Female biological resiliency: Differential stress response by sex in human remains from ancient Nubia

This research presents male-female differences in stress response evidenced in human remains from the Medieval site of Kulubnarti in Sudanese Nubia. This analysis is unique in that a direct comparison of subadult males and females is rarely possible using archaeological remains. Rather, such analyses invariably rely on evidence of subadult differences retained in adult (sexable) skeletons. In the case of Kulubnarti, natural mummification has made it possible to measure sex-specific differences among subadults as well as adults following five avenues of investigation: 1) mortality, 2) growth and development, 3) enamel hypoplasia, 4) cribra orbitalia, and 5) cortical bone maintenance. A comparison of mean life expectancy (eox) values for males and females aged 10–55+ years revealed a consistent pattern of greater female survivorship, particularly in childhood (age 10 category) where female life expectancy exceeds that of males by 19%. Measures of growth and development, enamel hypoplasia, cribra orbitalia, and cortical bone loss were subsequently used to test a hypothesis of greater female resiliency based on the mortality data. Male-female differences in skeletal maturation are pronounced with male skeletal ages averaging a significant 2.9 years below their dental age. Females show no significant differences with an average skeletal age 0.75 years ahead of dental age. Males begin hypoplasia formation one year earlier than females and, prior to age four, average 18% more hypoplasias (p<0.05). Also, by age 8, males have on average more than twice the frequency of cribra orbitalia (p<0.05). In contrast to their consistent pattern of reduced childhood stress, adult females lose significantly more cortical bone than their male counterparts and have less cortical bone across the adult age range. Nevertheless, females outnumber males of all ages with a sex-ratio below but parallel to that observed in modern populations. The rapid age-related reduction in males relative to females, even in old age, suggests a continuing female resiliency in spite of their greater rate of osteopenia and may reflect a reproductive advantage to the population through heightened female survival and adaptability.     

Epiphyseal union and dental eruption in Macaca mulatta

Age of dental eruption and epiphyseal fusion is estimated for the permanent dentition and long bone epiphyses of rhesus macaques (Macaca mulatta), with 299 skeletons of individuals with known age of death, from the Cayo Santiago skeletal collection. Epiphyses at a given joint tend to fuse at the same time. While males and females tend to have the same pattern of epiphyseal fusion, females' epiphyses fuse earlier than those of males, espeically at the elbow and knee joints. The order of epiphyseal fusion in rhesus macaques follows the general primate pattern. Times of dental eruption for males and females are generally the same, except for the relatively late eruption of the canine in the males. The order of eruption follows a common primate pattern (dm2?M1?I1?I2?M2?(P3,P4)?C?M3). Multiple regressions were calculated in order to allow determination of developmental state, or predictions of chronological age, from epiphyseal fusion and/or dental eruption scores in juvenile rhesus macaques. Standard deviations of residuals from these regressions indicate considerable variation in developmental state among aminals of the same chronological age. The lack of correlation between residuals from the separate skeletal and dental regressions, indicates that skeletal and dental development are largely independent.     

Skeletal development in Pan paniscus with comparisons to Pan troglodytes

Fusion of skeletal elements provides markers for timing of growth and is one component of a chimpanzee's physical development. Epiphyseal closure defines bone growth and signals a mature skeleton. Most of what we know about timing of development in chimpanzees derives from dental studies on Pan troglodytes. Much less is known about the sister species, Pan paniscus, with few in captivity and a wild range restricted to central Africa. Here, we report on the timing of skeletal fusion for female captive P. paniscus (n = 5) whose known ages range from 0.83 to age 11.68 years. Observations on the skeletons were made after the individuals were dissected and bones cleaned. Comparisons with 10 female captive P. troglodytes confirm a generally uniform pattern in the sequence of skeletal fusion in the two captive species. We also compared the P. paniscus to a sample of three unknown‐aged female wild P. paniscus, and 10 female wild P. troglodytes of known age from the Taï National Park, Côte d'Ivoire. The sequence of teeth emergence to bone fusion is generally consistent between the two species, with slight variations in late juvenile and subadult stages. The direct‐age comparisons show that skeletal growth in captive P. paniscus is accelerated compared with both captive and wild P. troglodytes populations. The skeletal data combined with dental stages have implications for estimating the life stage of immature skeletal materials of wild P. paniscus and for more broadly comparing the skeletal growth rates among captive and wild chimpanzees (Pan), Homo sapiens, and fossil hominins. Am J Phys Anthropol 2012. © 2012 Wiley Periodicals, Inc.     

Bilateral asymmetry in skeletal growth and maturation as an indicator of environmental stress.

This study examined the efficacy of bilateral asymmetry in epiphyseal union as an indicator of environmental stress affecting the skeleton. We compared the extent of asymmetry in the postcranial skeleton between two cemetery samples excavated from Medieval Kulubnarti, Sudanese Nubia. Past studies have strongly suggested that these ancient Nubians experienced environmental stress-the early Christian period (550-750 AD) population to a greater extent than the late Christian period (750-1450 AD) population. We hypothesized that if bilateral asymmetry is a reflection of stress, then it should be present or greater in the more stressed population, the early Christian period population, while absent or found to a lesser extent in the less stressed population, the late Christian period population. We computed two mean values, representative of right-side and left-side epiphyseal union, for each individual in both cemetery samples, and tested for significant differences. Bilateral asymmetry was significant in the combined cemetery sample of 90 individuals (P < 0.019). When cemetery samples were tested separately, bilateral asymmetry was significant for the early Christian period sample (P < 0.001), but not for the late Christian period sample. There were no differences attributable to sex. Finally, we discuss why we conclude that environmental stress was favored over a biomechanic explanation as the cause for asymmetry. To the extent that our results support previous findings that early Christian period individuals were more affected by environmental stress than late Christian period individuals, it is reasonable to consider bilateral asymmetry in skeletal growth and maturation a good indicator of environmental stress.     

Environmental stress increases skeletal fluctuating asymmetry in the moor frog Rana arvalis

Whether fluctuating asymmetry (FA) provides a useful metric indicator of the degree of environmental stress experienced by populations is still a contentious issue. We investigated whether the degree of FA in skeletal elements is useful in elucidating the degree of environmental stress experienced by frog populations, and further, tested the proposition that a trait’s sensitivity to stress—as reflected in the degree of FA—is related to the degree of directional selection experienced by the given trait. We compared the degree of FA in four bilateral skeletal elements of male and female moor frogs (Rana arvalis) originating from low (acidified) and neutral pH populations. While the degree of uncorrected FA was unrelated to the degree of acidity, the growth rate and age of the individuals, the size-corrected FA was significantly higher in low than in neutral pH populations and decreased with individual ages and growth rates. In addition, both measures of FA were significantly higher in males and in particular in traits presumably under high sexual selection as indicated by the degree of sexual size dimorphism. All in all, the results indicate that individuals from acidified localities are smaller, younger and exhibit a significantly higher degree of FA than individuals from neutral pH populations. These results constitute the first assessment of FA in amphibians and suggest that the degree of FA in skeletal traits can be a useful indicator of the degree of environmental stress experienced by amphibian populations.     

Patterns of enamel hypoplasia in two medieval populations from Nubia's Batn el Hajar

Analysis of enamel hypoplasia frequencies for two medieval populations representing the earliest and latest Christian periods of ancient Nubia reveals important diachronic shifts in childhood stress. The mean frequency for hypoplastic bands among the early Christians is 4.2, while the late Christian sample has a mean frequency of 3.7. In addition, the earlier Christians show a prolongation of hypoplastic occurrences through childhood corresponding to a prolonged period of intensified childhood mortality. The modal time interval between hypoplastic occurrences is also shorter for the early Christian children. A comparison of hypoplasia frequencies by sex also reveals a pattern of considerable interest. Females show both lower frequencies of hypoplasias as well as a delay in onset. The diachronic differences are consistent with other indications from paleopathology and paleodemography that childhood stress decreased in later Christian times. The sex differences suggest that during the infancy and early childhood females were more resilient than their male counterparts.     

Dental anthropology and paleodemography of the precolumbian populations of hispaniola from the third millennium B.C. to the Spanish conquest

The demography and dental traits of the skeletal samples from the necropoles of Cueva Roja (IIrd millennium b.C.), El Soco (800 a.D) and Juan Dolio (1400 a.D.) have been analyzed. The preceramic sample from Cueva Roja consists of some 50 individuals, the one from El Soco consists of 158 individuals and the one from Juan Dolio of 108 individuals. The demographic analysis has revealed a slight improvement of life conditions from the pre-contact period to the beginning of the contact period. Dental metrical traits show a marked overlapping of the metrical data for the anterior teeth. A reduction can be noted for the posterior teeth, especially for the first molar, from the preceramic period to the later ceramic period. The analysis of nutritional stresses, through the study of dental enamel hypoplasias, reveals a high incidence of stress in the preceramic population. In the preceramic group, it peaks late in childhood (3.5—3.9 years of age) which could be caused by a delay in weaning. Instead the more recent groups (El Soco and Juan Dolio) show evidence of an earlier occurrence of hypoplasia. Both peak at 3.0–3.4 years of age. The frequencies of hypoplasias calculated by type of tooth are less in the Tainos groups than in the preceramic one. From of the data now available, we can suppose that an amelioration of life conditions occurred from the preceramic period to the later ceramic period. As regards the Tainos groups, a slight improvement in life conditions can be noted from the precontact period to the period immediately before the European colonization. The dental non-metric traits show a strong homogeneity within the Taino groups. However, the preceramic group shows more marked differences when compared to the others. This could be supposed to be due to a different demic background between the Tainos and the group from Cueva Roja.     

Skeletal age, dental age, and the maturation of KNM-WT 15000

The skeleton of the Homo erectus boy from West Lake Turkana, Kenya (KNM-WT 15000), is remarkably complete, and this individual has thus provided a case study for several researchers examining Homo erectus growth. Using data from a longitudinal study of Montreal French-Canadian children, it is shown that while dental and skeletal ages match reasonably well at the level of a sample of children, individuals can display differences between skeletal and dental ages of 2 years or more. Furthermore, the relationship between these two markers may change over time in individual children. It is also possible to find children with patterns of dental maturation similar to KNM-WT 15000's pattern in the Montreal sample. Therefore, neither the discrepancy between skeletal age and dental age alone nor the pattern of dental maturation as assessed by dental stages precludes a human-like pattern of growth, including an adolescent growth spurt, for this individual. Some indicators (e.g., estimated body size for predicted age, and enamel formation) do suggest possible growth-patterning differences from modern humans, and therefore earlier maturation is a reasonable hypothesis, but caution is warranted, given the large degree of modern human variation in developmental markers and the inherent uncertainty in precise estimation of KNM-WT 15000's maturational parameters.     

Biocultural analysis of sex differences in mortality profiles and stress levels in the late medieval population from Nova Raca, Croatia

Human skeletal remains of 104 individuals from the late medieval (14th-18th century) Nova Raca cemetery, in continental Croatia, are described. Historic data from the parish Book of the Dead, relevant to a period in the early 19th century, suggest that females may have been under greater stress than males. To test this hypothesis, the skeletal material is analyzed for the presence and distribution of enamel hypoplasias and cribra orbitalia. Observations are also made on the presence and pattern of dental disease, skeletal infection, trauma, osteoarthritis, vertebral degenerative changes, and Schmorl's depression frequencies. The mortuary sample, consisting of 36 subadults and 68 adults, exhibits underrepresentation of subadults, and differential adult male/female mortality profiles. Peak female mortality is between 21-25 years, compared to peak male mortality between 31-35 years. Average adult female age at death is 29.9 years, compared to 34.1 years in adult males. Significant sex differences are present in the frequencies of enamel hypoplasia. Adult females have higher frequencies of hypoplastic teeth, and a larger number of defects in the teeth affected than in males. Subadults in the series also exhibit higher frequencies of hypoplastic teeth, and a larger number of defects in the teeth affected than in adults, documenting a relationship between enamel hypoplasia-causing stress events and reduced life expectancy. Significant sex differences are also present in dental pathology frequencies, possibly reflecting differences in resource access. Sex differences in vertebral osteoarthritis and Schmorl's depression frequencies may reflect differential activity patterns.     

Life stress on the Roman limes in continental Croatia

The purpose of the paper is to analyze and compare the demographic profiles and disease frequencies between a skeletal series from Zmajevac, a settlement on the Danubian limes, and a composite «non-limes» skeletal series consisting of human osteological remains from three large urban settlements to the west of the limes; roman Mursa (modern Osijek), Cibalae (Vinkovci) and Certissia (Štrbinci). To determine if life stresses were different in settlements on the limes the age and sex distribution in Zmajevac was compared to the composite «non-limes» series. All skeletons were also analyzed for the presence of dental pathology, dental enamel hypoplasia, cribra orbitalia, trauma, and physical stress.

Data collected from the skeletal series show that, with the exception of some indicators of physical stress, no significant differences in quality of life is evident. Both series are characterized by an underrepresentation of subadults from the youngest age category and by similar average adult male and female ages at death. In Zmajevac the average ages at death for adult males and females were 40.0 and 39.0 years respectively, in the composite «non-limes» series 37.4 years for both males and females. The frequencies of dental disease, subadult stress indicators, and trauma are similar in both series. The only consistent difference between the two series is noted in the frequencies of skeletal markers of physical stress, in particular the frequencies of vertebral osteoarthritis and Schmorl's defects. Total male and total female vertebral osteoarthritis frequencies in the two series are significantly different, as is the difference in total male frequencies of Schmorl's defects. Young adult males in the Zmajevac series seem to have been experiencing particularly heavy physical strain on the vertebral column. They exhibit significantly higher frequencies of both vertebral osteoarthritis and Schmorl's defects than young adult males from the composite non-limes series.     

Broken ribs: Paleopathological analysis of costal fractures in the human identified skeletal collection from the Museu Bocage,Lisbon, Portugal (late 19th to middle 20th centuries)

Although rarely reported in the anthropological literature, rib fractures are commonly found during the analysis of human skeletal remains of past and modern populations. This lack of published data precludes comparison between studies and restricts an accurate understanding either of the mechanisms involved in thoracic injuries or their impact on past societies. The present study aimed: 1) to report rib fracture prevalence in 197 individuals, 109 males, and 88 females, with ages at death ranging from 13 to 88 years old, from the Human Identified Skeletal Collection, Museu Bocage, Portugal (late 19th‐middle 20th centuries); 2) to test the hypothesis that a higher prevalence of rib stress fractures existed in the 133 individuals who died from respiratory diseases, in a period before antibiotics. The macroscopic analysis revealed 23.9% (n = 47) of individuals with broken ribs. 2.6% (n = 124) out of 4,726 ribs observed were affected. Males presented more rib fractures, and a significantly higher prevalence was noted for older individuals. Fractures were more frequently unilateral (n = 34), left sided (n = 19) and mainly located on the shaft of ribs from the middle thoracic wall. Nineteen individuals presented adjacent fractured ribs. Individuals who died from pulmonary diseases were not preferentially affected. However, a higher mean rate of fractures was found in those who died from pneumonia, a scenario still common nowadays. Since rib involvement in chest wall injury and its related outcomes are important issues both for paleopathology and forensic anthropology, further investigations are warranted. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Accuracy of dental age estimation charts: Schour and Massler,Ubelaker and the London Atlas

Dental age estimation charts are frequently used to assess maturity and estimate age. The aim of this study was to assess the accuracy of estimating age of three dental development charts (Schour and Massler, Ubelaker, and the London Atlas). The test sample was skeletal remains and dental radiographs of known‐age individuals (N = 1,506, prenatal to 23.94 years). Dental age was estimated using charts of Schour and Massler, Ubelaker, and The London Atlas. Dental and chronological ages were compared using a paired t‐test for the three methods. The absolute mean difference between dental and chronological age was calculated. Results show that all three methods under‐estimated age but the London Atlas performed better than Schour and Massler and Ubelaker in all measures. The mean difference for Schour and Massler and Ubelaker was ?0.76 and ?0.80 years (SD 1.27 year, N = 1,227) respectively and for the London Atlas was ?0.10 year (SD 0.97 year, N = 1,429). Further analysis by age category showed similar accuracy for all three methods for individuals younger than 1 year. For ages 1–18, the mean difference between dental and chronological ages was significant (P < 0.05) for Schour and Massler and Ubelaker and not significant (P > 0.05) for the London Atlas for most age categories. These findings show that the London Atlas performs better than Schour and Massler and Ubelaker and represents a substantial improvement in accuracy of dental age estimation from developing teeth. Am J Phys Anthropol 154:70–78, 2014. © 2014 Wiley Periodicals, Inc.     

Development of the hand and wrist bones in chimpanzees

Skeletal developmental of chimpanzees was studied cross-sectionally. By application of the TW2 method, we described the skeletal development of chimpanzees and compared their skeletal development with humans'. A development pattern of chimpanzees repeated accelerations and decelerations displaying “early-juvenile trough,” “pre-adolescent peak,” “mid-adolescent trough,” and “post-adolescent peak” in incremental curves. Sex differences in skeletal development are slower development in males during infant and early juvenile phases, and greater increment around the adolescent phase in males. Females are fully mature at younger ages than males, e.g. about one and a half years. In comparison with chimpanzees, humans have such characteristics as a longer slower period of juvenile development and a shorter spurt-like adolescent fast period which ends with full maturity.     

An evaluation of the miles method of ageing using the Tepe Hissar dental sample.

The Miles system of ageing, based upon analysis of the rate of molar wear, was evaluated using the available dental sample from Tepe Hissar, Iran. The independently estimated ages for the mandibles and maxillae of the same individuals were found to be highly correlated (r = 0.87, p less than 0.001). Ages of a subsample of the dentitions were compared with skeletal ages for the same individuals estimated from pubic symphyseal faces and found to be significantly correlated (r = 0.82, p less than 0.005) with no significant differences in the mean ages. Although a complete evaluation of the Miles method would require its testing on a controlled population, the available dental sample from Tepe Hissar provided evidence of the reliability and validity of the Miles method of ageing archeological populations on the basis of dental wear. Due to selective retention of burial remains, the available skeletal sample from Tepe Hissar I-III is not representative of the human populations of the site and can not be used to generate meaningful demographic statistics.     

Dental Indicators Suggest Health Improvement Associated with Increased Food Diversity in Modern Age Spain

The aim of this study is to investigate the health impact of the introduction of new food resources into the Spanish diet in the early Modern Age. For this purpose we compare the pathological conditions of teeth from skeletal remains dating from the Middle (Mediaeval) Ages (11th–15th century) with others of the Modern era (16th–18th century), sampled from historic cemeteries of north Iberia (Spain). Dental alterations like abscesses, periodontitis, calculus and dental wear, indicate oral hygiene and habits, and linear enamel hypoplasia (LEH) is considered as an indicator of nutritional status. Significant decreases of LEH occurred in Modern Age individuals in comparison to Mediaeval values, suggesting the positive influence of increased diversity of nutritional resources mainly due to intercontinental (America–Europe) trade.     

Human population differentiation in the peri-Baltic Mesolithic: the odontometrics of Oleneostrovskii mogilnik (Karelia)

Odontometric data are reported for Oleneostrovskii mogilnik, a Mesolithic cemetery in the Karelian USSR. Containing the skeletal remains of 148 individuals and dated to 7500b.p., it is the largest and oldest of the known peri-Baltic Mesolithic cemeteries. The dental data from this site are compared to those from Skateholm, where dental dimensions closely approximate the mean tooth sizes for all late Mesolithic European material. Olenii ostrov possesses a significantly smaller dentition, despite antedating the Skateholm sample by 1500 years. Geographic, archaeological, linguistic and ancillary dental data are discussed which argue strongly for the presence in Mesolithic northern Europe of at least two quasi-isolated human mating networks. One of these, documented by Olenii ostrov, may also represent the earliest evidence for the establishment in the taiga zone of populations whose descendants are the modern Saami (=”Lapps”).     

The diet of pygmy sperm whales, Kogia breviceps, stranded in New Zealand: implications for conservation

The stomach contents of 27 pygmy sperm whales, Kogia breviceps, stranded on New Zealand beaches between 1991 and 2003 are reported. These individuals comprise 16 males, 10 females, and one for which no sex information is available. The diet was found to include fish and crustaceans, but is comprised primarily of cephalopods, with 0–526 lower beaks, representing an estimated maximum of c. 60 kg of cephalopod prey consumed by any one whale. Cephalopod prey is attributed to 23 species from 13 families, and is dominated by juvenile individuals of the families Histioteuthididae and Cranchiidae (adults of which usually occur at depths exceeding 400 m). Perceived threats to this whale, particularly those affecting distribution and abundance of prey species, are also discussed. These are the first data reporting the diet of this whale species in New Zealand waters. A comparison of the diet of K. breviceps is made with that of the sperm whale, Physeter macrocephalus from New Zealand waters, and with the diet of Kogia known elsewhere.     

Mate Sampling and Assessment Procedures in Female Pied Flycatchers (Ficedula hypoleuca)

Models of mate sampling strategies predict that choosiness should decrease throughout the breeding season due to increasing costs of delaying mating. Therefore, individuals who start searching mates relatively late, should spend less time on sampling, and sample fewer candidates compared to early individuals. We observed mate searching behavior of female pied flycatchers (Ficedula hypoleuca) by radio-tracking in study areas with 6–12 unpaired males. Contrary to the prediction, the observed numbers of males sampled by the searching females increased with time, i.e. late arriving females visited more males than early arrivers. However, this seems to be due to more active sampling of males in short time by late-arriving females. The observed sampling pattern suggests some kind of comparison tactic, which seems, however, to be very variable among individual females. Mate-assessing females were characterized by a remarkably cryptic behavior, which may be 1) a way of gaining honest information about the male mating status or male/territory quality, or 2) a way of avoiding courtship costs.     

Oral health and the postcontact adaptive transition: A contextual reconstruction of diet in Mórrope,Peru

This work explores the effects of European contact on Andean foodways in the Lambayeque Valley Complex, north coast Peru. We test the hypothesis that Spanish colonization negatively impacted indigenous diet. Diachronic relationships of oral health were examined from the dentitions of 203 late‐pre‐Hispanic and 175 colonial‐period Mochica individuals from Mórrope, Lambayeque, to include observations of dental caries, antemortem tooth loss, alveolar inflammation, dental calculus, periodontitis, and dental wear. G‐tests and odds ratio analyses across six age classes indicate a range of statistically significant postcontact increases in dental caries, antemortem tooth loss, and dental calculus prevalence. These findings are associated with ethnohistoric contexts that point to colonial‐era economic reorganization which restricted access to multiple traditional food sources. We infer that oral health changes reflect creative Mochica cultural adjustments to dietary shortfalls through the consumption of a greater proportion of dietary carbohydrates. Simultaneously, independent skeletal indicators of biological stress suggest that these adjustments bore a cost in increased nutritional stress. Oral health appears to have been systematically worse among colonial women. We rule out an underlying biological cause (female fertility variation) and suggest that the establishment of European gender ideologies and divisions of labor possibly exposed colonial Mochica women to a more cariogenic diet. Overall, dietary change in Mórrope appears shaped by local responses to a convergence of colonial Spanish economic agendas, landscape transformation, and social changes during the postcontact transition in northern Peru. These findings also further the understandings of dietary and biocultural histories of the Western Hemisphere. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Skeletal indicators of subsistence patterns and activity régime in the Mesolithic sample from Grotta dell’Uzzo (Trapani,Sicily): a case study

The skeletal sample from Grotta dell’Uzzo, Sicily (2 adult females and 5 adult males) was compared to a number of more representative population samples from Western Europe and the Mediterranean Basin. The majority of these were from Italian pre- and protohistoric sites. The research protocol analyzed skeletal indicators of labour activity and sexual division of labour (body size and proportions, sexual dimorphism, limb lateralization, bone robustness, the development of muscular attachments, accessory articular facets, signs of muscular hyperfunction). Sexual dimorphism and limb lateralization showed some regular patterns of possible general significance in all the samples examined here. A general pattern of gracilization and de-specialization of physical activity is observed in the Mesolithic as compared to the Upper Palaeolithic samples. The main features of the Mesolithic samples are: a reduction of body size and bone robustness, a lower degree of sexual dimorphism and limb bone asymmetry, a reduction of the mechanical stress on the lower limbs indicated by less pronounced muscular attachments and reduced talar flattening. This trend is reversed towards the Neolithic period. The main features of these variations are discussed in relation to economic and environmental changes. The Uzzo sample fits well into the general picture of the Western European Mesolithic, although showing some intermediate features between the Mesolithic and the Neolithic samples. This paper is dedicated to the memory of the late Roland Menk, who made significant contribution to our understanding of the Mesolithic transition.