolution Karen Steudel
Genetic Admixture Robert C. Williams
Growing up to be a Primate Steven R. Leigh
Predationon Primates: Ecological Patterns and Evolutionary Consequences Lynne lsbell