Diet reconstruction in cave bears from craniodental morphology: past evidences,new results and future directions

ABSTRACT

The diet of the cave bear (Ursus spelaeus) is a controversial topic, as different paleobiological approaches (e.g. dental wear, isotopic biochemistry, skull morphometrics) result in different dietary inferences for the cave bear, ranging from carnivory to pure herbivory. Here, we review the main results obtained from these approaches, with special emphasis on those obtained from the morphometric analyses of the cave bear craniodental skeleton. Then, we compute a between-group Principal Components Analysis from a set of 3D-landmarks digitized on 103 mandibles of living bears and extinct cave bears and using a phylomorphospace approach. Moreover, we also reconstructed the evolutionary trajectory of the cave bear mandible from the hypothetical shape of its inferred ancestor. Our results indicate that the mandible of the cave bear possess specific traits indicative of a highly-herbivorous diet or, at least, more herbivorous than their closest living relative, the brown bear (Ursus arctos). Moreover, we also propose new directions for future research to obtain more detailed inferences on the potential food resources consumed by the cave bear being crucial to understand the ‘life and death’ of this vanished animal.     

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.     

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。     

Seasonal Mortality Patterns in Primates: Implications for the Interpretation of Dental Microwear

The microscopic traces of use wear on teeth have been extensively studied to provide information that will assist in elucidating the dietary habits of extinct hominin species. 1 - 13 It has been amply documented that dental microwear provides information pertaining to diet for living animals, where there is a strong and consistent association between dental microwear patterns and different types of foods that are chewed. The details of occlusal surface wear patterns are capable of distinguishing among diets when the constituent food items differ in their fracture properties. 14 - 20 For example, the microwear traces left on the teeth of mammals that crush hard, brittle foods such as nuts are generally dominated by pits, whereas traces left on the teeth of mammals that shear tough items such as leaves tend to be characterized by scratches. These microwear features result from and thus record actual chewing events. As such, microwear patterns are expected to be variably ephemeral, as individual features are worn away and replaced or overprinted by others as the tooth wears down in subsequent bouts of mastication. Indeed, it has been demonstrated, both in the laboratory and the wild, that short‐term dietary variation can result in the turnover of microwear. 17 , 21 - 23 Because occlusal microwear potentially reflects an individual's diet for a short time (days, weeks, or months, depending on the nature of the foods being masticated), tooth surfaces sampled at different times will display differences that relate to temporal (for example, seasonal) differences in diet. 24     

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.     

The Bronze Age burials from Cova Dels Blaus (Vall d′Uixó, Castelló, Spain): An approach to palaeodietary reconstruction through dental pathology, occlusal wear and buccal microwear patterns

This paper reports a palaeodietary investigation of the human remains found in the collective Bronze Age burial cave from Vall d′Uixó (Castelló, Spain). Dental pathology, tooth wear as well as buccal dental microwear were analysed. Percentages of dental pathologies were compared with Chalcolithic and Bronze Age sites from the same territory. Dental caries, ante-mortem tooth loss, periodontal disease and abscess frequencies indicate a diet rich in carbohydrate foods. However, dental calculus percentages and macroscopic wear patterns suggest a diet not exclusively relying on agricultural resources. In addition, buccal dental microwear density and length by orientation recorded on micrographs using a scanning electron microscope showed inter-group differences with regard to carnivorous hunter-gatherers and farming populations related to the amount of abrasives in the diet that could correspond to a different dependence on agricultural resources or food preparation technology.     

A three-dimensional analysis of tooth-root morphology in living bears and implications for feeding behaviour in the extinct cave bear

ABSTRACT

The morphology of both crowns and tooth-roots reflects dietary specialisation in mammalian carnivores. In this article, we analyse the tooth-root morphology of maxillary teeth from CT scans of living bears (Ursus arctos, Ursus americanus, Ursus maritimus, Ursus thibetanus, Melursus ursinus, Helarctos malayanus, Tremarctos ornatus and Ailuropoda melanoleuca) in order to make inferences about the diet and feeding behaviour of the extinct cave bear (Ursus spelaeus sensu lato). Specifically, we investigate two major mitochondrial clades of extinct cave bears recognized by previous authors: Ursus ingressus and Ursus spelaeus (U. spelaeus spelaeus, U. spelaeus ladinicus, U. spelaeus eremus). Our results indicate a close association between tooth-root surface area and feeding behaviour in all living bear species. Tooth-root surface area values of cave bears suggest that they relied more on vegetative matter than living brown bears (Ursus arctos) but subtle differences between these species/subspecies could also indicate different feeding strategies among the members of cave bear complex.     

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.     

Technical note: Artificial Resynthesis Technology for the experimental formation of dental microwear textures

Dental microwear formation on the posterior dentition is largely attributed to an organism's diet. However, some have suggested that dietary and environmental abrasives contribute more to the formation process than food, calling into question the applicability of dental microwear to the reconstruction of diet in the fossil record. Creating microwear under controlled conditions would benefit this debate, but requires accurately replicating the oral environment. This study tests the applicability of Artificial Resynthesis Technology (ART 5) to create microwear textures while mitigating the challenges of past research. ART 5 is a simulator that replicates the chewing cycle, responds to changes in food texture, and simulates the actions of the oral cavity. Surgically extracted, occluding pairs of third molars (n = 2 pairs) were used in two chewing experiments: one with dried beef and another with sand added to the dried beef. High-resolution molds were taken at 0, 50, 100, 2500, and 5000 simulated chewing cycles, which equates to approximately 1 week of chewing. Preliminary results show that ART 5 produces microwear textures. Meat alone may produce enamel prism rod exposure at 5000 cycles, although attrition cannot be ruled out. Meat with sand accelerates the wear formation process, with enamel prism rods quickly obliterated and “pit-and-scratch” microwear forming at approximately 2500 cycles. Future work with ART 5 will incorporate a more thorough experimental protocol with improved controls, pH of the simulated oral environment, and grit measurements; however, these results indicate the potential of ART 5 in untangling the complex variables of dental microwear formation.     

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。     

Dental microwear evidence for a dietary shift between two nonmaize-reliant prehistoric human populations from Indiana

Several recent studies have demonstrated the efficacy of dental microwear analysis (DMA) for dietary reconstruction among nonhuman primates, early hominids, and prehistoric humans. The current study seeks microwear evidence for a paleobotanically suggested change in the types of foods that were consumed by two temporally distinct populations of the North American eastern woodlands. This particular dietary shift between the Late Archaic and the Early/Middle Woodland periods did not include the introduction of maize or any other tropical cultigen. In contrast, most dietary reconstructions from this area have compared later populations that consumed tropical cultigens (such as maize) with those that did not. High-resolution casts of adult mandibular second molar protoconid phase II wear facets were viewed via a scanning electron microscope at 500x. Photomicrographs of the microwear features were analyzed with specialized software, Microware 2.2 (Ungar [1995] Scanning 17:57-59). Analysis of variance statistical tests were performed, with one variable requiring rank-transformation. A dietary transition is evidenced by a statistically significant increase in the mean number of pits and concomitant decreases in scratch width and scratch length from the Late Archaic to the Early/Middle Woodland. Overall, the diet became harder and less abrasive. The implication here is that dental microwear analysis is able to discern relatively subtle dietary transitions in human populations that may not be as readily accessible by other means of dietary reconstruction.     

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.     

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.     

The cave bear’s hibernation: reconstructing the physiology and behaviour of an extinct animal

Abstract

When studying an extinct species such as the cave bear (Ursus spelaeus ROSENMÜLLER 1794), it is possible to apply a variety of molecular biology techniques such as the study of stable isotopes or mitochondrial DNA (mDNA) to infer patterns of behaviour or physiology that would otherwise remain concealed. Throughout Europe and along time, differences in the isotopic values (δ¹³C and δ¹⁵N) of cave bears arise from environmental differences and the Pleistocene climatic evolution. The climate determines the hibernation length, during which the cave bears undergo a particular physiology that can be related to an increase in δ¹⁵N during climate cooling. In order to verify whether hibernation affected the isotopic values, we compared cave bears in different ontogenetic stages. The results show that perinatal values reflect the values for mothers during hibernation, while juveniles show differences in maternal investment. A previous study in the literature based on complete mitochondrial DNA sequences of several individuals collected from closely situated caves showed that each cave housed, almost exclusively, a single lineage of haplotypes. This pattern suggests extreme fidelity to the birth site, or homing behaviour, and that cave bears formed stable maternal social groups, at least for the purpose of hibernation. Studies of this type offer unexpected data on the palaeobiology of this extinct animal.     

Dental microwear in the orthodentine of the Xenarthra (Mammalia) and its use in reconstructing the palaeodiet of extinct taxa: the case study of Nothrotheriops shastensis (Xenarthra,Tardigrada, Nothrotheriidae)

The utility of orthodentine microwear analysis as a proxy for dietary reconstruction in xenarthrans (tree sloths, armadillos) was quantitatively and statistically accessed via low‐magnification stereomicroscopy. Features such as number of scratches and pits, as well as presence of gouges, hypercoarse scratches, > four large pits, > four cross scratches, and fine, mixed or coarse scratch texture were recorded in 255 teeth from 20 extant xenarthran species. Feature patterns are consistent with scar formation through abrasional (tooth–food) and attritional (tooth–tooth) contact. Number of scratches is the most dietary diagnostic microwear variable for xenarthrans, with herbivorous sloths characterized by > ten scratches and nonherbivorous armadillos by < ten scratches. Discriminant function analysis differentiated arboreal folivores (sloths) and frugivore‐folivores (sloths) both from each other and from fossorial carnivore‐omnivores (armadillos) and insectivores (armadillos). Microwear patterns in carnivore‐omnivores and insectivores are difficult to distinguish between; armadillo microwear may reflect a fossorial lifestyle (grit consumption) rather than primary diet. Cabassous centralis is anomalous in its microwear signal relative to all other insectivores. To test the utility of orthodentine microwear analysis as an indicator of palaeodiet in extinct xenarthrans, microwear in the ground sloth Nothrotheriops shastensis was quantitatively and statistically compared to microwear in extant taxa. Microwear patterns in N. shastensis are most comparable to extant folivores based on scratch number and hierarchical cluster analysis. This strongly supports an herbivorous diet for N. shastensis that is corroborated by multiple independent lines of evidence. Thus, orthodentine microwear analysis can be used to reconstruct diet in extinct xenarthrans. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 201–222.     

Phylogenetic signal in tooth wear dietary niche proxies

In the absence of independent observational data, ecologists and paleoecologists use proxies for the Eltonian niches of species (i.e., the resource or dietary axes of the niche). Some dietary proxies exploit the fact that mammalian teeth experience wear during mastication, due to both tooth‐on‐tooth and food‐on‐tooth interactions. The distribution and types of wear detectible at micro‐ and macroscales are highly correlated with the resource preferences of individuals and, in turn, species. Because methods that quantify the distribution of tooth wear (i.e., analytical tooth wear methods) do so by direct observation of facets and marks on the teeth of individual animals, dietary inferences derived from them are thought to be independent of the clade to which individuals belong. However, an assumption of clade or phylogenetic independence when making species‐level dietary inferences may be misleading if phylogenetic niche conservatism is widespread among mammals. Herein, we test for phylogenetic signal in data from numerous analytical tooth wear studies, incorporating macrowear (i.e., mesowear) and microwear (i.e., low‐magnification microwear and dental microwear texture analysis). Using two measures of phylogenetic signal, heritability (H²) and Pagel's λ, we find that analytical tooth wear data are not independent of phylogeny and failing to account for such nonindependence leads to overestimation of discriminability among species with different dietary preferences. We suggest that morphological traits inherited from ancestral clades (e.g., tooth shape) influence the ways in which the teeth wear during mastication and constrain the foods individuals of a species can effectively exploit. We do not suggest that tooth wear is simply phylogeny in disguise; the tooth wear of individuals and species likely varies within some range that is set by morphological constraints. We therefore recommend the use of phylogenetic comparative methods in studies of mammalian tooth wear, whenever possible.     

Dental microwear variability on buccal tooth enamel surfaces of extant Catarrhini and the Miocene fossil Dryopithecus laietanus (Hominoidea)

Analyses of buccal tooth microwear have been used to trace dietary habits of modern hunter-gatherer populations. In these populations, the average density and length of striations on the buccal surfaces of teeth are significantly cor-related with the abrasive potential of food items consumed. In non-human pri-mates, tooth microwear patterns on both occlusal and buccal wear facets have been thoroughly studied and the results applied to the characterization of dietary habits of fossil species. In this paper, we present inter- and intra-specific buccal microwear variability analyses in extant Cercopithecoidea (Cercopithecus mitis, C. neglectus, Chlorocebus aethiops, Colobus spp., Papio anubis) and Hominoidea (Gorilla gorilla, Pan troglodytes, Pongo pygmaeus). The results are tentatively compared to buccal microwear patterns of the Miocene fossils Dryopithecus and Oreopithecus. Significant differences in striation density and length are found among the fossil taxa studied and the extant primates, suggesting that buccal microwear can be used to identify dietary differences among taxa. The Dryopithecus buccal microwear pattern most closely resembles that of abrasive, tough plant foods consumers, such as the gorilla, in contrast to stud-ies of dental morphology that suggest a softer, frugivorous diet. Results for Oreopithecus were equivocal, but suggest a more abrasive diet than that previously thought.     

The link between dental microwear and feeding ecology in tree sloths and armadillos (Mammalia: Xenarthra)

The Xenarthra represents an enigmatic clade of placental mammals that includes living tree sloths, armadillos, and their extinct relatives, yet certain aspects of the biology of this group remains poorly understood. Here, we use scanning electron microscopy to test the hypothesis that orthodentine microwear patterns in extant xenarthrans are significantly different among different dietary groups. In a blind analysis, microwear patterns were quantified at a magnification of 500× by two independent observers for extant species from four dietary groups (carnivore–omnivores, folivores, frugivore–folivores, and insectivores). Independent observers recovered the same relative between‐group differences in microwear patterns. Insectivores and folivores have a significantly lower numbers of scratches and greater scar widths than frugivore–folivores and carnivore–omnivores, yet we were neither able to statistically distinguish insectivores from folivores, nor differentiate frugivore–folivores from carnivore–omnivores. Nevertheless, a clear distinction exists between taxa from the same trophic level and habitat, which suggests that orthodentine microwear reflects niche partitioning and habitat more than diet among related forms. We suggest that bite force and chewing mechanics have a strong influence on the formation of orthodentine microwear, which may explain some of the observed overlap between distinct groups (e.g. frugivore–folivores versus carnivore–omnivores). This study serves as a positive step forwards in our understanding of the ecological role of living xenarthrans, and serves as a foundation for using orthodentine microwear to reconstruct palaeoecology in extinct ground sloths, glyptodonts, and pampatheres. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Dental microwear and stable isotopes inform the paleoecology of extinct hominins

Determining the diet of an extinct species is paramount in any attempt to reconstruct its paleoecology. Because the distribution and mechanical properties of food items may impact postcranial, cranial, mandibular, and dental morphologies related to their procurement, ingestion, and mastication, these anatomical attributes have been studied intensively. However, while mechanical environments influence skeletal and dental features, it is not clear to what extent they dictate particular morphologies. Although biomechanical explanations have been widely applied to extinct hominins in attempts to retrodict dietary proclivities, morphology may say as much about what they were capable of eating, and perhaps more about phylogenetic history, than about the nature of the diet. Anatomical attributes may establish boundary limits, but direct evidence left by the foods that were actually (rather than hypothetically) consumed is required to reconstruct diet. Dental microwear and the stable light isotope chemistry of tooth enamel provide such evidence, and are especially powerful when used in tandem. We review the foundations for microwear and biogeochemistry in diet reconstruction, and discuss this evidence for six early hominin species (Ardipithecus ramidus, Australopithecus anamensis, Au. afarensis, Au. africanus, Paranthropus robustus, and P. boisei). The dietary signals derived from microwear and isotope chemistry are sometimes at odds with inferences from biomechanical approaches, a potentially disquieting conundrum that is particularly evident for several species.