Cougars’ key to survival through the Late Pleistocene extinction: insights from dental microwear texture analysis

Cougars (Puma concolor) are one of only two large cats in North America to have survived the Late Pleistocene extinction (LPE), yet the specific key(s) to their relative success remains unknown. Here, we compare the dental microwear textures of Pleistocene cougars with sympatric felids from the La Brea Tar Pits in southern California that went extinct at the LPE (Panthera atrox and Smilodon fatalis), to clarify potential dietary factors that led to the cougar''s persistence through the LPE. We further assess whether the physical properties of food consumed have changed over time when compared with modern cougars in southern California. Using dental microwear texture analysis (DMTA), which quantifies surface features in three dimensions, we find that modern and Pleistocene cougars are not significantly different from modern African lions in any DMTA attributes, suggesting moderate durophagy (i.e. bone processing). Pleistocene cougars from La Brea have significantly greater complexity and textural fill volume than Panthera atrox (inferred to have primarily consumed flesh from fresh kills) and significantly greater variance in complexity values than S. fatalis. Ultimately, these results suggest that cougars already used or adopted a more generalized dietary strategy during the Pleistocene that may have been key to their subsequent success.     

Microwear evidence for Plio-Pleistocene bovid diets from Makapansgat Limeworks Cave, South Africa

Makapansgat Limeworks Cave is a well-known Australopithecus africanus bearing locality that has spawned a considerable amount of paleoecological research because of its hominin component. Most recently, the paleoecology of this Plio-Pleistocene site has been studied by determining the diet and habitat of other extinct taxa, particularly the bovids. The diets of seven bovids (Aepyceros sp., Gazella vanhoepeni, Makapania broomi, Parmularius braini, Redunca darti, Tragelaphus sp. aff. T. angasii, and Tragelaphus pricei) have now been classified using taxonomic uniformitarianism, ecomorphology, stable carbon isotopes, and mesowear analysis. Here, dental microwear is applied to the same bovids for additional comparison and to further elucidate the strengths and weaknesses of each method. The different dietary proxy methods noted provide a temporal continuum, with genetic signals such as ecomorphology and taxonomic uniformitarianism indicating behavioral adaptations over geologic time, while nongenetic data such as stable carbon isotopes and mesowear reflect different aspects of average diet over extended portions of an animal's life, and dental microwear provides dietary snapshots.Microwear separated an extant baseline of ten bovid species into expected dietary categories and the Makapansgat bovids clearly fell into two groups with the same degree of separation as between extant grazers and browsers. The results indicate that a multidisciplinary approach produces a more accurate and robust reconstruction of past diets. In sum, the microwear analysis is in-line with the isotope and mesowear results, which suggest a stronger browsing component than either taxonomic uniformitarianism or ecomorphology imply.     

牙齿微痕研究在古食性重建中应用的简述

在古食性研究中,牙齿微痕是指动物在咀嚼食物的过程中在牙齿咬合面上产生的微观磨损痕迹。不同食性的动物具有不同的牙齿微痕特征,因此可以通过研究牙齿微痕特征来重建灭绝动物的古食性,为探讨动物演化和古生态环境变化提供重要信息。本文主要介绍牙齿微痕作为一种简单而高效的古食性重建方法在古生物领域中的应用。本文主要内容包括牙齿微痕的发展历史,形成机理与应用,以及近年来被广泛应用的牙齿微痕定量化分析——表面纹理分析法,并在最后浅谈了牙齿微痕研究未来可能研究的方向。     

Direct Comparisons of 2D and 3D Dental Microwear Proxies in Extant Herbivorous and Carnivorous Mammals

The analysis of dental microwear is commonly used by paleontologists and anthropologists to clarify the diets of extinct species, including herbivorous and carnivorous mammals. Currently, there are numerous methods employed to quantify dental microwear, varying in the types of microscopes used, magnifications, and the characterization of wear in both two dimensions and three dimensions. Results from dental microwear studies utilizing different methods are not directly comparable and human quantification of wear features (e.g., pits and scratches) introduces interobserver error, with higher error being produced by less experienced individuals. Dental microwear texture analysis (DMTA), which analyzes microwear features in three dimensions, alleviates some of the problems surrounding two-dimensional microwear methods by reducing observer bias. Here, we assess the accuracy and comparability within and between 2D and 3D dental microwear analyses in herbivorous and carnivorous mammals at the same magnification. Specifically, we compare observer-generated 2D microwear data from photosimulations of the identical scanned areas of DMTA in extant African bovids and carnivorans using a scanning white light confocal microscope at 100x magnification. Using this magnification, dental microwear features quantified in 2D were able to separate grazing and frugivorous bovids using scratch frequency; however, DMTA variables were better able to discriminate between disparate dietary niches in both carnivorous and herbivorous mammals. Further, results demonstrate significant interobserver differences in 2D microwear data, with the microwear index remaining the least variable between experienced observers, consistent with prior research. Overall, our results highlight the importance of reducing observer error and analyzing dental microwear in three dimensions in order to consistently interpret diets accurately.     

Dental microwear texture analysis of two families of subfossil lemurs from Madagascar

This study employs dental microwear texture analysis to reconstruct the diets of two families of subfossil lemurs from Madagascar, the archaeolemurids and megaladapids. This technique is based on three-dimensional surface measurements utilizing a white-light confocal profiler and scale-sensitive fractal analysis. Data were recorded for six texture variables previously used successfully to distinguish between living primates with known dietary differences. Statistical analyses revealed that the archaeolemurids and megaladapids have overlapping microwear texture signatures, suggesting that the two families occasionally depended on resources with similar mechanical properties. Even so, moderate variation in most attributes is evident, and results suggest potential differences in the foods consumed by the two families. The microwear pattern for the megaladapids indicates a preference for tougher foods, such as many leaves, while that of the archaeolemurids is consistent with the consumption of harder foods. The results also indicate some intraspecific differences among taxa within each family. This evidence suggests that the archaeolemurids and megaladapids, like many living primates, likely consumed a variety of food types.     

Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis

Many researchers have suggested that Australopithecus anamensis and Australopithecus afarensis were among the earliest hominins to have diets that included hard, brittle items. Here we examine dental microwear textures of these hominins for evidence of this. The molars of three Au. anamensis and 19 Au. afarensis specimens examined preserve unobscured antemortem microwear. Microwear textures of these individuals closely resemble those of Paranthropus boisei, having lower complexity values than Australopithecus africanus and especially Paranthropus robustus. The microwear texture complexity values for Au. anamensis and Au. afarensis are similar to those of the grass-eating Theropithecus gelada and folivorous Alouatta palliata and Trachypithecus cristatus. This implies that these Au. anamensis and Au. afarensis individuals did not have diets dominated by hard, brittle foods shortly before their deaths. On the other hand, microwear texture anisotropy values for these taxa are lower on average than those of Theropithecus, Alouatta or Trachypithecus. This suggests that the fossil taxa did not have diets dominated by tough foods either, or if they did that directions of tooth–tooth movement were less constrained than in higher cusped and sharper crested extant primate grass eaters and folivores.     

Quantitative differences in dental microwear between primate species with different diets and a comment on the presumed diet of Sivapithecus

Studies of dental microwear have been used to relate tooth form to function in a variety of recent and extinct mammals. Probably the most important aspect of microwear analysis is the possibility of using it to deduce the diet of extinct animals. Such deductions must be based on comparative studies of modern species with known diets, but to date, only qualitative studies have been attempted and all have been based on small samples. Here we report quantitative differences in dental microwear between primate species that are known to have different diets. Occlusal facets with different functions have previously been shown to exhibit different microwear patterns. However, the differences between facets of one species are shown to be far less than those between homologous facets of different species. Study of seven species of extant primates shows that enamel microwear can be used to distinguish between those with a mainly frugivorous diet and those with a mainly folivorous one. Microwear can also distinguish hard-object feeders from soft-fruit eaters. The microwear of Miocene Sivapithecus indicus cannot be distinguished statistically from that of the chimpanzee, but it is different from that of the other species. On this evidence S. indicus was not a hard-object feeder and the adaptive significance of its thick molar enamel is at present unknown.     

Dental microwear texture and anthropoid diets

Dental microwear has long been used as evidence concerning the diets of extinct species. Here, we present a comparative baseline series of dental microwear textures for a sample of 21 anthropoid primate species displaying interspecific and intraspecific dietary variability. Four dental microwear texture variables (complexity, anisotropy, textural fill volume, and heterogeneity) were computed based on scale-sensitive fractal analysis and high-resolution three-dimensional renderings of microwear surfaces collected using a white-light confocal profiler. The purpose of this analysis was to assess the extent to which these variables reflect variation in diet. Significant contrasts between species with diets known to include foods with differing material properties are clearly evident for all four microwear texture variables. In particular, species that consume more tough foods, such as leaves, tended to have high levels of anisotropy and low texture complexity. The converse was true for species including hard and brittle items in their diets either as staples or as fallback foods. These results reaffirm the utility of dental microwear texture analysis as an important tool in making dietary inferences based on fossil primate samples.     

Dental microwear textural analyses to track feeding ecology of reindeer: a comparison of two contrasting populations in Norway

Using dental microwear textural analysis, we aim to explore variations in feeding habits within and between wild reindeer populations (Rangifer tarandus) in Norway. Specimens from the two wild reindeer areas of Knutshø and Hardangervidda were hunted between late August and the end of September 2014, and found to share very similar topological and ecological characteristics (continental alpine tundra). Despite the homogenisation of plant resources at the end of the snow-free period, dental microwear textural analysis on cheek teeth indicates differences in feeding behaviors between the two populations, in that reindeer from Knutshø might display a more “grazing” signal than the ones from Hardangervidda. Such differences in dental microwear textures reflect the differences in feeding habits that could be linked with differences in population density of reindeer. The Knutshø reindeer density is lower than at Hardangervidda, where primary food resources like grasses, sedges, and lichens are less abundant. Analyses also show the differences in gender for the population of Knutshø, but more studies are necessary for the clearest interpretation of data. Our results emphasize the need to explore local variations at a monthly time frame in order to better assess the versatility of dental microwear textures before applying this kind of analysis to either extant or extinct multi-population scales.     

Dental microwear texture analysis: technical considerations

Dental microwear analysis is commonly used to infer aspects of diet in extinct primates. Conventional methods of microwear analysis have usually been limited to two-dimensional imaging studies using a scanning electron microscope and the identification of apparent individual features. These methods have proved time-consuming and prone to subjectivity and observer error. Here we describe a new methodological approach to microwear: dental microwear texture analysis, based on three-dimensional surface measurements taken using white-light confocal microscopy and scale-sensitive fractal analysis. Surface parameters for complexity, scale of maximum complexity, anisotropy, heterogeneity, and textural fill volume offer repeatable, quantitative characterizations of three-dimensional surfaces, free of observer measurement error. Some results are presented to illustrate how these parameters distinguish extant primates with different diets. In this case, microwear surfaces of Cebus apella and Lophocebus albigena, which consume some harder food items, have higher average values for complexity than do folivores or soft fruit eaters.     

Dental microwear and diets of African early Homo

Conventional wisdom ties the origin and early evolution of the genus Homo to environmental changes that occurred near the end of the Pliocene. The basic idea is that changing habitats led to new diets emphasizing savanna resources, such as herd mammals or underground storage organs. Fossil teeth provide the most direct evidence available for evaluating this theory. In this paper, we present a comprehensive study of dental microwear in Plio-Pleistocene Homo from Africa. We examined all available cheek teeth from Ethiopia, Kenya, Tanzania, Malawi, and South Africa and found 18 that preserved antemortem microwear. Microwear features were measured and compared for these specimens and a baseline series of five extant primate species (Cebus apella, Gorilla gorilla, Lophocebus albigena, Pan troglodytes, and Papio ursinus) and two protohistoric human foraging groups (Aleut and Arikara) with documented differences in diet and subsistence strategies. Results confirmed that dental microwear reflects diet, such that hard-object specialists tend to have more large microwear pits, whereas tough food eaters usually have more striations and smaller microwear features. Early Homo specimens clustered with baseline groups that do not prefer fracture resistant foods. Still, Homo erectus and individuals from Swartkrans Member 1 had more small pits than Homo habilis and specimens from Sterkfontein Member 5C. These results suggest that none of the early Homo groups specialized on very hard or tough foods, but that H. erectus and Swartkrans Member 1 individuals ate, at least occasionally, more brittle or tough items than other fossil hominins studied.     

Incisor microwear,diet, and tooth use in three Amerindian populations

Incisor microwear patterns have been shown to reflect aspects of diet and ingestive behaviors in a wide range of nonhuman primates. While some studies have suggested that anterior dental microwear might be used to infer unusual front tooth use practices in archaeological populations, quantitative work on modern human incisors has thus far been limited. In this study we examined dental microwear on the maxillary central incisors of three groups of humans: Aleutian Islanders (n = 16), Arikara from the Mobridge Site in South Dakota (n = 15), and a Late Woodland Bluff sample from Jersey County, Illinois (n = 17). High-resolution replicas were prepared and examined by scanning electron microscopy following conventional procedures. Photomicrographs were taken at consistent locations on the labial surface, and microwear was quantified using Microware 3.0 (Ungar, 1997). Statistical test results revealed significant differences among the groups in microwear feature densities, sizes, and shapes. The Aleut, Arikara, and Illinois Bluff samples showed a gradient of increasing microwear density, increasing linearity in feature shape, and decreasing feature size. These differences evidently correspond to amount of meat consumption, and apparently to degree of use of the incisors in heavy loading. No differences were observed between groups in heterogeneity of feature orientations, and no sex-related differences were found. Associations between incisor microwear on the one hand and subsistence practice and anterior tooth use on the other likely have important implications for the study of hominid paleobiology. Am J Phys Anthropol 109:387–396, 1999. © 1999 Wiley-Liss, Inc.     

Can Dental Microwear Textures Record Inter-Individual Dietary Variations?

Background

Dental microwear analyses are commonly used to deduce the diet of extinct mammals. Conventional methods rely on the user identifying features within a 2D image. However, recent interdisciplinary research has lead to the development of an advanced methodology that is free of observer error, based on the automated quantification of 3D surfaces by combining confocal microscopy with scale-sensitive fractal analysis. This method has already proved to be very efficient in detecting dietary differences between species. Focusing on a finer, intra-specific scale of analysis, the aim of this study is to test this method''s ability to track such differences between individuals from a single population.

Methodology/Principal Findings

For the purposes of this study, the 3D molar microwear of 78 individuals from a well-known population of extant roe deer (Capreolus caprelous) is quantified. Multivariate statistical analyses indicate significant seasonal and sexual differences in individual dental microwear design. These are probably the consequence of seasonal variations in fruit, seed and leaf availability, as well as differences in feeding preference between males and females due to distinct energy requirements during periods of rutting, gestation or giving birth. Nevertheless, further investigations using two-block Partial Least-Squares analysis show no strong relationship between individual stomach contents and microwear texture. This is an expected result, assuming that stomach contents are composed of food items ingested during the last few hours whereas dental microwear texture records the physical properties of items eaten over periods of days or weeks.

Conclusions/Significance

Microwear 3D scale-sensitive fractal analysis does detect differences in diet ranging from the inter-feeding styles scale to the intra-population between-season and between-sex scales. It is therefore a possible tool, to be used with caution, in the further exploration of the feeding biology and ecology of extinct mammals.     

Technical note: Dental microwear textures of "Phase I" and "Phase II" facets

The power stroke of mastication has been traditionally divided into two parts, one which precedes centric occlusion, and the other which follows it-"Phase I" and "Phase II," respectively. Recent studies of primate mastication have called into question the role of Phase II in food processing, as they have found little muscle activity or accompanying bone strain following centric occlusion. That said, many researchers today look to Phase II facets to relate diet to patterns of dental microwear. This suggests the need to reevaluate microwear patterns on Phase I facets. Here we use texture analysis to compare and contrast microwear on facets representing both phases in three primate species with differing diets (Alouatta palliata, Cebus apella, and Lophocebus albigena). Results reaffirm that microwear patterns on Phase II facets better distinguish taxa with differing diets than do those on Phase I facets. Further, differences in microwear textures between facet types for a given taxon may themselves reflect diet. Some possible explanations for differences in microwear textures between facet types are proposed.     

Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995-2007

Dental microwear analysis has proven to be a valuable tool for the reconstruction of aspects of diet in early hominins. That said, sample sizes for some groups are small, decreasing our confidence that results are representative of a given taxon and making it difficult to assess within-species variation. Here we present microwear texture data for several new specimens of Homo habilis and Paranthropus boisei from Olduvai Gorge, bringing sample sizes for these species in line with those published for most other early hominins. These data are added to those published to date, and microwear textures of the enlarged sample of H. habilis (n = 10) and P. boisei (n = 9) are compared with one another and with those of other early hominins. New results confirm that P. boisei does not have microwear patterns expected of a hard-object specialist. Further, the separate texture complexity analyses of early Homo species suggest that Homo erectus ate a broader range of foods, at least in terms of hardness, than did H. habilis, P. boisei, or the “gracile” australopiths studied. Finally, differences in scale of maximum complexity and perhaps textural fill volume between H. habilis and H. erectus are noted, suggesting further possible differences between these species in diet.     

Buccal dental microwear variability in extant African Hominoidea: taxonomy versus ecology

Buccal microwear patterns on teeth are good indicators of the abrasiveness of foodstuffs and have been used to trace the dietary habits of fossil species, including primates and hominids. However, few studies have addressed the variability of this microwear. The abrasiveness of dietary components depends not only on the hardness of the particles ingested, but also on the presence of dust and other exogenous elements introduced during food processing. These elements are responsible for the microwear typology observed on the enamel surfaces of primate teeth. Here we analyzed the variability of buccal microwear patterns in African Great Apes (Gorilla gorilla and Pan troglodytes), using tooth molds obtained from the original specimens held in several osteological collections. Our results suggest that ecological adaptations at subspecies or population level account for differences in microwear patterns, which are attributed to habitat and ecological conditions within populations rather than differences between species. The findings from studies on the variability of buccal dental microwear in extant species will contribute to a better understanding of extinct hominids’ diet and ecology.     

Preliminary examination of non-occlusal dental microwear in anthropoids: Implications for the study of fossil primates

Most studies of microscopic wear on non-human primate teeth have focused on the occlusal surfaces of molars. Recent analyses of the buccal surfaces of human cheek teeth have demonstrated an association between diet and dental microwear on the these surfaces as well. In the current study, we examine microwear on both the buccal and lingual surfaces of non-human primate molars to assess the potential of these surfaces to reveal information concerning anthropoid feeding behaviors. We compare frequency of microwear occurrence in 12 extant and 11 fossil anthropoid species. Among the living primates, the occurrence of microwear on non-occlusal surfaces appears to relate to both diet and degree of terrestriality. The implications of this research for the inference of feeding behaviors and substrate use in fossil cercopithecoids are discussed. © 1996 Wiley-Liss, Inc.     

In vivo and in vitro turnover in dental microwear

Given the potential usefulness of dental microwear analyses in interpretations of archaeological and paleontological material, it is surprising how little we know about changes in individual microwear features through time. The purpose of this study was to document the turnover in primate dental microwear through in vivo dental studies of monkeys raised on different diets, and through in vitro studies of the abrasive effects of monkey chow biscuits on isolated monkey teeth. As in previous studies, epoxy replicas were prepared from dental impressions and examined under a scanning electron microscope. Results indicate that, under certain conditions, the turnover in primate dental microwear can be on the order of days, hours, or even minutes. Individual microscopic wear features can be obliterated within 24 hours on the molars of laboratory monkeys, and monkey chow biscuits can easily scratch the enamel of isolated monkey teeth. Monkeys raised on a hard diet showed more rapid turnover in dental microwear than monkeys raised on a soft diet. However, paired-sample tests revealed that, for all animals, the molar shearing facets were being abraded at a significantly slower rate than molar crushing/grinding facets. In light of these results, investigators should make every effort to use large samples in interspecific comparisons of dental microwear involving species with variable diets. Another implication of these results is that changes in dental microwear might be useful indicators of changes in oral behavior over relatively short periods of time.     

植食性哺乳动物牙齿磨痕分析方法简介及其在古食性恢复中的应用前景

通过研究古哺乳动物的食性来探讨哺乳动物演化与古生态环境变化之间的关系是目前古生物学研究领域的一个热点,而牙齿磨痕分析是恢复古食性和重建古生态环境的重要手段。牙齿磨痕(dental wear)分析包括微痕(microwear)分析和中痕(mesowear)分析,两种方法均强调食性与牙齿磨痕模式的严格对应,即不同食性的动物具有不同的牙齿磨痕特征模式。近年来,牙齿磨痕分析方法以其简单、快捷和高效等优点已被广泛应用于奇蹄类、偶蹄类、啮齿类、长鼻类和食肉类等哺乳动物的食性研究。但哺乳动物的食性和摄食习性比较复杂,很可能会影响微痕和中痕分析对食性的分辨率。所以,为了获得更加详细的古食性信息和更高的食性分辨率,一方面要对微痕和中痕分析方法进行改进,增添稳定并具有食性识别意义的观测变量,另一方面,需要同时结合微痕和中痕分析,从而获得更加全面的食性信息。虽然牙齿磨痕分析目前主要应用于植食性哺乳动物的食性研究,但其原理对哺乳动物的其它类群也是适用的,随着磨痕分析方法的不断改进和其它类群磨痕数据库的建立,未来的牙齿磨痕分析将可以恢复更多类群的古食性,从而可以更加全面和准确地揭示古食性与古环境信息。     

MicroWeaR: A new R package for dental microwear analysis

Mastication of dietary items with different mechanical properties leaves distinctive microscopic marks on the surface of tooth enamel. The inspection of such marks (dental microwear analysis) is informative about the dietary habitus in fossil as well as in modern species. Dental microwear analysis relies on the morphology, abundance, direction, and distribution of these microscopic marks. We present a new freely available software implementation, MicroWeaR, that, compared to traditional dental microwear tools, allows more rapid, observer error free, and inexpensive quantification and classification of all the microscopic marks (also including for the first time different subtypes of scars). Classification parameters and graphical rendering of the output are fully settable by the user. MicroWeaR includes functions to (a) sample the marks, (b) classify features into categories as pits or scratches and then into their respective subcategories (large pits, coarse scratches, etc.), (c) generate an output table with summary information, and (d) obtain a visual surface‐map where marks are highlighted. We provide a tutorial to reproduce the steps required to perform microwear analysis and to test tool functionalities. Then, we present two case studies to illustrate how MicroWeaR works. The first regards a Miocene great ape obtained from through environmental scanning electron microscope, and other a Pleistocene cervid acquired by a stereomicroscope.