Dental microwear and diet Implications for determining the feeding behaviors of extinct primates with a comment on the dietary pattern of Sivapithecus.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 55:331-336 (1981) Dental Microwear and Diet: Implications for Determining the Feeding Behaviors of Extinct Primates, With a Comment on the Dietary Pattern of Sivapithecus HERBERT H. COVERT AND RICHARD F. KAY Department of Anthropology, Duke Uniuersity, Durham, North Carolina 27706 (H.H.C.)and Department of Anatomy, Duke University Medical Center, Durham, North Carolina 27710 (R.l?K.) KEY WORDS Dental microwear, Diet, Jaw movements ABSTRACT Dental microwear is of special interest for two reasons. First, it has been proposed that specific dental microwear patterns are associated with specific diets and therefore that the diets of extinct forms may be deduced by analysis of microwear. Second, it has been suggested that the geometry of wear striations indicates the direction of masticatory movement. We tested these ideas by analyzing microwear of laboratory animals fed different diets. Twelve American opossums (Didelphis marsupialis) were fed soft cat food for 90 days. Two control animals were fed only this base diet, five animals had plant fiber added to their diet, four animals had chitin added to their diet, and one animal had fine ground pumice added to its diet (for the last 30 days of the feeding period). We examined the wear surface below the paracristid on the Ms and M, of each animal by SEM. No microwear pattern differences were observed on the plant fiber-fed,chitin-fed, or control animal's molars. The pumice-fed opossum had a distinct microwear pattern with many parallel striations, resembling those foundon the teeth of grass-eating hyraxes (Walker et al., 1978).These results suggest that 1) exogenous grit (this study) or plant parts containing opaline phytoliths (Walker et al., 1978)produce similar microwear patterns, and 2) the diets of extinct forms cannot always be deduced by the analysis of dental microwear. The absence of fine parallel striations on teeth of Siuapithecus examined by us suggests that grass parts were not an important part of its diet and that it avoided dietary fine grit. Furthermore, we found striations on opossum molars with deep, broad heads and shallow, narrow tails oriented in opposite directions on the the same Phase I wear facet. This suggests that the geometry of striations on Phase I wear facets does not allow one to determine the direction of masticatory movement. Recent interest has focused on the use of scanning electron microscopy (SEM) to study dental wear in primates and other mammals. Evidence of microwear patterns has been advanced to support hypotheses about dietary pattern and/or differential tooth use, as well as to make inferences about jaw movements during mastication and other oral activities. If microwear distinctions can be recognized and firmly established for many sorts of diets and oral activity patterns, this method of analysis would provide an important adjunct for 0002-9483/81/5503-0331$02.00 0 1981 ALAN R. LISS.INC. determining the oral behavior of extinct primates. At present, we can make reliable generalizations about these behaviors in fossil primates only based on the structure of their teeth by analogy with those of living species with known oral behavior. Similarly, if it can be established that the conformation of wear is indicative of the direction of movements during tooth-tooth contacts this would be an Received April 18. 1980: accepted December 29. 1980. 332 H.H. COVERT AND R.F. KAY important adjunct to in vivo studies of jaw movements in the intercuspal range. In one well-documented instance, enamel microwear was shown to be altered by a seasonal variation in diet. The enamel microwear of two sympatric hyraxes, Procavia johnstoni and Heterohyrax brucei, were analyzed by Walker et al. (1978) using SEM. The microwear of the two species was similar during the dry season when both browsed on bush and tree leaves. However, during the wet season Procavia johnstoni ate grass and its microwear was quite distinct from that of Heteroliyrax brucei, which remained strictly a browser. The molar enamel of grass-eating P. johnstoni was covered with many fine parallel striations, possibly produced by opaline phytoliths in the grasses. Work is presently underway by Walker and colleagues who hope to use other similar “natural-experiments” to recognize dietary patterns. Because of the potential that microwear studies may have for dietary interpretations of extinct species, it would be desirable to make comparisons of microwear among many animals with a variety of different diets. In most instances, however, data of the sort used by Walker et al. (1978) is unavailable. A museum specimen is practically never accompanied by information about its diet covering the interval of several months before its death. An alternative strategy followed here is to feed specially formulated diets to laboratory animals and analyze the resulting dental wear. An added advantage of this approach over studies of feral animals is that there can be more precise control over all aspects of the dietary pattern, allowing one to consider and eliminate possible complicating dietary factors. Laboratory studies of the sort reported here provide data about which food constituents produce wear (and which do not). Clearly, if we cannot establish diagnostic criteria for specialized dietary regimes in a controlled laboratory situation, it would be overly optimistic to expect to interpret dietary patterns of extinct species based on wear except in special, unusual circumstances. Ryan (1979a,b)investigated the relationship of the direction and shape of microwear striations to the direction of tooth movement. He found, in in vitro studies simulating masticatory movement, that the initial point of contact between striation-forming grit and tooth surface was often deeper and wider than the rest of the striation, which tapers in the direction opposite to relative tooth movement. Ryan concluded by examining dental microwear that the direction of tooth movement in mastication could be determined. He documented several cases where wear striations produced in vivo during Phase I mastication, for which jaw movement direction is known, had the predicted configuration. The data supplied by our studies allow us to evaluate critically the studies of Ryan. In this study we compare the pattern of enamel microwear developed on the molars of American opossums (Didelphis marsupialis) fed specially prepared laboratory diets which include plant fiber, chitin, and dietary grit (pumice) - three materials which could produce enamel striations on the teeth of feral mammals. We examine the implications of our findings with respect to the use of microwear for assessing the diets of extinct species and for the determination of jaw movement direction during mastication. MATERIALS AND METHODS A laboratory experiment has a major advantage for studying the pattern of enamel microwear which is lacking in a study of animals in their natural habitat. Because there is precise control over what the animals eat, more certainty is possible concerning the agent causing the wear patterns. We selected the American opossum as our research animal because its masticatory behavior is well understood (Crompton and Hiiemae, 1970), and because opossums will readily eat a variety of foods. Twelve animals were selected whose lower left third molar was little worn. The criterion of selection was that each of the trigonid cusps (paraconid, metaconid, and protoconid) have little, if any, dentin showing on the leading edge of the shearing crests. Each animal was fed daily 184 gm (one can) of the base test diet, “Friskies Buffet - liver and chicken parts” for an initial 4-day habituation period. This diet is soft and free from abrasives or grit which could cause wear on the opossum’s teeth. After 4 days the diets of nine of the 12 animals were changed. To simulate a “herbivorous” diet, 15% (by dry weight) plant fiber (coarsely ground soybean hulls, particle size range of 3 to 9 mm) was added to the diets of five animals. To simulate an “insectivorous” diet, 15% (by dry weight) chitin (particle size range of 3 to 9 mm) (supplied by United States Biomedical Corporation, Cleveland, Ohio) was added to the diets of four animals. Three control animals were DENTAL MICROWEAR AND DIET fed only the base diet, All animals were continued on these diets for 90 days with one exception. One of the control animals was fed 90% base diet and 10% finely ground pumice (by dry weight) for the last 30 days of the feeding period. The 15% plant fiber is taken as a reasonable approximation of the amount of this constituent incorporated into the diet of herbivorous primates, For example, the leaves eaten by the primate herbivore, Presbytis johni, contain 27% to 69% plant fiber (by dry weight), and this species eats leaves 46% of the time (Oates et al, 1980),giving an overall figure of 13-34% fiber in the total diet. The chitin content of insects ranged from 3 to 8% (by dry weight) for five species examined by Tsao and Richards (1952). We have found that crickets contain approximately 10% chitin. The 15% chitin added to the opossums’ diet is a slightly higher quantity than the chitin ingested by insectivorous primates. The 10% grit added to the diet of the opossums may be a less realistic approximation of grit content in the natural diet of any primate, but it may be supposed that animals which root and dig for their food may include close to 10% soil in their diet. At the end of the 90-day feeding period the opossums were sacrificed. The left M, and M, were extracted from each mandible, cleaned with a water-pik (Sears Aqua Jet by Water Pik), and allowed to dry. The molars were rinsed in acetone, mounted on metal stubs, and sputter-coated with approximately 200 A AuPd alloy under a vacuum in a “Film-Vac Inc. mini-coater.” Each tooth was given a code number different from the animal’s number so that the researcher examining the teeth by SEM would not be prejudiced by the knowledge of the animal’s diet. The wear surface below the leading shearing edge of the paracristid was examined on each molar at various magnifications under a JEOL-T20 scanning electron microscope. Special care was taken to examine each tooth at a nearly identical orientation and location, about normal to the leading shearing edge of the paracristid, as diagramed in Figure 1. This surface was chosen for examination because it is the primary Phase I shearing surface on the lower molars of Didelphis (Crompton and Hiiemae, 1970). Micrographs were taken at this location on all specimens at the same magnification ( X 350) to allow for comparisons of microwear patterns. The overall appearance of the wear surface was recorded including the approximate 333 Fig. 1. Didelphis marsupialis. Anterolateral view of A, the lower left molar series and B, M, (of the same molar series), illustrating the orientation used in this study to analyze the microwear pattern of Phase I wear facets. The stippled area on B indicates the wear facet examined on each molar. number of striations and their size, shape, and orientation. In addition to analyzing the microwear on these molars, we obtained an Indian Siuupithecus specimen (high-precision casts were generously supplied by Dr. P.D. Gingerich) and examined the microwear on a Phase I shearing surface (facet la). ENAMEL WEAR AND DIET The microwear patterns of representative animals fed various diets are shown in Figure 2A-D respectively. There are no qualitative differences between the microwear patterns of the plant-fiber-fed, chitin-fed, or control groups in these micrographs or in others taken on the remaining animals. The microwear of most specimens (Fig. 2A-C) is relatively smooth, with a few pits and striations oriented in various directions. In contrast, the wear surface below the leading edge of the pumicefed opossum (Fig. 2D) has relatively rough wear with few pits and a great number of parallel and relatively uniform-sized striation. This pattern of microwear is quite distinctive from that of the other opossums and appears to be similar to the microwear pattern of the grass-eating hyrax figured in Walker et al. (1978). These results lead us to conclude that it is not always possible to deduce the diets of animals from their microwear patterns. Thus, 334 H.H.COVERT AND R.F. KAY Fig. 2. Didelphis marsupidis. Micrographs ( X 350) of microwear pattern on wear surface below the paracristid on lower left (right for C) molar of A,plant-fiber-fed animal, B. chitin-fed animal, C. control animal, and D.pumice-fed animal. E. Siuapithecus sp. Micrograph ( X 350) of microwear pattern on Phase I wear facet ( # l a )on upper right first molar. while specific wear patterns may be produc- ed by a specific diet (for example, all chitin-fed animals have similar microwear), these wear patterns may not be diagnostic for a particular diet (the plant fiber and chitin-fed animals have similar microwear). This sug- gests that in many instances molar wear patterns may have little resolving power for determination of diets of fossil animals. An alternative interpretation of these results is that 90 days (the length of the feeding period in this experiment) may not be 335 DENTAL MICROWEAR AND DIET long enough for animals to develop dietspecific wear patterns. We consider this unlikely for two reasons. First, as noted above, Walker et al. (1978) report that microwear patterns change seasonally in one hyrax species. The dry season is only 5 months long and animals sampled during the dry season had distinctly different wear patterns than those in the wet season. This suggests that microwear patterns are changing in less than 150 days. Second, in this study, one animal had a very distinctive wear pattern after having pumice added to its diet for 30 days, demonstrating that dental microwear can change quite rapidly. While dental microwear may not always allow one to deduce the diets of fossil animals, these data are potentially informative in some cases. As reported above, the pumice-fed animal has a wear pattern similar to that of grass-eating P. johnstoni. An important structural component of grasses is opaline phytoliths. Baker et al. (1959) suggested that opaline phytoliths may be the major agent causing dental wear in sheep. They reported that plant opal is harder than enamel (5.5-6.5 for opal and 4.5-5.0 for enamel on Moh’s hardness scale), lending credence to the suggestion of Walker, et al. (1978)that opaline phytoliths are the agent causing striations on the teeth of P. johnstoni. If wear facets on teeth lack fine parallel striations then this animal probably excluded exogenous grit andlor grasses or other plants with hard particles from its diet. Such a conclusion is interesting in light of the wear pattern we observed on a molar of Siuupithecus (GSI D-185). This molar had a smooth wear pattern with few pits or striations (Fig. 2E), suggesting that this animal was not eating food containing exogenous grit or grasses or other plants containing phytoliths (at least during the time period immediately preceding its death). ENAMEL WEAR AND JAW MOVEMENT DIRECTION In Didelphis the majority of wear striations below the leading edge of the paracistid are parallel to the direction of Phase I jaw movement during mastication. Most striations are of nearly uniform width throughout their length. Those which have a deep, wide head and narrow, shallow tail like that described by Ryan (1979a,b)do not always or even typically have the tapered tail in the direction opposite tooth movement. contrary to Ryan’s suszes- tion. Figure 3A-C shows striations from the same Phase I wear facet. These micrographs were made a t various magnifications, all within the range utilized by Ryan. In Figure 3A the head of a striation points toward the leading edge of the paracristid, whereas in Figure 3B the head points in the opposite direction. If the paracristid occludes only in Phase I mastication and hence, in one direction as described by Crompton and Hiiemae (1970), Ryan’s contention that masticatory direction can be deduced by striation geometry is not supported. Further evidence that does not support this hypothesis is seen in striations below the paracristid which have their deepest enamel penetration in the middle, with shallower and narrower tails occurring at both ends of the striation (Fig. 3C). SUMMARY A knowledge of the diets of extinct primates is essential for understanding their evolution. Currently, we can make a few generalizations about the diet of extinct primates on the basis of the relative development of shearing, crushing, and grinding features on their molars (e.g.,Kay, 1975). The study of dental microwem also has proved useful as a means of distinguishing browsing from grazing dietary regimes (Walker et al., 1978). Here we have attempted a preliminary assessment of whether one can recognize other diets based on the wear characteristics of the teeth. This was done by feeding different diets to opossums for 90 days in a controlled laboratory environment and examining the dental wear. We were unable to distinguish between the microwear of the plant-fiber-fed, chitin-fed, or control animals. Thus, we cannot expect to distinguish between the microwear of insectivorous or herbivorous fossil primates. Dental microwear data are informative in some ways. The opossum with pumice added to its diet has quite distinctive microwear, similar to microwear of the grasseating hyrax described by Walker et al. (1978). This suggests that the analysis of microwear can provide information that animal ate grit or parts of plants containing silica. The smooth wear observed on the Siuapithecus specimen we examined suggests that this animal was excluding grass and exogenous grit from its diet. We also examined the geometry of wear striations on the Phase I wear facet below the Daracristid. On the basis of Rvan’s 11979a.b) 336 H.H. COVERT AND R.F. KAY Fig. 3. Didelphis marsupialis. A. Micrograph ( X 1,000)of a striation with a deep, broad head and shallow tail pointing away from the paracristid. B. Micrograph ( X 1,500) of a striation with a deep, broad head and shallow, narrow tail pointed toward the paracristid (on same molar as A). C. Micrograph ( X 350) of a striation which is deepest and broadest in its middle, with shallow and narrow tails at both ends of the striation. In all instances, the paracristid is located a t the top of the micrograph. experimental work it would be predicted that these striations would have a deep wide head and shallow, narrow tail oriented away from the leading edge of the paracristid, parallel to the direction of mastication. We found striations with this geometry, with the opposite orientation, and with a deep, wide middle section with shallow and narrow tails at both ends. This suggests that Ryan's hypothesis about the geometry of striations and their relationship with the direction of mastication is incorrect. ACKNOWLEDGMENTS This work was supported by NSF grant BNS-77-08939 to R.F. Kay. We thank Susan Hutchinson for her help with the SEM. We also thank Dr. K. Rose who read and commented on this manuscript. LITERATURE CITED Baker, G. Jones, LHP. and Wardrop, ID (1959) Cause of wear in sheep's teeth. Nature 184:1583-1584. Crompton. AW, and Hiiemae. K (1970)Molar occlusion and mandibular movements during occlusion in the American opossum Didelphis marsupialis L. Zool. J. Linn. Soc. 49:21-41 Kay, RF (1975) The functional adaptations of primate molar teeth. Am. J . Phys. Anthropol. 41:195-216. Oates, JF, Waterman, PG, and Choo. GM (1960)Food selection by the South Indian leaf-monkey, Presbytis johni, in relation t o leaf chemistry. Oecologia 4545-56. Ryan, AS (1979a)Wear striation direction on primate teeth: A scanning electron microscope examination. Am. J. Phys. Anthropol. 50:155-168. Ryan, AS (1979b) A preliminary scanning electron microscope examination of wear striation direction on primate teeth. J. Dent. Res. 58:525-530. Tsao, CH, and Richards, AG (1952) Studies on arthropod cuticle, IX. Quantitative effects of diet, age, temperature and humidity on the cuticles of five representative species of insects. Ann. Entomol. Soc. Am. 45:585-599. Walker, A, Hoeck. HN. and Perez, L (1978) Microwear of mammalian teeth as an indicator of diet. Science 20k908-9 10.