Molar Wear Research Articles

Age-related tooth wear in African rainforest hunter-gatherers.

Central African small-scale foragers subsist primarily on hunting game activities and wild plant-food gathering. Starch-rich tubers are underground storage organs (USOs) and staple food resources in savanna and tropical rainforests. However, little is known about the effect of USO consumption on tooth wear development in living hunter-gatherers. We report age- and sex-dependent tooth wear rates in forest-dwelling Baka Pygmies with well-documented wild-yam-tuber-based diet to explore the long-term impact of USO mechanical hardness and abrasiveness on the wearing down of the teeth. Percentages of dentine exposure (PDEs) of permanent left mandibular first molars (M1 ) were recorded using in vivo high-resolution replicas of Baka individuals (aged 8-33 years), inhabiting Le Bosquet district in Cameroon (Western Africa). Regression and covariance analyses were used to test the effect of individual aging by sex on PDE rates. We found a strong increase of PDE by age among Baka individuals. No evidence of sexual dimorphism in wear patterns suggests similar sex-related dietary and masticatory demands during growth. Overall, greatest dentine exposure values ≈4% denote unexpected slow wear down rates for foraging diets relying on USO consumption. The low molar wear rates with age found in Baka Pygmies contrast with extensive wear rates in savanna-dwelling foragers, reflecting differences in thermal processing techniques affecting fracture toughness and grittiness of mechanically challenging foods. Our findings reveal that culture-specific dietary proclivities influence tooth wear among foraging behaviors with important implications in hominin dietary versatility and abrasive stress on chewing surfaces.

Clinical presentation of two phenotypes of tooth wear patients

ObjectiveTo assess the clinical presentation of wear lesions in two phenotypes of tooth wear (TW) patients based on distribution and morphological features of wear. Materials and methods103 patients (mean age = 43.1 years) were divided into two groups based on cluster analysis; cluster A (61 patients) and cluster B (42 patients). The distribution of wear lesions, scores of presence or absence of 10 defined morphological TW criteria and number of teeth fulfilling each criteria were compared between groups. Intra- and inter-examiner reliability of the 10 TW criteria was determined by Cohen’s kappa and intraclass correlation coefficient. ResultsWhile cluster A had more wear in maxillary anterior teeth and mandibular molars compared with the same opposing tooth groups (p < 0.001, p < 0.007 respectively), there were no differences for cluster B. Cluster A was characterized by higher prevalence of 4 chemical morphological criteria and the highest number of teeth affected by one chemical criteria, whereas cluster B had a higher prevalence of one mechanical criteria and higher number of teeth affected by an additional mechanical criteria. Both intra- and inter-examiner values for the defined TW criteria were fair to excellent. ConclusionThe results may indicate a more chemical background for TW in cluster A and mechanical background in cluster B. Furthermore, clinicians may use certain clinical features of TW to distinguish between individuals who belong to a specific TW cluster with a presumed chemical or mechanical etiology. These preliminary findings need to be confirmed in future studies.

Root growth compensates for molar wear in adult goats (Capra aegagrus hircus).

One reason for the mammalian clade's success is the evolutionary diversity of their teeth. In herbivores, this is represented by high-crowned teeth evolved to compensate for wear caused by dietary abrasives like phytoliths and grit. Exactly how dietary abrasives wear teeth is still not understood completely. We fed four different pelleted diets of increasing abrasiveness (L: Lucerne; G: grass; GR: grass and rice husks; GRS: grass, rice husks, and sand) to four groups of a total of 28 adult goats, all with completely erupted third molars, over a six-month period. Tooth morphology was captured by medical computed tomography scans at the beginning and end of the controlled feeding experiment, and separation lines between the crown and root segments were defined in the upper right second molar (M2), to gauge absolute wear. Using bootstrapping, significant differences in volume loss between diets L/G and GR/GRS were detected. A small but nevertheless consistent volume gain was noted in the roots, and there was a significant, positive correlation between crown volume loss and root volume gain. This growth could possibly be attributed to the well-known process of cementum deposition and its relation with a putative feedback mechanism, in place to attenuate wear caused by abrasive diets.

The pay-off of hypsodonty - timing and dynamics of crown growth and wear in molars of Soay sheep

BackgroundSeveral lineages of herbivorous mammals have evolved hypsodont cheek teeth to increase the functional lifespan of their dentition. While the selective drivers of this trend and the developmental processes involved have been studied in greater detail, thus far no quantitative information is available on the relationship between additional investment into tooth growth and the resulting extension of the functional period of these teeth. To achieve this, we performed a detailed analysis of molar crown growth in known-age Soay sheep repeatedly injected with different fluorochromes.ResultsOur study revealed that in sheep molars especially the formation of the crown base portion is prolonged in comparison with other herbivorous artiodactyl species. Our results demonstrate that growth of the crown base accounted for more than half of the total crown formation time (CFT) of the anterior lobes of the first (approx. 220 days of total CFT of 300 days), second (approx. 260 of 460 days) and third (approx. 300 of at least 520 days) molars, and that the formation of this crown portion occurred largely after the teeth had already reached functional occlusion. By combining data on wear-related changes in crown morphology from the literature with the reconstructed additional investment into the crown base portion, it was possible to relate this additional investment to a prolongation of the functional periods of the molars ranging from 4 years in the M1 to 6 years in the M3.ConclusionsOur results allow to establish a quantitative link between an additional investment into molar crown growth of sheep and the extension of the functional period of these teeth. The reported findings enable an assessment of the adaptive value, in terms of increased longevity, of an additional investment into crown elongation in a mammalian herbivore.

Functional relationship between dental macrowear and diet in Late Pleistocene and recent modern human populations

AbstractMany aspects of diet and behaviour can be gleaned from dental wear, including environmental conditions, food‐fracture properties, food processing techniques, and cultural habits. Specifically, the angulation (flat vs. steep) of molar wear has been used as an indicator of food toughness and has also been implicated in the use of grinding stones and pottery in food processing. In this work, we focus on the sequential phases of the power stroke of mastication in a functional way, measuring the inclination of molar wear facets through the occlusal fingerprint analysis method. Specifically, we have calculated the angulation of wear facets in upper and lower molars of Palaeolithic humans, extant hunter‐gatherers, and proto‐farmers to discern differences between groups with different diets.Contrary to previous analyses, our study shows that the molars of Late Pleistocene specimens are characterized by significantly steeper angles than those of modern hunter‐gatherers.The flat molar wear found in the latter group could be related to the excessive mixture of exogenous materials accidentally introduced into their foods, as indicated by ethnographic evidence. On the contrary, the steep wear angles characterizing the Palaeolithic group are probably associated with the consumption of a less abrasive diet, which could be ultimately due to food preparation techniques that incorporated less dust and grit into their diets.

Maxillary first molar wear: a longitudinal study of children.

The aim of this study is to examine the correlation between tooth wear and age by quantitatively measuring maxillary first molar wear in children. A total of 150 maxillary dental models were analyzed in 30 subjects (male, 11; female, 19) with an age range of 6–14 years. Maxillary first molar wear were assessed based on area, volume and the shortest distance from the buccal occlusal plane to the central pit point (BCPH). The area and volume of the tooth cusps were measured at four different offset-plane heights (0.2, 0.4, 0.6, and 0.8 mm). Relationship between age and the amount of wear or BCPH were statistically analyzed. Correlation and regression analyses were also performed, and age estimation was obtained with linear regression analysis. Repeated measures analysis of variance (ANOVA) revealed significant differences between age and the amount of wear based on area, volume, and offset-plane height. Except age of 8 and 10, 12 and 14's 0.2-mm offset-plane-measured volume, all area and volume measurement of all ages and offset-plane height showed a significant amount of increase. Wear speeds were calculated using the BCPH. Among age and measurement variables, the correlation coefficient was strongest when the volume was measured from the 0.4-mm offset-plane. As age increases, the amount of wear, as quantified by area and volume measurements, also increases. According to this study, a regression equation that can be used for age estimation is follows: Age (y)=0.16×0.4V+0.85 (R2=0.490) using volume.

Estimating the age of western grey kangaroos (Macropus fuliginosus ocydromus)

Scientific studies and population management may benefit from knowledge of the age structure of a target population. We evaluated traditional and newly developed methods of estimating the age of kangaroos with data from 336 western grey kangaroos (Macropus fuliginosus) culled from a wild population in south-western Australia. We compared their ages based on molar progression with data on head, leg, and foot length, a balanced sum of all three measures, dried eye-lens weight, and molar wear score, and derived formulae to estimate age from each variable. Molar wear score has a linear relationship to molar progression and therefore leads to similar estimations of age, but requires only one complete arcade of molars. Because the relationships between age and the lengths of head, foot and leg are curvilinear, these become less reliable indicators of age with increasing age but the accuracy can be improved by considering a combination of the lengths of head, foot, and leg. Estimation of age from dried lens weight is more accurate than estimation from morphometry. The use of morphometry to estimate the age of kangaroos older than two years is more reliable than previously thought and requisite data can be collected from live animals. Where lethal methods are needed to collect samples, a largely intact skull, a single arcade of molars, or the lens extracted from one eye can reliably be used to estimate age.

Reconstructing molar growth from enamel histology in extant and extinct Equus

The way teeth grow is recorded in dental enamel as incremental marks. Detailed analysis of tooth growth is known to provide valuable insights into the growth and the pace of life of vertebrates. Here, we study the growth pattern of the first lower molar in several extant and extinct species of Equus and explore its relationship with life history events. Our histological analysis shows that enamel extends beyond the molar’s cervix in these mammals. We identified three different crown developmental stages (CDS) in the first lower molars of equids characterised by different growth rates and likely to be related to structural and ontogenetic modifications of the tooth. Enamel extension rate, which ranges from ≈400 μm/d at the beginning of crown development to rates of ≈30 μm/d near the root, and daily secretion rate (≈17 μm/d) have been shown to be very conservative within the genus. From our results, we also inferred data of molar wear rate for these equids that suggest higher wear rates at early ontogenetic stages (13 mm/y) than commonly assumed. The results obtained here provide a basis for future studies of equid dentition in different scientific areas, involving isotope, demographic and dietary studies.

Facial skeleton asymmetry and its relationship to mastication in the Early Medieval period (Great Moravian Empire, Mikulčice, 9th–10th century)

ObjectivesThe aim of this study was to analyse the relationship of mastication and directional asymmetry (DA) of upper facial skeleton in Early Medieval sample from the Mikulčice settlement (Czech Republic). DesignThe settlement is divided into two burial areas of presumably different socioeconomic status: the castle and the sub-castle. The material consisted of 193 individuals (125 castle, 68 sub-castle). The relationship of facial skeleton DA and mastication was analysed by examining tooth wear and mandibular shape by means of 3D geometric morphometrics. Tooth wear of premolars and molars was evaluated using appropriate scoring systems. 3D coordinates of 35 mandibular landmarks were scanned using MicroScribe G2X digitizing system. ResultsThe results did not reveal any significant differences in tooth wear DA or mandible DA values between burial areas or sexes. Mandibular shape, however, differed significantly between burial areas and sexes. Directional changes of mandibular landmarks supported a right chewing side preference in the sample. Significant relationship between upper facial skeleton DA and mandible DA was recorded. ConclusionsDifferences in subsistence between burial areas and sexes did not translate into differences in mandible DA and dental wear. However, mandibular shape analysis revealed prominence of areas affected by masticatory muscles in individuals from the castle. Higher consumption of tough material, such as meat, has been proposed as possible explanation. The right side was found to be preferential for chewing. The relationship between upper facial skeleton DA and mandible DA was concluded to be the result of the compensatory and adaptive function of mandible.

Dental evidence for wild tuber processing among Titicaca Basin foragers 7000 ybp.

The objective of this work is to characterize dental wear in a skeletal sample dating to the Middle/Late Archaic period transition (8,000-6,700 cal. B.P.) from the Lake Titicaca Basin, Peru to better define subsistence behaviors of foragers prior to incipient sedentism and food production. The dental sample consists of 251 teeth from 11 individuals recovered from the site of Soro Mik'aya Patjxa (SMP), the earliest securely dated burial assemblage in the Lake Titicaca Basin and the only burial assemblage in the region from an unequivocal forager context. Occlusal surface wear was quantified according to Smith (1984) and Scott (1979a) to characterize diversity within the site and to facilitate comparison with other foraging groups worldwide. General linear modeling was used to assess observation error and principal axis analysis was used to compare molar wear rates and angles. Teeth were also examined for caries and specialized wear. Occlusal surface attrition is generally heavy across the dental arcade and tends to be flat among posterior teeth. Only one carious lesion was observed. Five of the 11 individuals exhibit lingual surface attrition of the maxillary anterior teeth (LSAMAT). Tooth wear rates, molar wear plane, and caries rates are consistent with terrestrial foraging and a diverse diet. The presence of LSAMAT indicates tuber processing. The results therefore contribute critical new data toward our understanding of forager diet in the Altiplano prior to plant and animal domestication in the south-central Andes.

Convergent Traits in Mammals Associated with Divergent Behaviors: the Case of the Continuous Dental Replacement in Rock-Wallabies and African Mole-Rats

The study of convergences in mammals is crucial to understand the evolutionary processes underlying the origin of shared traits. A classic example is the independent evolution in the pygmy rock-wallaby, the silvery mole-rat, and manatees of continuous dental replacement to compensate for high dental wear. The origins of continuous dental replacement in mammals remain unresolved. As the functional study of a trait may permit pinpointing the adaptive nature of its independent evolution, we aimed at comparing first the morpho-functional characteristics of the masticatory apparatus between the pygmy rock-wallaby and their closest relatives, and then with some published data on the silvery mole-rat. 3D geometric morphometric and biomechanical analyses were complemented by dental microwear analyses. Our results showed that the pygmy rock-wallaby clearly departs from its relatives in having a wider skull, a shorter snout, and a dentition situated more distally. These cranial modifications, previously observed in the silvery mole-rat, are probably linked with a neotenic development. Because of higher developmental constraints on marsupial skulls, such adjustment in the pygmy rock-wallaby may have improved the force generated by adductor muscles at molars for comminution of tough and abrasive plants. In contrast, the strong attrition combined with the ingestion of dust during high activity of digging and feeding might contribute to both molar damage and high wear in the silvery mole-rat. Our results stress the importance of combining morphological, developmental, and functional data to show that different behaviors related to ecology can explain the convergent occurrence of continuous dental replacement in mammals.

Quantitative and Qualitative Assessment of the Wear of Primary EnamelAgainst Three Types of Full Coronal Coverage

Aims: the objective of the study was to assess the wear of primary teeth against three types of crown coverage, both quantitavely and qualitatively. Methods: specimens of 30 extracted primary molars, were mounted against 10 specimens of zirconia crowns (group A), 10 specimens of preveneered stainless steel crowns (group B), and 10 extracted primary molars and 10 specimens of stainless steel crowns (group C) and were undergone in vitro wear testing using an abrasive machine. Measurement of the amount of weight loss was performed, in addition to a scanning electron microscopic examination of the worn enamel surfaces. Results: the greatest wear was recorded in zirconium specimens, and the lowest was in preveneered stainless steel crowns with a significant difference noted between the three groups (p<0.001).The micro-morphological wear characteristics revealed the most aggressive wear with complete loss of enamel structure in zirconium specimens. Conclusions: the zirconium crowns induced the most severe wear in primary molars, followed by stainless steel crowns, and the least wear was induced by preveneered stainless steel crowns.

Quantitative measurement of maxillary second molar wear using Korean virtual dental models

Quantitative measurement of maxillary second molar wear using Korean virtual dental models

A revision of the Late Cretaceous–Paleocene eutherian mammalCimolestesMarsh, 1889

Cimolestes Marsh is a North American eutherian mammal primarily known from latest Cretaceous deposits in Alberta, Wyoming, Saskatchewan, and Montana. At present, five species of Cimolestes are considered valid, all Lancian in age; they include one of the largest North American Late Cretaceous therian mammals as well as one of the smallest, a size range far exceeding that within other genera of tribosphenic therians contemporary with Cimolestes, such as the leptictoid eutherian Gypsonictops Simpson or genera of alphadontid or pediomyid marsupials. Moreover, the species of Cimolestes display a disparity of dental morphology in addition to size well in excess of interspecific differences within these genera. Given these considerations, Cimolestes is clearly a grade-taxon, uniting species sharing an adaptively subzalambdodont dentition, but showing divergent specializations within this pattern that are inconsistent with monophyly of its presently included species. To correct these imbalances, this paper limits Cimolestes to Cimolestes incisus Marsh and Cimolestes stirtoni Clemens; Cimolestes magnus Clemens and Russell, Cimolestes cerberoides Lillegraven, and Cimolestes propalaeoryctes Lillegraven are reclassified in the new genera Altacreodus, Ambilestes, and Scollardius, respectively. Altacreodus magnus, having a massive shearing dentition, is reconfirmed as showing a relationship to some Tertiary ‘creodonts’ not shared by other species of Lancian cimolestids; Ambilestes cerberoides exhibits a distinctive molar wear pattern that emphasized horizontal grinding, not orthal shear; Scollardius propalaeoryctes, the smallest species in this revision and having hyper-faunivorous molars, was not ancestral to Paleogene Palaeoryctidae, as indicated in part by contradictions in premolar number and morphology.

Tooth wear and feeding ecology in mountain gorillas from Volcanoes National Park, Rwanda.

Ecological factors have a dramatic effect on tooth wear in primates, although it remains unclear how individual age contributes to functional crown morphology. The aim of this study is to determine how age and individual diet are related to tooth wear in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. We calculated the percent of dentine exposure (PDE) for all permanent molars (M1-M3) of known-age mountain gorillas (N = 23), to test whether PDE varied with age using regression analysis. For each molar position, we also performed stepwise multiple linear regression to test the effects of age and percentage of time spent feeding on different food categories on PDE, for individuals subject to long-term observational studies by the Dian Fossey Gorilla Fund International's Karisoke Research Center. PDE increased significantly with age for both sexes in all molars. Moreover, a significant effect of gritty plant root consumption on PDE was found among individuals. Our results support prior reports indicating reduced tooth wear in mountain gorillas compared to western gorillas, and compared to other known-aged samples of primate taxa from forest and savanna habitats. Our findings corroborate that mountain gorillas present very low molar wear, and support the hypothesis that age and the consumption of particular food types, namely roots, are significant determinants of tooth wear variation in mountain gorillas. Future research should characterize the mineral composition of the soil in the Virunga habitat, to test the hypothesis that the physical and abrasive properties of gritty foods such as roots influence intra- and interspecific patterns of tooth wear.

Dust in the wind: How climate variables and volcanic dust affect rates of tooth wear in Central American howling monkeys.

Two factors have been considered important contributors to tooth wear: dietary abrasives in plant foods themselves and mineral particles adhering to ingested food. Each factor limits the functional life of teeth. Cross-population studies of wear rates in a single species living in different habitats may point to the relative contributions of each factor. We examine macroscopic dental wear in populations of Alouatta palliata (Gray, 1849) from Costa Rica (115 specimens), Panama (19), and Nicaragua (56). The sites differ in mean annual precipitation, with the Panamanian sites receiving more than twice the precipitation of those in Costa Rica or Nicaragua (∼3,500 mm vs. ∼1,500 mm). Additionally, many of the Nicaraguan specimens were collected downwind of active plinian volcanoes. Molar wear is expressed as the ratio of exposed dentin area to tooth area; premolar wear was scored using a ranking system. Despite substantial variation in environmental variables and the added presence of ash in some environments, molar wear rates do not differ significantly among the populations. Premolar wear, however, is greater in individuals collected downwind from active volcanoes compared with those living in environments that did not experience ash-fall. Volcanic ash seems to be an important contributor to anterior tooth wear but less so in molar wear. That wear is not found uniformly across the tooth row may be related to malformation in the premolars due to fluorosis. A surge of fluoride accompanying the volcanic ash may differentially affect the premolars as the molars fully mineralize early in the life of Alouatta.

Temporal changes in molar wear rate of a sika deer population under density‐dependent food limitation

AbstractNegative effects of density‐dependent food limitation on molar wear rate in ungulate populations, as well as unworn molar size and its sex differences in ruminants, have been studied for a long time. However, these studies were based on comparisons of populations from different districts or habitats. If drastic changes in food habits and life history occurred under density‐dependent resource limitation, it is of great interest whether this change caused temporal changes in molar wear rate, and whether the degree of hypsodonty changed under this short but intensive selective pressure. We examined the temporal change in molar wear rate using long‐term monitoring data of a sika deer (Cervus nipon) population on Nakanoshima Island, Hokkaido, Japan. Corresponding to the change in food habits, the molar wear rate changed mainly because of the amount of soil that was secondarily ingested when deer fed on fallen leaves. Molar wear rate was the fastest level after the first population crash on Nakanoshima Island among extant sika deer populations. Nevertheless, we did not find any evidence of increased hypsodonty in Nakanoshima deer. It is possible that natural selection for increased molar durability (hypsodonty) has been working on Nakanoshima deer, but the adaptive change has not yet appeared at a statistically significant level.

Wear on the deciduous molars in a Mediaeval English human population: a study using crown height

This work comprises a study of mandibular deciduous molar wear in an archaeological population using measurement of crown height. The aims are twofold. Firstly, to investigate the nature of the relationship between wear on the deciduous molars and dental age. Secondly, to evaluate, using crown height, two existing methods of recording deciduous molar wear: the measurement of the percent of the occlusal surface made up of exposed dentine described by Clement and Freyne (2012), and the ordinal wear stage method of Dawson and Robson Brown (2013). The study material is immature skeletal remains (N = 76, dental age range 15 months–11.5 yrs) from a British Mediaeval site. Results show that crown height bears an approximately linear relationship with dental age for both first and second deciduous molars, and regression residuals are homoscedastic suggesting little inter-individual variation in wear rates. The second molar wears at a faster rate and its crown height bears a closer relationship with dental age. In the second molar, percent dentine exposure bears a non-linear relationship with dental age and with crown height, and for both molars the regression residuals of percent dentine exposed upon dental age are heteroscedastic. The ordinal wear stages of Dawson and Robson Brown (2013) are strongly correlated with dental age but different wear stages may correspond to dissimilar increments of crown height. Molar crown height is a sensitive and direct measure of occlusal wear, and its homoscedastic, linear relationship with dental age facilitates controlling for the effects of age when dental wear is used to study childhood diet in archaeological populations.

Laminin‐332 deficient mice present defects during tooth enamel development (LB547)

The epithelial ameloblasts are separated from the maturing enamel surface by an atypical basal lamina (BL) that is enriched in laminin (Lm)‐332. This heterotrimeric protein (α3, ß3 and γ2 chains) provides structural integrity to BLs and exerts effects on various epithelial cell processes including cell adhesion. Mouse models that lack expression of individual Lm‐332 chains die shortly after birth. However, recently a viable mouse model of Lm‐332 deficiency has been developed which expresses a doxycycline‐controllable human Lm γ2 transgene under the cytokeratin 14 promoter on the Lm γ2 knockout background (PLoS One 7(9):e45546). To investigate the role of Lm‐332 in enamel development, we examined the upper and lower maxillae from ~8‐week‐old wt and Lm‐332 deficient mice. At the light microscope level, incisors from Lm‐332 deficient mice showed severe structural changes at the level of the enamel organ. In decalcified samples, the organic matrix of forming enamel was altered and residual matrix was found throughout the maturation stage, suggesting Lm‐332 is required for both formation and mineralization of enamel. CT‐scans and scanning electron microscope analyses showed that Lm‐332 deficient mice exhibited hypomineralized enamel layer and occlusal surface wear in molars. The alterations in enamel formation observed in this mouse model are similar to those in teeth of patient with junctional epidermolysis bullosa due to Lm‐332 mutations. These mice will be an invaluable tool to study the role of Lm‐332 in enamel formation and better understand the role of the atypical BL found at cell‐enamel interfaces.Grant Funding Source: Supported by CIHR, NIH/NHLBI P01HL029594, Shriners of North America

A Comparison of Observed Molar Wear Rates in Extant Herbivorous Mammals

Here we review published molar wear rates, measured in terms of tooth height loss per year (mm yr-1) published on natural populations of ungulates (25 species), rodents and lagomorphs (Glires; 14 species) and macropodid marsupials (seven species). Although the data are limited, they nevertheless reveal consistent patterns, and raise new questions. Among ungulates, wear rates are uncorrelated with body mass but are positively correlated with hypsodonty. Browsers show lower wear rates than do mixed feeders or grazers. Percentage of grass in the diet shows a non-linear relationship with wear rates suggesting that levels of dietary abrasives result from a complex interaction among forages, habitat characteristics and feeding behaviours (whether or not grass itself is a significant abrasive agent). Rodents exhibit higher wear rates, and kangaroos lower wear rates, than do ungulates feeding on similar diets. Hypselodont rodents and lagomorphs show rates of molar wear an order of magnitude higher than do grazing ungulates.