Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve,Madagascar

In 1987, a long-term study of the demography of Lemur catta was begun in southern Madagascar. Eighty-five ringtailed lemurs were captured, marked, and released. Adult age classes were estimated using patterns of dental attrition. Including young, 155 individuals from nine groups were identified and monitored over 18 months. The study population of the reserve remained stable, with a growth rate of 0.98. Group sizes ranged from nine to 22 individuals (mean 14). Home ranges were larger (32 ha) and population densities lower (135/km²) than those for previously studied populations, and there was a relationship between habitat quality (e.g., no. of large trees) and these factors. At the beginning of the study, there were more adult males than females, but the sex ratio reached 1.00 by the last census. Females first gave birth at 3 years of age, and 80% or more of the females gave birth in 2 consecutive years. Fifty-two percent of the infants died in the first year and, given preliminary findings, only 40% of those born reach adulthood. Age-specific fertility patterns were similar to those reported for anthropoid primates. Forty-seven percent of the adult males migrated or were missing within a year. This included 78% of the 3–4 year olds and 38% of older age classes. No females were observed to migrate. One group split during the study. Demographic patterns are discussed and related to patterns in other populations of ringtailed lemurs as well as in anthropoids.     

Sex Differences in Hadza Dental Wear Patterns

Among hunter-gatherers, the sharing of male and female foods is often assumed to result in virtually the same diet for males and females. Although food sharing is widespread among the hunting and gathering Hadza of Tanzania, women were observed eating significantly more tubers than men. This study investigates the relationship between patterns of dental wear, diet, and extramasticatory use of teeth among the Hadza. Casts of the upper dentitions were made from molds taken from 126 adults and scored according to the Murphy dental attrition scoring system. Females had significantly greater anterior occlusal wear than males when we controlled for age. Males exhibited greater asymmetry in wear, with greater wear on the left side in canines, first premolars, and first molars. We suggest that these sex differences in wear patterns reflect the differences seen in the diet, as well as in the use of teeth as tools.     

Intraspecific variation in hair delta(13)C and delta(15)N values of ring-tailed lemurs (Lemur catta) with known individual histories, behavior, and feeding ecology

Stable carbon and nitrogen isotope compositions were analyzed from hair samples of 30 sympatric ring-tailed lemurs (Lemur catta) inhabiting the Beza Mahafaly Special Reserve, Madagascar. All lemurs were known individuals involved in a longitudinal study, which allowed us to explore the degree to which group membership, sex, health status, and migration influenced their stable isotope compositions. The differences in delta(13)C and delta(15)N values between groups were small (<1.5 per thousand) but highly significant. In fact, each group was tightly clustered, and discriminant function analysis of the stable isotope data assigned individuals to the group in which they were originally collared with over 90% accuracy. In general, the differences between groups reflected the degree to which they utilized forested versus open habitats. As open habitats at Beza Mahafaly often correspond to areas of anthropogenic disturbance, these data suggest that isotopic data can be useful for addressing questions of lemur conservation. There were few sex differences, but significant differences did occur between individuals of normal and suboptimal health, with those in poor health (especially those in the worst condition) being enriched in (15)N and to a lesser degree (13)C compared with healthy individuals. Moreover, lemurs that had emigrated between 2003 and 2004 had different delta(13)C and delta(15)N compositions than their original groups.     

Analysis of dental attrition and mortality in the Medieval village of Tirup, Denmark

New directions and new questions raised in the study of health in the past justify this reanalysis of the pattern of dental attrition in the Medieval Danish population of Tirup. Dental attrition was scored on all permanent molars from the Tirup skeletal sample. Scores were analyzed by means of logistic regression of the probability of having entered a given stage of wear for a given tooth in a way that is very similar to transition analysis. The primary determinant of dental attrition was age at death. In addition to age, the effects of sex, side, and dating were analyzed. In order to assess the homogeneity of the process of wearing teeth down, a third-order polynomial in age-at-death was also fitted to the transition probabilities. It was found that age is the single most important determinant of dental attrition, and that sex or side did not differentiate the rate of attrition. In several transitions, there was evidence of heterogeneity, indicating both random and systematic interpersonal differences in the rate of attrition and an association between the rate of attrition and age-at-death. It was found that attrition proceeded more quickly after AD 1300 than prior to that date. It is suggested that this was due to a possible general deterioration of living conditions in Northern Europe and an increased reliance on grain for food during the first half of the 14th century. The temporal effect on attrition rate accounts for some but not all the observed heterogeneity wear.     

Temporomandibular joint osteoarthritis in a British skeletal population

The potential role of dental function in TMJ osteoarthritis is examined in an ancient British population. Human skeletal remains from five archaeological sites in England (n = 369) were studied to assess the associations between the presence of osteoarthritis and dental function variables, in particular antemortem tooth loss and dental attrition. Individuals aged over 17 years with at least a portion of either the left or right TMJ were included in the study. Each individual was scored for the occurrence of arthritic lesions on the mandibular condyle and glenoid fossa, the level of dental attrition, and antemortem tooth loss. A loglinear analysis was performed with osteoarthritis as the dependent variable and tooth loss, attrition, sex, and age as the independent variables. Tooth loss and sex are not significantly associated with TMJ osteoarthritis when attrition and age are included in the analysis. Attrition is significantly associated with osteoarthritis even when the analysis corrects for age. The significant association of attrition with osteoarthritis suggests that dental functions may have an influence, separate from ageing, on the development of TMJ osteoarthritis.     

Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar

In this paper, I provide data on the possible effects of group size and seasonal changes in food availability on the activity and habitat use patterns of two species of prosimian primate: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). General and subtle seasonal differences were observed between lemur species in (1) group size and composition, (2) activity profiles, and (3) habitat use. Rufous lemur groups were larger (mean = 8 individuals) and contained more adults than red-bellied lemur groups (mean = 3 individuals). The overall degree and distribution of diurnal activity differed between lemur species and varied within species with seasonal changes in food availability. In general, rufous lemurs traveled more often than red-bellied lemurs. During food scarcity, both species increased the amount of time spent feeding, although peak feeding and traveling times differed. Both species also preferred horizontal substrates; however, during food scarcity, red-bellied lemurs used terminal branches more often while feeding than rufous lemurs. In addition, red-bellied lemurs used the lower middle story forest and rested in taller, upper canopy trees more often than rufous lemurs. Differences in activity and habitat use patterns between lemur species were more related to seasonal changes in food availability than overall differences in group size. These behavioral patterns may represent different strategies used by each lemur species to avoid directly competing for similar resources during times of food scarcity. © 1996 Wiley-Liss, Inc.     

Ageing and dental attrition in a medieval rural Danish population

The rate of attrition on the permanent molars may depend on culturally and economically determined conditions of living. In order to analyse the relation the probability of having entered the stages of attrition is analysed by means of logistic regression on age at death. It is shown that not all teeth continue to be worn at the same rate throughout life and that there is an association between advanced attrition and risk of dying. The rate of dental attrition does not differ much by sex but there are some indications that male teeth are worn quicker than female teeth. This greater rate of attrition might be due to greater consumption of food in males than in females. The stages of dental attrition give some information on the age at death but they are poor age indicators on their own.     

Log-linear analysis of dental caries occurrence in four skeletal series.

Four skeletal series (Corinth, Greece; Gran Quivira, New Mexico; Semna South, Sudanese Nubia, and a large group from scattered sites in England) were coded for sex, jaw, tooth group, dental attrition, dental caries, site and time period. Through thec concepts of a basal level of caries and a cariosity gradient, a single model was found which best described the occurrence of this disease in these samples. All factors were found to contribute significantly to the model. Within the possible subsamples the general characteristics are that the profiles of males, of the mandibulae and of those with light attrition are more likely to have lower overall dental caries levels and to be relatively more carious in the back of the mouth than the front when compared to the pooled sample of all teeth and caries. The opposite is also found to be generally true; the teeth of females, maxillae and heavy attrition are associated with more caries, especially toward the front of the mouth. These results imply that samples appearing otherwise homogeneous display much variation. They also reveal distinct regularities in the reactions of diverse human groups to dental caries.     

Self-Assessed General Health and Dental Status Among the Elderly in a Swedish County

A random sample of non-institutionalized elderly people in Örebro County, Sweden, has been examined. The present paper reports on the general health conditions obtained from interviews in this population and on the relation between general health and dental status. Eighty-one percent of the clinically examined subjects considered that they were healthy or fairly healthy. A higher percentage of women as compared to men regarded themselves to be moderately or very ill. Women also used more drugs than men did. Only 6% did not feel strong enough for extensive dental treatment. Physically handicapped people used dental services less than the rest of the population did. Otherwise, general health seemed to have limited influence on the use of dental services. Subjects with better dental status reported less frequent illness, chronic diseases, and medication as compared to subjects with poorer dental status. The self-assessed general health, also in the presence of age, sex, and residence variables, showed significant correlation with the dental status but not if socio-economic variables were also included in a regression model.     

Developmental stress and telomere dynamics in a genetically polymorphic species

A central objective of evolutionary biology is understanding variation in life‐history trajectories and the rate of aging, or senescence. Senescence can be affected by trade‐offs and behavioural strategies in adults but may also be affected by developmental stress. Developmental stress can accelerate telomere degradation, with long‐term longevity and fitness consequences. Little is known regarding whether variation in developmental stress and telomere dynamics contributes to patterns of senescence during adulthood. We investigated this question in the dimorphic white‐throated sparrow (Zonotrichia albicollis), a species in which adults of the two morphs exhibit established differences in behavioural strategy and patterns of senescence, and also evaluated the relationship between oxidative stress and telomere length. Tan morph females, which exhibit high levels of unassisted parental care, display faster reproductive senescence than white females, and faster actuarial senescence than all of the other morph–sex classes. We hypothesized that high oxidative stress and telomere attrition in tan female nestlings could contribute to this pattern, since tan females are small and potentially at a competitive disadvantage even as nestlings. Nestlings that were smaller than nest mates had higher oxidative stress, and nestlings with high oxidative stress and fast growth rates displayed shorter telomeres. However, we found no consistent morph–sex differences in oxidative stress or telomere length. Results suggest that oxidative stress and fast growth contribute to developmental telomere attrition, with potential ramifications for adults, but that developmental oxidative stress and telomere dynamics do not account for morph–sex differences in senescence during adulthood.     

Severe wear and tooth loss in wild ring-tailed lemurs (Lemur catta): a function of feeding ecology, dental structure, and individual life history

The ring-tailed lemurs at Beza Mahafaly Special Reserve, Madagascar, exhibit a high frequency of severe wear and antemortem tooth loss. As part of a long-term study, we collected dental data on 83 living adult ring-tailed lemurs during 2003 and 2004. Among these individuals, 192 teeth were scored as absent. The most frequently missing tooth position is M1 (24%). As M1 is the first tooth to erupt, its high frequency of absence (primarily a result of wear) is not remarkable. However, the remaining pattern of tooth loss does not correlate with the sequence of eruption. We suggest that this pattern is a function of 1) feeding ecology, as hard, tough tamarind fruit is a key fallback food of ring-tailed lemurs living in gallery forests; 2) food processing, as tamarind fruit is primarily processed in the P3-M1 region of the mouth; and 3) tooth structure, as ring-tailed lemurs possess thin dental enamel. The incongruity between thin enamel and use of a hard, tough fallback food suggests that ring-tailed lemurs living in riverine gallery forests may rely on resources not used in the past. When comparing dental health in the same individuals (n=50) between 2003 and 2004, we found that individual tooth loss can show a rapid increase over the span of one year, increasing by as much as 20%. Despite this rapid loss, individuals are able to survive, sometimes benefiting from unintentional assistance from conspecifics, from which partially processed tamarind fruit is obtained. Although less frequent in this population, these longitudinal data also illustrate that ring-tailed lemurs lose teeth due to damage and disease, similar to other nonhuman primates. The relationship between tooth loss, feeding ecology, dental structure, and individual life history in this population has implications for interpreting behavior based on tooth loss in the hominid fossil record.     

Habitat Degradation and Seasonality Affect Physiological Stress Levels of Eulemur collaris in Littoral Forest Fragments

The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.     

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.     

Spatial Ecology of the Endangered Milne-Edwards’ Sifaka (Propithecus edwardsi): Do Logging and Season Affect Home Range and Daily Ranging Patterns?

Primates often live in human-altered habitats; Malagasy lemurs are no exception. It is important to understand if habitat alteration affects primates’ space use patterns across multiple spatial and temporal scales, as this drives population density. We quantified the daily, seasonal, and annual space-use of seven groups of Milne-Edwards’ sifaka (Propithecus edwardsi) living in unlogged and logged rain forest in Ranomafana National Park, Madagascar between December 2002 and November 2003. Concurrent data showed that sifakas consumed higher quality foods in the unlogged than in logged forests; thus we explored how space use patterns were related to energy use strategies. Sifaka groups in the logged rain forest traveled 7–13% less per day than groups in the unlogged rain forest, despite their larger home ranges (median: 46.12 and 23.52 ha, in the logged and unlogged forests, respectively). Sifakas may thus use an energy-minimizing strategy at the scale of the individual day but an energy-maximizing strategy at the annual home range scale. Sifakas exhibited fidelity to the home range across seasons, but their core area of use shifted considerably with season. We found no difference in population density between sites. However, given the interannual variability in sifaka foods, a multiyear study is needed to assess if energy strategies observed in this study are consistent across longer time periods. Our findings suggest that lemurs may persist in logged habitats by altering spatial use patterns; future work should attempt to quantify the threshold level of forest regeneration from logging that will allow lemurs to persist at similar densities as in unlogged forest.     

Paleoepidemiology of a central California prehistoric population from CA-Ala-329: dental disease

Ala-329 is a prehistoric central California site located on the southeastern margin of San Francisco Bay, dating from approximately 500 AD up to pre-European contact. A large earth mound, Ala-329, has yielded many well preserved burials, approximately 300 of which are included in this study. The most common pathological lesions seen in this population are in the dentition. Advanced attrition is pervasive, affecting all individuals with teeth in occlusion for 2 years or more. Deciduous teeth are involved even in very young children and often show severe wear before replacement. In the permanent dentition, all elements are involved by the second decade; in the oldest age category (41+ years), all individuals show severe wear throughout their dentitions. In fact, by the end of the third decade, the majority of individuals have no enamel remaining. Mild periodontal involvement is found in 74% of adults, socket resorption in 53%, and abscesses in 31% of the relevant sample. Interestingly, although dental abscesses are found more than twice as often among males, socket resorption is seen more often among females. Dental caries are seen in only 10 individuals. The high incidence of periodontal remodeling, socket resorption, and dental abscesses is probably a secondary result of severe dental attrition. It is hypothesized that a large quantity of abrasives in the diet is responsible for the extreme degree of attrition, in fact, among the most severe for any population yet described.     

Lemur habitat and dental senescence in Ranomafana National Park, Madagascar

Not only can teeth provide clues about diet, but they also can be indicators of habitat quality. Conspecific groups living in different habitats with different kinds of foods may exhibit different rates of dental attrition because their teeth are less well adapted to some foods than to others. Ecological disequilibrium describes the situation in which animals live in habitats to which they are relatively poorly adapted. We test whether dental senescence, the wear-related decrease in dental functionality that is associated with decreased survival of infants born to older Propithecus edwardsi females, can be explained by ecological disequilibrium. Specifically, we compare the rates of dental wear in sifaka groups living in nearby habitats that differ in the degree of anthropogenically induced disturbance. We hypothesize that sifakas living in disturbed areas have an unusual rate of tooth wear compared to those living in a more pristine area, and that dental senescence is a consequence of an atypically high wear rate in a degraded habitat. To test whether habitat quality affects tooth wear more generally, we compare rates of use-wear in two subsets of Microcebus rufus living in either relatively undisturbed or disturbed habitats. Contrary to our predictions, we did not detect different rates of tooth wear in disturbed versus undisturbed habitats for either species and consider that reproductively detrimental dental senescence in P. edwardsi females is unlikely to be a pathological consequence of ecological disequilibrium.     

Ontogenetic correlates of diet in Malagasy lemurs

There is a well-documented relationship between development and other life-history parameters among anthropoid primates. Smaller-bodied anthropoids tend to mature more rapidly than do larger-bodied species. Among anthropoids of similar body sizes, folivorous species tend to grow and mature more quickly than do frugivorous species, thus attaining adult body size at an earlier age. This pattern conforms to the expectations of Janson and van Schaik's "ecological risk aversion hypothesis," which predicts that rates of growth and maturation should vary in inverse relation to the intensity of intraspecific feeding competition. According to the ecological risk aversion hypothesis (RAH), species experiencing high intraspecific feeding competition will grow and mature slowly to reduce the risk of mortality due to food shortages. Species experiencing low levels of intraspecific feeding competition will shorten the juvenile period to reduce the overall duration of this high-risk portion of the life cycle. This paper focuses on development and maturation in lemurs. We show that folivorous lemurs (such as indriids) grow and mature more slowly than like-sized frugivorous lemurs (e.g., most lemurids), but tend to exhibit faster dental development. Their dental developmental schedules are accelerated on an absolute scale, relative to craniofacial growth, and relative to particular life-history landmarks, such as weaning. Dental development has a strong phylogenetic component: even those lemurids that consume substantial amounts of foliage have slower dental development than those indriids that consume substantial amounts of fruit. Implications of these results for the RAH are discussed, and an explanation for this hypothesis' failure to predict lemur growth schedules is offered. We propose that the differing developmental schedules of folivorous and frugivorous lemurs may reflect different solutions to the ecological problem of environmental instability: some rely on a strategy of low maternal input and slow returns, while others rely on a strategy of high maternal input and fast returns.     

Book review: Advances in Human Palaeopathology

Severe dental wear and tooth loss is often assumed to impede the processing, breakdown, and energetic conversion of food items, thereby negatively impacting individual health, reproduction, and survival. Ring‐tailed lemurs at the Beza Mahafaly Special Reserve demonstrate exceptionally high frequencies of severe dental wear and antemortem tooth loss, yet often survive multiple years with these impairments. To test the hypothesis that these lemurs mitigate tooth loss through behavioral adjustments, we collected 191 h of observational data from 16 focal subjects, eight without tooth loss and eight with between 3% and 44% loss. These data indicate dentally‐impaired ring‐tailed lemurs show compensatory behaviors consistent with the demands of living in a social group. During early afternoon (12:00–14:30 h) individuals with loss showed trends towards higher frequencies of foraging and grooming, while individuals without loss rested significantly more often. Individuals with >10% loss (n = 7) showed higher frequencies of feeding, foraging, and grooming, and lower frequencies of resting during this period than individuals with <10% loss (n = 9). Individuals with tooth loss maintained relatively higher levels of feeding and foraging throughout the day. These individuals licked tamarind fruit at higher frequencies, likely spending more time softening it before ingestion. These individuals did not demonstrate longer feeding bouts overall, although bouts involving tamarinds were significantly longer. Individuals with marked toothcomb wear engaged in higher rates of certain types of allogrooming, demonstrating that social behaviors are used to compensate for reduced grooming efficiency. These data have implications for interpreting behavioral responses to dental impairment in the fossil record. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Comportements alimentaires,aspects biologiques et sociaux au Néolithique : le cas du Crès (Hérault,France)

The aim of this article is to present an anthropological and stable isotope study (carbon and nitrogen) of 49 individuals from the Middle Neolithic population of Le Crès (Béziers, Hérault, France). The age, sex, stature and dental health were compared to the isotopic results to determine the possible relationship between diet and social behaviours. Results show no links between these parameters and the recorded isotopic variability. The study of the dental health shows a high level of attrition, related to the diet and a feminine tendency for caries.     

Social segregation in male,but not female yearling rhesus macaques (Macaca mulatta)

Males and females of many species sex‐segregate, ranging from complete separation of habitats to social segregation within the same space, sometimes varying across seasons and lifespan development. Mechanisms for such segregation are not well understood, though some have suggested that sex differences in preferred juvenile behaviors lead to greater behavioral compatibility within than between sexes. This within‐sex behavioral compatibility may be the source of sex‐segregation. As juvenile behavioral sex differences are well‐documented in rhesus monkeys, we examined sex‐segregation patterns of yearling rhesus monkeys engaged in three different types of behavior: rough play, parallel play, and grooming. We observed male and female rhesus yearlings from five stable long‐term age‐graded social groups of 67–183 animals. Behavioral observations were designed to collect equal numbers of rough play, grooming, and parallel play bouts. In addition, sex composition and proximity to adults was recorded for each bout. Across all behaviors, more all‐male groups and fewer mixed sex‐groups were observed than expected by chance. All‐female groups occurred at the level expected by chance. Thus, males sex‐segregated regardless of type of behavior, while females did not sex‐segregate. Female groups were observed in proximity to adults more often than expected by chance. These results suggest that behavioral compatibility may produce sex‐segregation in male yearling rhesus monkeys, possibly preparing males and females for different social roles and segregation as adults. Am. J. Primatol. 72:87–92, 2010. © 2009 Wiley‐Liss, Inc.