Dental topography and molar wear in Alouatta palliata from Costa Rica

Paleoprimatologists depend on relationships between form and function of teeth to reconstruct the diets of fossil species. Most of this work has been limited to studies of unworn teeth. A new approach, dental topographic analysis, allows the characterization and comparison of worn primate teeth. Variably worn museum specimens have been used to construct species-specific wear sequences so that measurements can be compared by wear stage among taxa with known differences in diet. This assumes that individuals in a species tend to wear their molar teeth in similar ways, a supposition that has yet to be tested. Here we evaluate this assumption with a longitudinal study of changes in tooth form over time in primates. Fourteen individual mantled howling monkeys (Alouatta palliata) were captured and then recaptured after 2, 4, and 7 years when possible at Hacienda La Pacifica in Costa Rica between 1989-1999. Dental impressions were taken each time, and molar casts were produced and analyzed using dental topographic analysis. Results showed consistent decreases in crown slope and occlusal relief. In contrast, crown angularity, a measure of surface jaggedness, remained fairly constant except with extreme wear. There were no evident differences between specimens collected in different microhabitats. These results suggest that different individual mantled howling monkeys wear their teeth down in similar ways, evidently following a species-specific wear sequence. Dental topographic analysis may therefore be used to compare morphology among similarly worn individuals from different species.     

A coprological survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata

Fecal samples from 155 mantled howling monkeys (Alouatta palliata palliata) examined at Centro Ecologico La Pacifica, Guanacaste Province, Costa Rica, revealed 75 (48%) had parasitic infections. A sampling of nine howling monkeys from Santa Rosa National Park. Costa Rica indicated only one infected animal (11%). Only three of 19 (16%) spider monkeys (Ateles geoffroyi) also from Santa Rosa were infected. Controrchis biliophilus, Trypanoxyuris minutus, unidentified strongylid eggs and Isospora sp. oocysts were found. Three monkeys from La Pacifica died and were examined for adult helminths. They were infected with Ascaris lumbricoides, C. biliophilus and T. minutus.     

Dust accumulation in the canopy: A potential cause of dental microwear in primates

Dental microwear researchers consider exogenous grit or dust to be an important cause of microscopic wear on primate teeth. No study to date has examined the accumulation of such abrasives on foods eaten by primates in the forest. This investigation introduces a method to collect dust at various heights in the canopy. Results from dust collection studies conducted at the primate research stations at Ketambe in Indonesia, and Hacienda La Pacifica in Costa Rica indicate that 1) grit collects throughout the canopy in both open country and tropical rain forest environments; and 2) the sizes and concentrations of dust particles accumulated over a fixed period of time differ depending on site location and season of investigation. These results may hold important implications for the interpretation of microwear on primate teeth. © 1995 Wiley-Liss, Inc.     

Food procurement and tooth use in two sympatric lemur species

This study of two lemur species (Lemur catta and Propithecus v. verreauxi) in Madagascar combines observations of food procurement and initial food placement in the mouth with comparisons to food toughness and external properties. Food toughness was hypothesized to play a decisive role in determining food placement during ingestion. It was found that tougher foods are generally ingested on the postcanines for all foods eaten. However, when leaves and fruits are analyzed separately, food size and shape, represented here by mass and food type, are more reliable predictors of initial food placement. Larger leaves and bulkier fruits and stalks are ingested posteriorly. Leaf toughness is not related to leaf size, though the toughness and size of the most commonly eaten fruits are correlated. Furthermore, ingestive food toughness, which is the maximum toughness, and "average" food toughness may make different mechanical demands on the masticatory apparatus that have consequences for jaw morphology.     

Interpreting food processing through dietary mechanical properties: a Lemur catta case study

Knowledge of dietary mechanical properties can be informative about physical consequences to consumers during ingestion and mastication. In this article, we examine how Tamarindus indica fruits can affect dental morphology in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly special reserve in southwestern Madagascar. Ring-tailed lemurs in tamarind dominated gallery forests exhibit extreme wear and tooth loss on their postcanine dentition that has been related to processing T. indica fruits. We measured and compared mechanical properties of individual food parts in the diet of ring-tailed lemurs in different seasons in 1999-2000, 2008, and 2010. Fracture toughness, hardness, and modulus of foods were measured with a portable mechanical tester. The ripe fruits of T. indica are indeed the toughest and hardest foods ingested by the lemurs. In addition, they are among the largest foods consumed, require high numbers of ingestive bites to process, and are the most frequently eaten by volume. During controlled cutting tests of the ripe fruit shell, multiple runaway side cracks form alongside the cut. Similarly, the lemurs repeatedly bite the ripe shell during feeding and thereby introduce multiple cracks that eventually fragment the shell. Studies of enamel microstructure (e.g., Lucas et al.: BioEssays 30 (2008) 374-385; Campbell et al., 2011) advance the idea that the thin enamel of ring-tailed lemur teeth is susceptible to substantial micro-cracking that rapidly erodes the teeth. We conclude that micro-cracking from repeated loads, in combination with the mechanical and physical properties of the fruit, is primarily responsible for the observed dental damage.     

新疆罗布泊小河墓地居民的口腔健康与饮食

小河墓地是新疆罗布泊地区一处重要的早期青铜时代墓地。本文主要对该墓地出土颅骨所附牙齿的磨耗程度及牙结石沉积状况进行了观察、量化统计和分析,同时也对该人群其他的口腔疾病如根尖脓肿、颞下颌关节病变、生前牙齿脱落等做了简单的统计,以期从古病理学的角度获取当时居民的口腔健康、食物类型和饮食习惯等信息。本研究发现:1)小河人群的牙齿磨耗程度远远高于对比组的古代居民,其上腭圆枕及颞下颌关节炎出现率较高,存在牙齿崩裂现象,且其前后部牙齿磨耗差异不大。这一方面说明其食物加工技术比较落后,食物粗糙坚硬;另一方面小河居民的经济生活方式和食物构成都比较复杂,不同的食物对前部和后部牙齿磨耗的程度造成了不同的影响;此外,小河人群风沙肆虐的生活环境也对其严重牙齿磨耗的形成产生了一定影响。2)小河人群异常严重的牙结石沉积归功于其高蛋白质和碳水化合物的饮食,以及生活用水的水质。3)统计分析发现两性存在上、下颌犬齿的磨耗差异,而这一情况可能暗示了在家庭手工业方面存在男女分工的现象。     

Dental microwear in live, wild-trapped Alouatta palliata from Costa Rica

One problem with dental microwear analyses of museum material is that investigators can never be sure of the diets of the animals in question. An obvious solution to this problem is to work with live animals. Recent work with laboratory primates has shown that high resolution dental impressions can be obtained from live animals. The purpose of this study was to use similar methods to begin to document rates and patterns of dental microwear for primates in the wild. Thirty-three Alouatta palliata were captured during the wet season at Hacienda La Pacifica near Canas, Costa Rica. Dental impressions were taken and epoxy casts of the teeth were prepared using the methods of Teaford and Oyen (1989a). Scanning electron micrographs were taken of the left mandibular second molars at magnifications of 200x and 500x. Lower magnification images were used to calculate rates of wear, and higher magnification images were used to measure the size and shape of microwear features. Results indicate that, while basic patterns of dental microwear are similar in museum samples and samples of live, wild-trapped animals of the same species, ecological differences between collection locales may lead to significant intraspecific differences in dental microwear. More importantly, rates of microwear provide the first direct evidence of differences in molar use between monkeys and humans.     

Population trends of the mantled howler groups of La Pacifica,Guanacaste, Costa Rica

A complete survey of La Pacifica in Guanacaste Province, Costa Rica was conducted in July 1984 in order to determine whether the howler (Alouatta palliata) population had declined since 1972 as a result of deforestation. During the 6-day survey, 257 howlers were located, representing 16 different social groupings and nine solitary animals. The total number of howlers, the number and location of groups, and the age-sex composition were very similar to a 1972–1976 survey of the same population. Age-sex composition of La Pacifica howler groups was similar to those of another population of mantled howlers in Costa Rica and of populations in Mexico and in Panama, although La Pacifica had a higher mean number of adult females per group. There was no evidence to support the hypothesis that the La Pacifica howler population has declined in recent times.     

Patterns of molar wear in hunger-gatherers and agriculturalists

Tooth wear records valuable information on diet and methods of food preparation in prehistoric populations or extinct species. In this study, samples of modern and prehistoric hunger-gatherers and agriculturalists are used to test the hypothesis that there are systematic differences in patterns of tooth wear related to major differences in subsistence and food preparation. Flatness of molar wear is compared for five groups in hunger-gatherers (N = 298) and five groups of early agriculturalists (N = 365). Hunger-gatherers are predicted to develop flatter molar wear due to the mastication of tough and fibrous foods, whereas agriculturalists should develop oblique molar wear due to an increase in the proportion of ground and prepared food in the diet. A method is presented for the quantitative measurement and analysis of flatness of molar wear. Comparisons of wear plane angle are made between teeth matched for the same stage of occlusal surface wear, thus standardizing all groups to the same rate of wear. Agriculturalists develop highly angled occlusal wear planes on the entire molar dentition. Their wear plane angles tend to exceed hunger-gatherers by about 10 degrees in advanced wear. Wear plane angles are similar within subsistence divisions despite regional differences in particular foods. This approach can be used to provide supporting evidence of change in human subsistence and to test dietary hypotheses in hominoid evolution.     

Effects of dietary fracture toughness and dental wear on chewing efficiency in geladas (Theropithecus gelada)

Chewing efficiency has been associated with fitness in mammals, yet little is known about the behavioral, ecological, and morphological factors that influence chewing efficiency in wild animals. Although research has established that dental wear and food material properties independently affect chewing efficiency, few studies have addressed the interaction among these factors. We examined chewing efficiency, measured as mean fecal particle size, as a function of seasonal shifts in diet (and corresponding changes in food fracture toughness) in a single breeding population of a grazing primate, the gelada monkey, at Guassa, Ethiopia. We also measured dental topographic traits (slope, angularity, and relief index) and relative two‐ and three‐dimensional shearing crest lengths in a cross‐sectional wear series of gelada molars. Chewing efficiency decreased during the dry season, a pattern corresponding to the consumption of foods with higher fracture toughness. Older individuals experienced the most pronounced decreases in chewing efficiency between seasons, implicating dental wear as a causal factor. This pattern is consistent with our finding that dental topographic metrics and three‐dimensional relative shearing crest lengths were lowest at the last stage of wear. Integrating these lines of behavioral, ecological, and morphological evidence provides some of the first empirical support for the hypothesis that food fracture toughness and dental wear together contribute to chewing efficiency. Geladas have the highest chewing efficiencies measured thus far in primates, and may be analogous to equids in their emphasis on dental design as a means of particle size reduction in the absence of highly specialized digestive physiology. Am J Phys Anthropol 155:17–32, 2014. © 2014 Wiley Periodicals, Inc.     

Survey of the howling monkey population at La Pacifica: A seven-year follow-up

We surveyed the howling monkey population at La Pacifica in Costa Rica over a 1-month period in July and August 1991. The survey method consisted of an initial 6-day survey, directly comparable to a 1984 survey, and at least two repeat surveys of all areas to locate all groups and to identify all animals. The initial survey indicated an increase in the number of groups and a decrease in the size of groups from earlier surveys, though the group composition was unchanged. We used the results of initial and repeat surveys to determine population size and composition. We located 30 groups with a total of 370 animals. Twenty-one groups contained animals marked with collars and/or legbands, and four additional groups contained animals with clearly identifiable white markings. Although the population structure has changed over 7 years, it is still within the species-typical range for Alouatta palliata.     

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     

Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs

Data collected on the feeding behavior, food intake, and chemical analyses of plant foods were used to document seasonal variation in diet and nutrition in Eulemur mongoz in northwestern Madagascar. E. mongoz conforms to the general Eulemur dietary pattern, with a predominantly frugivorous diet supplemented mainly by leaves, flowers, and nectar. Phytochemical analysis revealed high water contents in all the main plant foods; mature fruit and flowers contained the most water-soluble carbohydrates; immature leaves were richest in protein and essential amino acids; the limiting amino acids in all plant foods were methionine and cystine; ash (mineral) content was highest in petioles and mature leaves; crude lipid content was highest in seeds; and crude fiber content was indistinguishable between immature and mature fruit and leaves. High-fiber foods were eaten during both seasons; the wet season diet was dominated by high-energy foods (mature fruit, nectar, and seeds), while the dry season diet contained foods high in energy (mature fruit and flowers) and high in protein (immature leaves) and minerals (mature leaves and petioles). However, nutrient intake did not vary between seasons, implying that nutrient requirements are met throughout the year. These results suggest we draw more conservative conclusions when interpreting dietary variability in the absence of chemical analysis, and also draw into question the idea that nutritional stress is a factor in the timing of reproduction in lemurs and, by extension, is linked to the prevalence of female dominance and small group size in lemurs.     

A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar

Chemical deterioration of teeth is common among modern humans, and has been suggested for some extinct primates. Dental erosion caused by acidic foods may also obscure microwear signals of mechanical food properties. Ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar, display frequent severe tooth wear and subsequent tooth loss. In contrast, sympatric Verreaux's sifaka display far less tooth wear and infrequent tooth loss, despite both species regularly consuming acidic tamarind fruit. We investigated the potential impact of dietary acidity on tooth wear, collecting data on salivary pH from both species, as well as salivary pH from ring-tailed lemurs at Tsimanampesotse National Park, Madagascar. We also collected salivary pH data from ring-tailed lemurs at the Indianapolis Zoo, none of which had eaten for at least 12 hr before data collection. Mean salivary pH for the BMSR ring-tailed lemurs (8.098, n=41, SD=0.550) was significantly more alkaline than Verreaux's sifaka (7.481, n=26, SD=0.458). The mean salivary pH of BMSR (8.098) and Tsimanampesotse (8.080, n=25, SD=0.746) ring-tailed lemurs did not differ significantly. Salivary pH for the Indianapolis Zoo sample (8.125, n=16, SD=0.289) did not differ significantly from either the BMSR or Tsimanampesotse ring-tailed lemurs, but was significantly more alkaline than the BMSR Verreaux's sifaka sample. Regardless of the time between feeding and collection of pH data (from several minutes to nearly 1 hr), salivary pH for each wild lemur was above the "critical" pH of 5.5, below which enamel demineralization occurs. Thus, the high pH of lemur saliva suggests a strong buffering capacity, indicating the impact of acidic foods on dental wear is short-lived, likely having a limited effect. However, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. These data also suggest that salivary pH varies between lemur species, corresponding to broad dietary categories.     

Growth of Mantled Howler Groups in a Regenerating Costa Rican Dry Forest

We examined population dynamics in mantled howlers (Alouatta palliata palliata) in a regenerating tropical dry forest in Santa Rosa National Park (SRNP), Costa Rica. The population has grown at a rate of about 7% per annum during the past decade. The growth in numbers from 342 in 1984 to 554 in 1992 reflects an increase in the number of groups (from 25 to 34) and a slight increase in their average size (from 13.6 to 16.3). Population density has increased from 4.9 to 7.9 individuals per km ². Santa Rosa's population density and group compositions are similar to those at several other mantled howler sites, but densities of mantled howlers are much higher at two other well-studied sites: La Pacifica and Barro Colorado Island (BCI). We relate the low density of howlers at Santa Rosa to local historical and ecological factors. Howler populations at high and low densities differ in average group size and sex ratio. At high population densities, groups are larger and include more adult females. The number of male howlers per group appears to be more strictly limited and less variable than the number of females is. However, there is greater variation in male group membership at Santa Rosa than at La Pacifica or BCI, and at Santa Rosa there are more generating forests available into which males and females can disperse and form new groups. We present case studies describing two ways in which new howler groups are formed, and we suggest that, compared to females and compared to males at high density sites, males are relatively advantaged in the uncrowded habitats at Santa Rosa and other low density sites.     

Tooth chipping can reveal the diet and bite forces of fossil hominins

Mammalian tooth enamel is often chipped, providing clear evidence for localized contacts with large hard food objects. Here, we apply a simple fracture equation to estimate peak bite forces directly from chip size. Many fossil hominins exhibit antemortem chips on their posterior teeth, indicating their use of high bite forces. The inference that these species must have consumed large hard foods such as seeds is supported by the occurrence of similar chips among known modern-day seed predators such as orangutans and peccaries. The existence of tooth chip signatures also provides a way of identifying the consumption of rarely eaten foods that dental microwear and isotopic analysis are unlikely to detect.     

Factors Influencing Interannual and Intersite Variability in the Diet of <Emphasis Type="Italic">Trachypithecus francoisi</Emphasis>

Comparative studies of the diet of the same species in different habitats, and over the long term, are essential to understanding a species’ behavioral and ecological plasticity. Moreover, such studies can help researchers and managers evaluate a species’ capacity to cope with changes in habitat quality resulting from natural processes or human disturbance, which is important for developing conservation strategies. We compared dietary data for François’ langur (Trachypithecus francoisi) collected at Nonggang and Fusui Nature Reserves, Guangxi Province, China, over 2 separate study periods to evaluate interannual and intersite variation in diet. Young leaves were the preferred staple foods for langurs, whereas mature leaves and seeds served as fallback foods in response to seasonal shortage in the abundance of young leaves. Species composition of the diets and the percentage of feeding records for plant species varied between the 2 study periods. The langurs at both study sites fed selectively, and they did not base their diet simply on the abundance of plant species in the habitat. However, the plant species eaten by langur groups inhabiting the 2 different reserves were markedly different, and the top 10 food species eaten by the Fusui group showed no overlap with those eaten by the Nonggang group. The variation may be related to differences in forest composition resulting from different level of human disturbance. In summary, our results indicate that François’ langurs exhibit a comparable dietary pattern both temporally and geographically, but there is marked interannual and intersite difference in species composition of the langur diet.     

Mantled howler population of Hacienda La Pacifica, Costa Rica, between 1991 and 1998: effects of deforestation

A survey of the mantled howler (Alouatta palliata) population on Hacienda La Pacifica, Guanacaste, Costa Rica, was done in July and August of 1998 to determine population parameters following deforestation due to major canal construction between 1990 and 1994. The survey was carried out in a manner identical to our 1991 survey and consisted of a single pass and two re-surveys of all forested areas of the farm. As canal construction effectively increased fragmentation of the habitat, we predicted decreased population and group size over this time. Results indicated that between the 1991 and 1998 survey, group size decreased but not significantly, and there were significantly fewer adult males and adult females per group. Population size, however, remained unchanged as there was an increase in animals in the immature age classes. An increase in the infant to adult female ratio suggests a stable or even expanding population, which could represent recovery from the initial disturbance of deforestation. Thus, despite changes in the forest and land use patterns, the area now appears to support the same number of howlers as found in previous surveys.     

Morphology is not Destiny: Discrepancy between Form,Function and Dietary Adaptation in Bovid Cheek Teeth

Mammal teeth have evolved morphologies that allow for the efficient mechanical processing of different foods, therefore increasing dietary energy uptake for maintenance of high metabolic demands. However, individuals masticate foods with biomechanical properties at odds with the optimal function of a given tooth morphology. Here, we investigate tooth form and function using two quantitative 3D methods at different scales on the same individuals of nine bovid species. Dental topometry quantifies the gross morphology, and therefore, reflects evolutionary adaptive patterns. Surface texture analysis infers mechanical occlusal events, which reflect the actual tooth function, and is free from the influence of morphology. We found that tough foods can be satisfactorily exploited by grazing species with enamel ridge morphologies not more complex than those found in intermediate feeders and browsers. Thus, the evolution of enamel complexity is likely determined by a balance between adaptation and constraints. Wider enamel ridges seem to be a common functional trait in bovids to compensate for severe wear from abrasive foods and/or chipping from hard foods. Our results demonstrate that supposedly essential functional adaptations in tooth morphology may not be required to process food efficiently. This emphasizes the large plasticity between “optimal” morphology and the potential function of the tooth, and underscores the need to appreciate (apparently) maladaptive structures in mammalian evolution as nevertheless effective functioning units.