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Applications of Scanning Electron Microscopy to Taphonomic Problems * PAT SHIPMAN Department of Earth and Planetary Sciences The johns Hopkins University Baltimore, Maryland 21218

T

to reconstruct past environments and hominid behaviors have only four sources of information: (1)geological evidence; (2) the preserved remains of various hominid and nonhominid species; (3) occasionally, artifacts fashioned and used by our near or distant ancestors; (4) imagination or divine inspiration. Given that the last of these is difficult to use in persuading critics and that the interpretation of artifacts and geological exposures is best discussed by others, I shall focus in this paper on the fossil or osteological evidence of once-living animals and its interpretation. Powerful as such evidence may be in providing glimpses of the past, it is vulnerable to massive distortion. Various agents that act on bones and teeth during the postmortem and predepositional period differentially destroy, preserve, transport, or concentrate skeletal elements until an assemblage may bear little resemblance to the animal community (or bone community) from which it was drawn. As a taphonomist, I must ask of each assemblage how badly it misrepresents the original collection of bones or species. This question underlies all attempts at paleoecological reconstruction. Answering it is equally important whether the assemblage has been retrieved from an archeological stie only a few thousand years old or from a paleontological site many millions of years old. In order to answer this question, various studies1-15of modern processes of death, decay, and dispersal of bones have been carried out. HOSE WHO TRY

* Funding for the research reported in this paper was provided by grants from the Boise Fund and The National Institutes of Health Biomedical Research Program (#5 SO 7 RR07041-13) and is continued by the National Science Foundation (BNS 80-1397).

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However, even as our knowledge of how to interpret the past has expanded, one stumbling block has remained: museum collections. These are problematical because of the great changes in excavation and documentation techniques over the last 100 years. For example, to identify the agent that has concentrated the bones into an assemblage, we look to geological evidence (Is the site a lake bed or overbank deposit?) or spatial distribution data (Are the bones aligned in one predominant direction? Are the bones clumped or evenly distributed? Do they occur in articulated units?) that are often missing or poorly documented even in sites excavated as little as 25 years ago. Further, many paleontological or archaeological sites have been incompletely collected. Piles of ”poor specimens” or ”indeterminate fragments” - which in reality, can be identified if sufficient time and expertise are available-are often left at the site or hurriedly stuffed into bags to be dumped in some inconvenient location (the museum basement) and forgotten. This too-common occurrence means that there is a twofold sampling of the original assemblage: first, by survival of taphonomic events and second, by the selection process of the excavators. Worse yet, museums are full of surface-collected material, for which such data are not available no matter how meticulous the researchers were. It might be concluded that museum collections are useless from a taphonomic or paleoecological point of view and ought to be scrapped, save for a few relatively complete specimens for other types of studies. Nothing could be further from the truth. I have utilized a technique and developed a data base that permits the extraction of a maximum amount of information about the taphonomic history of a bone directly from the specimen itself. The level of confidence with which this approach can be used is high enough to compensate for lost or unrecorded data and sufficient to warrant its application even when modern standards of excavation and documentation are met. The premise underlying the research is simple. As any observant researcher dealing with fossils or bones has noticed, specimens frequently show signs of surface damage. Often, intuitive assessment of the causes of such damage are reported.lb-21It is clear that prior to the unfortunate effects of careless excavation or preparation, such damage is caused by the set of destructive, postmortem agents that reduces the original bone assemblage, made up of all the remains of all animals that die, to that fraction which is preserved, buried, and later excavated. But how do these destructive agents -carnivores, tool-bearing hominids, rivers, weather, plants, and so on-attack the bones? And what accounts for the survival of some elements and the complete destruction of others?

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It is well doc~mented4-~.22 that the differential survival of skeletal elements is a result of the interaction of the structure of these elements with the destructive agents to which they are exposed. Vertebrae, for example, are often transported out of depositional areas because they have a high ratio of spongy to compact bone and thus float easily.19.23~4The same structural constraints make the articular ends of long bones more vulnerable to destruction by hungry predators than the denser shafts.25 Researchers in mechanics and materials science26 have related the mechanical strength of a bone, or part of a bone, to its microscopic structure. Thus the differences in resistance to fracturing under compression between, say, fibulae and femora, may be due to the differences in the percentage of vascular channels or of poorly mineralized new bone in the area in question. For this reason, I have examined, at a microscopic level, the interaction of various destructive taphonomic agents with bones to determine how these agents attack the bone structurally and to document the results of this attack. The marks resulting from the agents investigated to date have proven distinctive and, therefore, diagnostic of the event that caused them. Thus, the presence of similar marks on bones or fossils can be used to deduce the taphonomic events to which that specimen was exposed. The theoretical justification for the approach used lies in an updated version of the uniformitarian principle. As Simpson27 has pointed out, all historical sciences are concerned with retrodiction, or the tracing of past events, rather than prediction per se. Because both paleoanthropology and taphonomy are historical sciences, certain constraints are imposed on the methods appropriate for answering taphonomic and paleoanthropological questions. Such science must depend on the modern concept of uniformitarianism - what some workers call actualism~8~29 - in which an understanding of the causal mechanisms by which given events produce given effects is achieved. Then, if these effects are manifested in historical data, the existence of the corresponding events can be deduced. Simps0n2~proposes the following three-step approach that is appropriate for investigations in historical sciences: 1. studying and understanding the causal mechanisms and processes by which modern events produce particular effects; 2. obtaining and ordering the historical data (the evidence of various effects); and 3. confronting the historical data in the light of the knowledge of modern processes and deducing that particular events have occurred.

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An explicitly Simpsonian approach was used in the research discussed here. Step 1was made up of the detailed SEM analysis of the microscopic effects of various known taphonomic events on modem bones and teeth and the discovery of the causal mechanisms by which the effects are produced; Step 2 involved making and inspecting replicas of the surfaces of fossils of unknown taphonomic history; and Step 3 was the evaluation of the evidence of past events preserved on the surfaces of the fossils from which the taphonomic history of each specimen will be deduced. It is only through carefully formulated applications of the uniformitarian principle (as redefined by Simpson) that any knowledge of the past can be gained. An objection that might be raised to the approach proposed here is that it assumes that taphonomic events in the past were the same as those observed today. In fact, the underlying assumption of this approach is distinctly different from that criticized by this objection. It is not assumed that the past is the same as the present, for it is apparent that environments, whole animal communities, species and species' behaviors can and do change over time. Instead, it is assumed that however much the details of species, environments and communities may change, the physical, mechanical, and chemical principles by which alterations in bones and teeth are produced do n0t.3~The emphasis on discovering and understanding the causal mechanisms by which particular events produce particular effects is therefore essential to this research. Further, care must be taken in interpreting the fossil record so that the appropriate level of resolution of the results is not exceeded. Conclusions must take the form, for example, that "this fossil shows marks that best match those produced by the solution of bones and teeth by the gastric juices of owls" rather than "this fossil was swallowed by an owl." Given the constraints of retrodiction inherent in working in an historical science, this is an acceptable and, in fact, optimal level of resolution. Because the focus of this research is on the interaction of taphonomic agents with bone on a structural level, all specimens were inspected using the scanning electron microscope (SEM). The SEM offers several advantages over conventional light microscopes, including superior resolution of three-dimensional structures, greater depth of field, and the capability for higher magnification of specimens. Inspection of the same specimen with a light microscope and the SEM has shown that the latter often reveals features that are unclear or invisible under the light microscope euen when the magnifications are the same (FIG. 1A & B). Although the SEM offers considerable advantages, its use necessitates

FIGURE1. Comparison of light and scanning electron microscopy (all dimensions are in millimeters). A. A n experimental s de with a stone tool on a bone, The photograph was taken with a Leitz Orthoplot microscope and Orthomat camera. The po d of this light microscope makes it difficult to see the features of the slicing mark. B. The same area of the same mark shows ail when photographed at a comparable magnification with the Etec Omniscan scanning electron microscope.

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replication of specimens because: (1)even a large-chambered SEM (such as the ETEC Omniscan I use) cannot accept specimens larger than 4 in X 2 in X 1 in; and ( 2 )it is necessary to coat specimens with 200 of goldpalladium to prevent charging effect^,^' but it may be undesirable to coat original specimens. Fortunately, Walker3*,33 has developed a technique that produces replicas with a resolution of .25 microns or less. Xantopren blue coldcure silastomer (Unitek Corp., Monrovia, Calif.) is used to make a mold of the desired surface that is demarcated with plasticine; Araldite epoxy resin (Ciba-Geigy Corp., Ardsley, NY) is used to make a positive from this mold, which can then be coated, mounted, and inspected. The original specimen, once cleaned of miniscule particles of Xantopren and plasticine, is entirely unharmed and unaltered. To date, several hundred specimens representing the effects of taphonomic agents on modern and fossil bones, have been investigated in this way. These agents are:

A

1. Tooth marks made by nonhominids a. tooth scratches b. gnawing marks c. punctures 2. Cutmarks made by hominids with stone artifacts a. slicing marks b. scraping marks c. chopping marks 3. Preparators’ marks made on fossils with metal tools 4. Spiral fracturing a . by weathering b. by hominids 5 . Burning of bone in fires 6. Weathering 7. Root-etching by grass plants 8. Abrasion by sedimentary particles 9. Digestion by predatory mammals and birds.

These nine taphonomic agents or events include some of the best-known destructive forces to which bones might be exposed and those judged to occur most commonly. Obviously, some were chosen because of their potential for revealing information about the behaviors of our ancestors. Although the total number of specimens inspected so far is in the hundreds, the sample size for some events is small and results must therefore be treated as preliminary.

FIGURE2. Gross inspection is not always sufficient to distinguish between tooth marks and cutmarks (all dimensions are in millimeters). A. A replica of several tooth scratches on a bone. The original replica is 21 mm long in maximum dimension. B. A replica of several slicing marks made on a bone with a stone tool. The original replica is 11.5 mm long in maximum dimension.

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The first three events investigated - tooth marks, cutmarks, and preparators’ marks-were treated as a set. These events were expected to, and found to, produce grossly similar marks, so distinguishing among the different causes of such marks is important. Imputing the damage seen on ancient bones to hominids’ activities is controversial.21~3*~36 Therefore, it is suggested that this explanation be used only when two critera are fulfilled: (I)the alterations or damage observed are congruent with hominid activities, as judged against a control sample; and ( 2 ) the alterations or damage are demonstrably different from that known to be caused by nonhominid agents. That is, only the distinctive attributes of the damage or alteration can be considered diagnostic, since many events may produce grossly similar results. It is important to demonstrate that the effects seen can be distinguished from random noise. Upon gross inspection, tooth marks and tool marks of various sorts can be indistinguishable (FIG.2); but at higher magnifications, profound differences can be detected that relate directly to the mode of production of the marks. The following types of tooth or cutmark have been defined and criteria developed for their recognition, based on a sample of modern bones chewed by feral carnivores or rodents and an experimental sample cut with newly made stone a r t i f a ~ t s . 3 ~ A tooth scratch is produced by drawing a pointed tooth cusp across the surface of a bone as the animal closes its mouth (FIG. 3A). This type of mark is probably most often made by carnivores‘ canines. Tooth scratches are elongate grooves that may vary from V-shaped to U-shaped in cross-section, depending on the morphology of the tooth cusp. The bottom of nadir of the groove is smooth. Tooth scratches may occur on bones singly, as sets of parallel or subparallel marks, or as clusters of marks, or as clusters of marks differing widely in orientation. The functional equivalent of a tooth scratch produced by a stone artifact is a slicing mark. Slicing marks are produced by drawing the edge of a stone artifact across the surface in a direction continuous with the long axis of the edge. The result is an elongate groove that may or may not be narrower than a tooth scratch, depending on the artifact and tooth cusp used. Slicing marks may be V-shaped in cross-section and always show multiple fine striations within the main groove and parallel to its long axis (FIG. 3B). These fine striations are drag marks or tracks made by the fine projections that deviate to one side or the other of the edge of the artifact (FIG. 3C). Too, microscopic pieces of stone or bone dislodged during the cutting process may also create such striations. It is

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important to note that all slicing marks inspected to date (N

=

40) possess these striations and that none of the tooth scratches (N = 40)

do. It seems likely that there is considerable selection pressure working to keep the enamel surface of pointed tooth cusps sufficiently smooth that small pieces do not break off and expose the tooth to the danger of infection. Grossly similar marks are also made by preparators or excavators when metal tools slip and scratch the surface of the bone or fossil. Preparators' marks may be very fine and only barely visible without magnification. Although generally similar in shape to tooth scratches, preparators' marks have very irregular, scalloped edges (FIG. 3D) that have not been observed in tooth scratches. Of course, preparator's marks on bones or fossils will not contain any matrix and may be lighter in color than the adjacent bone surface. Punctur~sare produced by the concentration of a biting force through a single tooth cusp, often a canine, at an angle roughly perpendicular to the bone surface. The result is a depressed fracture with rounded, roughly circular outline. In some cases, microscopic fragments of bone can be seen pushed inwards into the surface (FIG. 4A). Punctures may have a stepped appearance because the area of depression is greatest at the bone surface and decreases as the distance from the surface increases. Chopping marks are produced in a manner functionally similar to that responsible for punctures: a stone artifact is used to strike a bone surface with a blow directed roughly perpendicular to the bone surface. Because the edge of the artifact is not drawn across the bone but is rather pushed in it, there are no striations. Chopping marks are broad and V-shaped in cross-section; like punctures, they often show fragments of bones crushed inwards at the nadir. Unlike punctures, chopping marks are elongated ovals or grooves in outline (FIG. 4B). FIGURES 5A and B show the third functional group of tooth and tool marks: gnawing and scraping marks. Gnawing marks result from a biting action in which an animal's upper and lower incisors are drawn across a bone towards each other as the animal closes its mouth. Rodents, from mice to porcupines, carnivores (especiallyjuveniles), and some herbivore~3~,4~ are known to gnaw bones for reasons ranging from the need to trim down ever-growing incisors to nutritional deficiencies. The resultant marks are broad, shallow, flat-bottomed grooves that may have fine striations. Often, there are two or more gnawing marks parallel and adjacent to each other on a bone. Gnawing marks are the only type

FIGURE4. Comparison of functionally equivalent marks made by striking a bone with teeth and tools (all dimensions are in millimeters). A. A puncture made by a carnivore's tooth on a rib. The stepped appearance of the depressed area and the nearly circular outline are typical. B. A chopping mark, made with a greywacke chopper on a bone. Left: The V-shaped cross-section and elongate outline of the chopping mark are apparent at low magnification. Right: A twofold increase in magnification reveals the fragments of bone crushed inwards at the nadir and the lack of fine striations that are typical of chopping marks.

FIGURE 5. Comparison of functionally equivalent marks made with teeth and tools (all dimensions are in millimeters). A. A gnawing mark made by a rodent’s incisors on a pig phalanx. Such marks are typically broad, shallow, and flat-bottomed. They often occur as a parallel series of marks and may or may not show fine striations, depending on the morphology of the incisors. B. This scraping mark was made by drawing a stone tool across a bone in a direction roughly perpendicular to the long axis of the edge. Diagnostic of scraping marks are multiple fine, parallel striations covering a broad area rather than being confined to a clear groove.

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of tooth or tool mark that I have been able to identify consistently from gross inspection in a blind test. Scraping marks are the equivalent to gnawing marks. They are produced by drawing an artifact across a bone surface in a direction roughly perpendicular to the long axis of the edge. The result is a series of fine parallel striations across a broad area of bone that may lie below the general level of the bone surface but in which there is no readily identifiable nadir. In contrast to slicing marks, then, scaping marks are not confined to a main groove (FIG. SB). The distinctions among these various types of marks are clear if the SEM is used and the specimens carefully prepared. Marks possessing all of the criteria of these various types of marks have been observed on fossils, most notably on a sample of 85 marks from 75 fossils from Olduvai Gorge, T a n ~ a n i a . 3The ~ importance of removing all preservatives and glue before replicating a fossil cannot be emphasized too strongly, since such substances completely obscure the relevant characteristics of the underlying marks. It has been possible, using this approach, to document the earliest known uses of stone artifacts on animal tissues from Olduvai sites dating to 1.79 +- .03 million years,37,41 and to distinguish the results of such activities from carnivore activities. In addition, because it is possible to deduce the sequence in which marks were made if they overlap one another, another somewhat surprising fact about the Olduvai fossils has been documented: in many instances, a single bone will show both toothmarks and tool marks and, in a few specimens, toothmarks overlap tool marks. This means that carnivores scavenged remains already processed by hominids, and, with larger sample size, it will probably be shown that hominids scavenged remains from carnivores as well. That this competition for carcasses or bones occurred even when one species had already processed the bones suggests that perhaps eating the meat off of the bones was not the only or primary purpose for which early hominids desired bones. This is supported by an analysis of the location of the various types of marks (TABLE 1).Nineteen bones bearing cutmarks and 36 bones bearing tooth marks can be identified as to skeletal element in the replicated Olduvai sample. The skeletal elements in question were classified either as nonmeat-bearing (metapodia, podia, and vault bones of bovids and equids) or meat-bearing (all other skeletal elements). The distribution of the cutmarks and tooth marks reveals that cutmarks occur with nearly equal frequencies (N= 9 and N = 10)on these two categories of skeletal elements, but tooth marks occur substantially more often (N= 29 vs. N

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TABLE 1 Number of Specimens

Type of Mark Slicing

2

2 2 1

1 1 1 1 1 1 1 1 1 1 1

Scraping

2

Chopping

1 1 1

Tooth marks*

12 6 4 3 3 2 2

1 1 1 1 1 1 1 1 1 1 1 1 1 1

Anatomical Location Metatarsal shaft Radial shaft Long bone shaft Humeral shaft Metacarpal shaft Proximal ulna Distal metacarpal Rib shaft Tibial crest Proximal radius Scapular blade Humeral shaft Radial shaft Metatarsal shaft Long bone shaft Metacarpal shaft Metapodial shaft Proximal phalanx shaft Long bone shaft Long bone shaft Proximal rib Humeral shaft Rib shaft Femoral shaft Tibial crest Proximal metacarpal Scapular glenoid Proximal ulna Radial shaft Radioulnar shaft Mandibular corpus Hyoid Parietal Proximal femur Acetabulum Distal tibia Fibular shaft Metatarsal shaft Cuneiform Indeterminate fragment

* Toothmarks include tooth scratches, punctures, and gnawing.

+ = meat-bearing;

-

=

nonmeat-bearing; 7

=

unknown.

Meat Bearinnt

-

+ 7 ++ + + + + + +-

7 -

7 7

+ + + + ++ + + + + + + + + + +7


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= 6) on meat-bearing elements. A Chi-squared test reveals that these distributions are significantly different ( x 2 =5.39585, with one degree of freedom: p < .03).Since the makers of the tooth marks (mainly carnivores) can be assumed to be primarily interested in meat-eating, the distribution of tooth marks is not surprising. However, because the distribution of cutmarks is substantially different and includes nearly equal numbers of each type of bone, it may be that the hominids making these marks were not solely interested in obtaining meat from the bones (contra Isaac42). In fact, they were apparently as interested in some other substance (skin? tendon or ligament? periosteum?) as they were in meat, judging from these data. This finding throws an entirely different light on the origins of processing animal carcasses with stone artifacts. It is possible, and perhaps even likely, that the earliest uses of stone artifacts on bones were to obtain tendons or other tissues for binding or tying things together . Three objections might be raised to this interpretation. The first is that the sample of tooth- and cutmarks on identifiable skeletal elements (N= 54) is biased and thus nonrepresentative of the total population of marks. I consider this alternative explanation for the perceived differences in patterns to be very unlikely. The total sample of replicated marks was chosen by Rick Potts43 during a study of Olduvai materials and was not selected for this particular study. Potts also chose that sample without regard to either skeletal element or type of mark, the latter of which could not be determined prior to our collaborative ~ o r k in 3 ~any case. The second objection that might be raised is that bovids butchered by Paleo-Indians in North America of ten show cutmarks on their metapodia and podia. However, such marks are actually the result of skinning44 or tendon removal rather than meat procurement per se, which fact supports my interpretation. Finally, it might be argued that the skin or other substances removed from these areas by early hominids were discarded as waste material -the cellophane wrapper on the package, by analogy-and were not sought or utilized in and of themselves. This is a reasonable alternative hypothesis to mine and I cannot see any way of testing whether the removed substances were utilized or discarded. Spiral fracturing of bones was also investigated because this type of breakage is often, controversially, attributed to hominid actions.21,24,26 Two types of spiral fractures, differing in their microscopic structure, have been distinguished during SEM examination. Type I spiral fractures occur in bones fractured by natural weathering or trampling.36 The frac-

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ture plane apparently lies between two adjacent bundles of collagen fibers, which can be seen on the fracture surface as elongate, stringlike structures (FIG.6A). The parallel laminae and the intervening networks of vascular channels are clearly visible in the compact bone of a tibia1 shaft with a type I fracture. Any agent (weathering, trampling, hominids, or carnivores) that creates a spiral fracture either by producing torque in a direction consistent with the predominant collagen fiber direction or by breaking the bonds between adjacent bundles of fibers will make a type I fracture. Type I1 fractures, in contrast, run perpendicular to the predominant fiber direction (FIG.6B). The fracture surface is characteristically roughened and stepped. The path of the propagating fracture front apparently follows the course of a single lamina for a short distance, then traverses that lamina obliquely until intersecting another lamina, which is then followed for a short distance, and so on. The effect is rather like the path taken by a crack in a brick wall. Type I1 fractures can be caused only be agents capable of exerting torsional stress sufficient to overcome the structural strength of the bone; such fractures cannot occur from such passive agents as weathering or trampling. Further work is in progress to determine the proportions of type I and type I1 fractures that can be expected to occur in carnivore-damaged and hominid-damaged assemblages. Another possible hominid interaction with bone was investigated: burning, or the direct exposure of bone to flames. Burning of defleshed bones for as little as 15 minutes creates a distinctive suite of characteristics that can be used to identify burned bone even in the absence of free carbon as charring. The heat denatures the collagen sufficiently to produce not only longitudinal cracks, such as are commonly seen in weathering3 but also transverse cracks. These latter are caused by the recoiling of the ends of broken collagen fibers that are normally under tension in the bone. The intersection of the growing longitudinal and transverse cracks, which are not superficial as they are in weathering, may naturally quarter bones (FIG. 7A). In addition, polygonal cracking occurs on the areas of subchondral bone. Such bone, underlying articular cartilage in life, is highly vascular. Heating propagates cracks between adjacent foramina, thus delineating polygonal plates. As the heating drives water out of the bone structure, the edges of these plates are forced outwards, rendering the plates concave. Comparable cracking has not been observed in bones subjected to any other agent, although mosaic cracking (compare FIG. 7B and 8F) is grossly, but not microscopically, similar.

FIGURE6. Spiral fractures (all dimensions are in millimeters) A. A typical type I spiral fracture produced by weathering of a topi tibia. Left: A low power micrograph of the fracture surface shows parallel structures. Right: A twofold increase in magnification of the area in the box shows that these structures are the laminae of the bone, separated by networks of vascular canals seen in section. B. A type I1 spiral fracture was produced on the same tibia by manual application of torsion in a direction perpendicular to the naturally occurring spiral fracture shown in FIGURE6a. Left: The characteristic stepped and roughened appearance of type I1 fractures can be seen in this micrograph. Right: A twofold increase in magnification of the area in the box shows the perpendicular intersection of the fracture front with the lamellae.

FIGURE 7. The effects of burning on bone (all dimensions are in millimeters). A. This sheep phalanx was exposed to direct flame for 15 minutes. The longitudinal and transverse cracks produced by heating have intersected to quarter the bone. B. The subchondral bone on the distal articular surface of the phalanx shows that cracks propagate among vascular foramina, delineating polygonal plates. Additional heating causes the plates to curl upwards at the edges in a characteristic pattern.


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Weathering, which can be an important paleoenvironmental and taphonomic indicator, has also been examined. Weathering breaks bones down by changes in state: from wet to dry, hot to cold, frozen to thawed. Behrensmeyer3 has defined five weathering stages based on modern bones from Amboseli National Park, Kenya; similar stages can also be observed in fossils16.17~45.FIGURE 8A-F presents a preliminary model of how weathering occurs on a microscopic and structural level. All specimens used in this analysis were collected from semiarid plains in East Africa; no attempt was made to establish the rates of weathering for these bones. Although Gifford46 and Behrensmeyer3 have calculated weathering rates in areas with comparable habitats, weathering rates can vary tremendously in different microhabitats within the same overall habitat. However, it is clear from their work and from work in Canada (Haynes, personal communication) that bones may maintain their structural integrity for 10-15 years, although the first signs of weathering may appear in less than one year. Once weathering rates are established in a variety of habitats, it may be possible to set maximum and minimum limits on the length of time a fossil or ancient bone assemblage was exposed to the elements prior to burial from knowledge of its weathering stage. Another useful paleoenvironmental indicator that was investigated is root-etching. The specimens used in this part of the study were those of a dog that had died less than one year prior to excavation. The bones ranged from entirely buried to entirely unburied: trampling by cows was responsible for burial when it occurred. In all cases, the plants whose roots had etched the bone were savannah grasses. It can be seen in FIGURE9A-D that tiny rootlets invade and eventually enlarge all naturally occurring foramina on the bone surface. The growing roots secrete acids that dissolve the bone matrix and transform the smooth-edged foramina into scalloped-edged holes. The surface of the bone is partially dissolved as well and becomes highly sculptured or billowed in appearance. The presence of such surface damage and irregular foramina can be used as direct evidence of the existence of vegetation in the substrate to which the bones were buried. It is not expected that different plants will produce distinctly different types of etching. Digestion of bones by various mammalian and avian predators has also been examined. Although small vertebrates are generally sensitive indicators of microhabitats,48,49 they are often useless as paleoenvironmental indicators because their bones have been transported by water or

FIGURE8. Microscopic effects of weathering (all dimensions are in millimeters). A. Weathering stage 0.There is no alteration of the natural bone surface. 8. Weathering stage

1. Tiny longitudinal cracks appear (see arrows); the woven texture of the bone is the normal appearance of immature bone. C. Weathering stage 2 . A brickwork pattern is formed

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predators far from the area in which the animals lived.50 Korthsl has suggested techniques for identifying fluvially transported assemblages of microvertebrates, but Mellett52 has suggested that microvertebrate fossils are most often collected in the stomachs and digestive tracts of predators. Bones from scat of striped hyenas, wolves, spotted hyenas, coyotes, and from regurgitated pellets from six species of owls (Strigiformes) and five species of hawks, eagles or falcons (Falconiformes) have been inspected. In all cases, digested bones share the following common characteristics:

1. Hairs are present in vascular foramina or in other holes in the bones, down to the size of Haversian canals. Although hair itself is unlikely to be preserved, DeNiro (personal communication) has suggested that recognizable traces of keratin may be preserved in digested and fossilized bones. 2. Bone surfaces show solution effects that take the form of the loss of surface bone, the exposure of Haversian systems and osteocyte lacunae, and thinning and rounding of broken edges. 3. Where extensive solution of the bone has occurred, it is most pronounced at the metaphysis where trabeculae are commonly exposed. 4. Teeth show varying degrees of solution effects, ranging from the etching of enamel and dentinal tubules to the complete destruction of roots and dissolving of most of the enamel crown52 (see FIG. 10A-D). These features apparently vary in their severity with the pH of the gastric juices of the species in question and the length of time the bones are in the stomach. Teeth seem to be a more reliable indicator of digestion effects than bones, in which the presence of epiphyseal plates may greatly accelerate the creation of solution effects. It is possible to distinguish between skeletal remains digested by Falconiformes and Strigiformes, which are known to have gastric juices of significantly different pH.54 In all specimens examined to date, (N = 48) molars digested by as transverse cracks intersect the already-existing longitudinal cracks. A puncture is visible in the lower lefthand corner of the micrograph. D. Weathering stage 3. Propagation of diagonal cracks and widening of these cracks into valleys creates a diamond pattern typical of this stage. E. Weathering stage 5. Continued weathering results in the loss of much of the external bone, leaving a highly disorganized and sculptured surface. F. Mosaic cracking. This type of weathering is often found on subchondral bone. The pattern is formed by polygonal mounds of bone separated by broad valleys linking adjacent vascular foramina.

FIGURE9. The effects of root-etching (all dimensions are in millimeters). A. Grass roots cover nearly the entire surface of this bone, which is visible only in the center of this micrograph as a flat surface. B. A close-up of the central area of FIGURE9A shows tiny rootlets invading naturally occurring foramina. Note the smooth outline of the foramina. C . The difference between root-etching (left) and normal bone surface is marked. The former is highly sculptured by criss-crossing channels. D. A close-up of that root-etched area shows that the foramina have been enlarged by the rootlets that invaded them. The outlines of the foramina are now ragged and scalloped.

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FIGURE10. Variability in the effects of digestion by raptors (all dimensions are in millimeters). A. A rodent humerus swallowed by a long-eared owl shows that the gastric juices attacked the epiphyseal cartilage and the adjacent bone more strongly than the mid-shaft region. Rodent hairs protrude from some of the holes dissolved into the bone. €3. A distal radius of a rodent eaten by a screech owl. All of the external bone is digested away, leaving only cancellous bone into which many tiny rodent hairs have been driven. C. A rodent molar digested by a barred owl. The roots are opened up and the enamel is somewhat eroded, but the tooth is basically intact. D. An occlusal view of a rodent molar eaten by a golden eagle. The roots are completely digested away and all of the enamel has been stripped off, save areas at the left and center where there are deep infoldings of enamel. All that remains of this tooth is the dentin that originally underlay the enamel crown.

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Falconiformes have lost some or all of their enamel whereas those digested by Strigiformes have not. The fossil record of the nocturnal Strigiformes and overwhelmingly diurnal Falconiformes goes back to the Eocene,55 so by inference it may be possible to establish both that a particular small animal was eaten and that it was nocturnal or diurnal, as judged from the type of predator that ate it. It is hoped that further controlled experiments will reveal criteria that will permit identification of major groups of mammalian predators, as well. Finally, abrasion by windborne or waterborne sedimentary particles was investigated. Such abrasion is known to occur in bones washed down rivers as well as those left on the land surface in areas of high and persistent winds. In both cases, surface bone is removed, exposing the internal structure of the element (FIG. 11A & B). The thin layer of compact bone overlying cancellous bone may be removed by scouring in much the same way that a pebble caught in a depression creates a hole in a larger rock. Abrasion of compact bone may open up vascular channels lying just beneath the surface and push fragments of bone into them. Although it is unclear how long a bone must be exposed to fluvial transport or aeolian abrasion to produce different degrees of alteration, further experimental work may provide these data. This review of the preliminary results of my work demonstrates the enormous potential for gleaning useful information from museum specimens. Various hominid activities (processing of carcasses, bone breaking, burning) can be distinguished reliably from the activities of other agents of damage, based on the microscopic characteristics of the resultant marks. In addition, a range of paleoenvironmental indicators can be recognized, such as the effects of root-etching, weathering, abrasion, or digestion by predators. Although much more work is needed to quantify results, enlarge sample sizes, and explore possible sources of variability in effects, these preliminary results are encouraging. A great deal of taphonomic information is encoded in the damage on bone surfaces; all that we need to decode it are the proper techniques, good control samples, and an adequate understanding of the processes by which bones are damaged. ACKNOWLEDGMENTS

I thank Karen Davis, Wendy Bosler, Jennie Rose, Linda Perez, Dan Kiehart, and Pat Maurice for technical assistance. Help and advice in Kenya were provided by Richard and Meave Leakey, Francis Kamaruga,

FIGURE11. Abrasion by windblown sand (all dimensions are in millimeters) A. Abrasion of this metapodial has produced pockmarks or pits and has opened up vascular canals that originally lay just under the bone surface. B. A close-up of one such canal reveals the fragments of bone pushed into the canal.


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