Dental indicators of health and stress in early Egyptian and Nubian agriculturalists: a difficult transition and gradual recovery

Although agriculture is now the globally predominant mode of food production, studies of the skeletal remains of early agriculturalists have indicated high levels of physiological stress and poor health relative to hunter-gatherers in similar environments. Previous studies identifying this trend in different regions prompt further research of the causes and effects of subsistence transitions in human societies. Here, 242 dentitions from five ancient Egyptian and Nubian populations are examined: 38 individuals from Jebel Sahaba (Upper Paleolithic), 56 from Badari (Predynastic), 54 from Naqada (Predynastic), 47 from Tarkhan (Dynastic), and 47 from Kerma (Dynastic). These populations span the early period of agricultural intensification along the Nile valley. Skeletal remains were scored for the presence of linear enamel hypoplasia (LEH) of the dentition, an established indicator of physiological stress and growth interruption. The prevalence of LEH was highest in the "proto-agricultural" (pastoralist) Badari population, with a gradual decline throughout the late Predynastic and early Dynastic periods of state formation. This suggests that the period surrounding the emergence of early agriculture in the Nile valley was associated with high stress and poor health, but that the health of agriculturalists improved substantially with the increasing urbanization and trade that accompanied the formation of the Egyptian state. This evidence for poor health among proto- and early agriculturalists in the Nile valley supports theories that agricultural intensification occurred as a response to ecological or demographic pressure rather than simply as an innovation over an existing stable subsistence strategy.     

From the mouths of babes: Dental caries in infants and children and the intensification of agriculture in mainland Southeast Asia

Many bioarchaeological studies have established a link between increased dental caries prevalence and the intensification of agriculture. However, research in Southeast Asia challenges the global application of this theory. Although often overlooked, dental health of infants and children can provide a sensitive source of information concerning health and subsistence change. This article investigates the prevalence and location of caries in the dentition of infants and children (less than 15 years of age) from eight prehistoric mainland Southeast Asian sites collectively spanning the Neolithic to late Iron Age, during which time rice agriculture became an increasingly important subsistence mode. Caries prevalence varied among the sites but there was no correlation with chronological change. The absence of evidence of a decline in dental health over time can be attributed to the relative noncariogenicity of rice and retention of broad‐spectrum subsistence strategies. No differences in caries type indicating differences in dental health were found between the sites, apart from the Iron Age site of Muang Sema. There was a higher prevalence of caries in the deciduous dentition than the permanent dentition, likely due to a cariogenic weaning diet and the higher sensitivity of deciduous teeth to decay. The level of caries in the permanent dentition suggests an increased reliance on less cariogenic foods during childhood, including rice. The absence of a temporal decline in dental health of infants and children strengthens the argument that the relationship between caries and agricultural intensification in Southeast Asia was more complex than the general model suggests. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.     

Patterns of systemic stress during the agricultural transition in prehistoric Japan

This study documents and interprets systemic stress during the agricultural transition in prehistoric Japan using linear enamel hypoplasia (LEH) defects and cribra orbitalia (CO) lesions. Middle to Final Jomon cultures (5000–2300 BP) from Honshu Island represent the foraging samples, while Yayoi cultures (2500–1700 BP) represent the early agricultural samples. Jomon foragers from eastern Japan had broad‐based, intensive economies. Jomon foragers from western Japan had a greater focus on seasonally available, nutritionally poor resources, while Yayoi people were descendents of migrants from the East Asian continent and introduced wet rice economies to Japan. This study tests the hypotheses that wet rice economies will be associated with a lower prevalence of teeth/individuals affected by LEH defects in western Japan, while few differences in the prevalence of teeth/individuals with LEH defects will be observed between eastern Jomon people and Yayoi farmers. It is further predicted that similar CO prevalence will be observed between Jomon and Yayoi people given environmental similarities. Significantly greater frequencies of teeth affected by LEH defects are observed among western Jomon compared to Yayoi people. The prevalence of teeth with LEH defects is slightly elevated among eastern Jomon foragers compared to Yayoi agriculturalists. Significant differences in CO prevalence are not observed. Systemic stress prevalence in western Japan likely declined following wet‐rice agriculture because this crop provided a predictable, renewable resource base. Systemic stress prevalence was similar between eastern Jomon and Yayoi people because both groups practiced intensive subsistence strategies. Similar CO prevalence reflects infectious diseases associated with living conditions. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Ecological stress and linear enamel hypoplasia in Cebus

Although it is assumed that monkeys in some environments experience more nutritional or physiological stress than others, little research has been conducted on this topic. This study examines the relationship between linear enamel hypoplasia (LEH) frequency, a physiological indicator of stress, and environmental stressors. To test this relationship, LEH frequencies were calculated for 144 Cebus from 54 locations in Brazil. Habitat, temperature range, and annual rainfall were compared between individuals with and without LEH. The LEH frequency for Cebus from semideciduous forests was significantly higher than that for monkeys from coastal areas, the rainforest, and the savanna (χ² = 9.97, df = 1; P = 0.0016). A significantly higher LEH frequency was also found for monkeys living in environments with the mean annual temperature between 15 and 18°C than for those in environments greater than 18°C (χ² = 7.74, df = 1, P = 0.0054). However, no significant difference was found between LEH frequency and annual rainfall (t = 1.22, P = 0.23) or the average difference in rainfall between the driest and wettest months (t = 0.77, P = 0.44). These results indicate that levels of physiological stress can differ among environments and that habitat and temperature, but not precipitation, may be driving the difference in stress levels among environments. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Brief communication: linear enamel hypoplasia and the shift from irregular to regular provisioning in Cayo Santiago rhesus monkeys (Macaca mulatta)

This study investigates changes in the prevalence of linear enamel hypoplasia (LEH) before and after the shift from irregular to regular provisioning in the Cayo Santiago rhesus monkey population. Prior to 1956, monkeys on this island colony did not receive consistent provisions, and were reported to be in poor health (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). A regular provisioning program, instituted in August 1956, resulted in the improved health of individuals and the growth of the population (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). LEH, a developmental defect of enamel, is a sensitive indicator of systemic physiological stress (Goodman and Rose [1990] Yrbk. Phys. Anthropol. 33:59-110). It was therefore hypothesized that the prevalence of LEH would be higher in monkeys who were irregularly provisioned than in monkeys who experienced regular provisioning. To test this hypothesis, teeth were examined for LEH in a sample of 181 female rhesus monkeys. The results support the hypothesis: the mean number of defects was statistically significantly higher in the preprovisioned group than it was in the postprovisioned one. When LEH prevalence was assessed using only defects occurring on antimeric pairs, the preprovisioned group again had a higher prevalence than the postprovisioned one, although the difference was not statistically significant, most likely because of the reduced sample size. The results of this study indicate that changes in LEH prevalence, at least in this population of rhesus monkeys, are associated with changes in nutritional status.     

禄丰古猿带状牙釉质发育不全的再观察

牙釉质发育不全是反映牙齿发育过程中遭遇生理性刺激的有效指标。本文对来自云南禄丰石灰坝的禄丰古猿(Lufengpithecus lufengensis)261枚单颗恒齿进行观察分析,发现223枚牙齿普遍罹患带状牙釉质发育不全(LEH),比例为85.4%,高于其它已报道过的中新世古猿、化石人科成员及现生大猿。另一方面,用扫描电镜和数码显微镜着重分析了12枚犬齿,均有多条LEH,且雄性犬齿的LEH条数多于雌性;相邻LEH间的釉面横纹数在14-25条之间。结合禄丰古猿釉面横纹的生长周期(9天),估算相邻LEH之间的时间间隔为4.8-6.6月,季节性营养不良可能是禄丰古猿釉质发育不全的主要原因。     

Linear enamel hypoplasia in gibbons (Hylobates lar carpenteri)

This study describes the expression of linear enamel hypoplasia (LEH), a sensitive dental indicator of physiological stress, in Thailand gibbons (Hylobates lar carpenteri). Previous studies of enamel hypoplasia in hominoids have focused on great apes, with little attention given to the expression of this stress indicator in gibbons. In that gibbons differ from both monkeys and great apes in numerous life history features, LEH expression in gibbons might be expected to show significant differences from both. In this study, 92 gibbon specimens from two sites in Thailand were compared with several samples of monkeys and great apes in their expression of LEH. The intertooth distribution of LEH in gibbons was compared to that of chimpanzees and rhesus monkeys. Gibbon populations from both sites exhibit LEH frequencies intermediate between those of the monkey samples, in which LEH prevalence is usually low, and those of the great ape samples, in which LEH prevalence is high. Gibbons differ significantly from monkeys, but not great apes, in the number of individuals whose teeth record multiple stress events. Multiple episodes of stress are rarely recorded in the teeth of monkeys, while multiple stress events occur with higher frequency in gibbons and great apes. Taxonomic variation in the duration of crown formation, the prominence and spacing of perikymata on dental crowns, life history features, and/or experience of physiological stress may explain these patterns. The intertooth distribution of LEH in gibbons is, for different reasons, unlike that of either chimpanzees or rhesus monkeys. The mandibular canines of gibbons have significantly more LEH than any of their other teeth. Aspects of crown morphology, perikymata prominence/spacing, enamel thickness, and crown formation spans are potential causes of taxonomic variation in the intertooth distribution of LEH.     

Enamel hypoplasias and physiological stress in the Sima de los Huesos Middle Pleistocene hominins

This study presents an analysis of linear enamel hypoplasias (LEH) and plane-form defects (PFD) in the hominine dental sample from the Sima de los Huesos (SH) Middle Pleistocene site in Atapuerca (Spain). The SH sample comprises 475 teeth, 467 permanent and 8 deciduous, belonging to a minimum of 28 individuals. The method for recording PFD and LEH is discussed, as well as the definition of LEH. The prevalence of LEH and PFD in SH permanent dentition (unilateral total count) is 4.6% (13/280). Only one deciduous tooth (lower dc) showed an enamel disruption. Prevalence by individual ranges from 18.7-30%. The most likely explanation for the relatively low LEH and PFD prevalence in the SH sample suggests that the SH population exhibited a low level of developmental stress. The age at occurrence of LEH and PFD was determined by counting the number of perikymata between each lesion and the cervix of the tooth. Assuming a periodicity of nine days for the incremental lines, the majority of LEH in the SH sample occurred during the third year of life and may be related to the metabolic stress associated with weaning.     

Stature and robusticity during the agricultural transition: Evidence from the bioarchaeological record

The population explosion that followed the Neolithic revolution was initially explained by improved health experiences for agriculturalists. However, empirical studies of societies shifting subsistence from foraging to primary food production have found evidence for deteriorating health from an increase in infectious and dental disease and a rise in nutritional deficiencies. In Paleopathology at the Origins of Agriculture (Cohen and Armelagos, 1984), this trend towards declining health was observed for 19 of 21 societies undergoing the agricultural transformation. The counterintuitive increase in nutritional diseases resulted from seasonal hunger, reliance on single crops deficient in essential nutrients, crop blights, social inequalities, and trade. In this study, we examined the evidence of stature reduction in studies since 1984 to evaluate if the trend towards decreased health after agricultural transitions remains. The trend towards a decrease in adult height and a general reduction of overall health during times of subsistence change remains valid, with the majority of studies finding stature to decline as the reliance on agriculture increased. The impact of agriculture, accompanied by increasing population density and a rise in infectious disease, was observed to decrease stature in populations from across the entire globe and regardless of the temporal period during which agriculture was adopted, including Europe, Africa, the Middle East, Asia, South America, and North America.     

邓州八里岗仰韶时期居民的体质变迁

河南邓州八里岗遗址出土的仰韶早期与中晚期人骨体质状况的对比分析表明,八里岗仰韶文化在其延续千年的时间内,居民体质状况从早期到中晚期出现一系列变化。具体表现为女性身高的减少、男女性下肢功能活跃度的降低以及四肢长骨纤细化的倾向。古病理指征则展现出龋病发生的显著增加、头骨钝伤的减少以及女性胫骨骨膜反应增多等表现。这些体质状况的变迁,与八里岗仰韶文化发展过程中日趋定居的生活方式、农业经济渐趋成熟以及食物加工技术的进步有关。与此同时,女性的社会地位开始呈现下降的趋势。八里岗仰韶居民的体质特征改变与这一阶段仰韶社会的发展状况及古代人类的行为模式存在密切联系。     

Yugoslav Mesolithic dental reduction

Yugoslav Mesolithic dentition exhibits maximum mesiodistal reduction compared with contemporary European and North African groups. This reduction is not explained entirely by attrition, and may be seen as a continuation of the European Upper Paleolithic trend. Buccolingual dimension does not reduce as much. In fact, this dimension in premolars and molars is larger than in other groups. This observation also occurs in Natufians, who were grain collectors, hunters, and gatherers. The Yugoslav Mesolithic group was collecting and domesticating Cerelia as well as fishing and hunting. Linear enamel hypoplasias (LEH) indicate childhood stress through the fifth year, which corroborates previously reported incidence of rickets in this group. The central maxillary incisors and canines manifest higher degrees of LEH, but the appearance on the second molars suggest a more severe physiological disruption. Sex differences in distributions of alveolar resorption and calculus suggest differences in diet or nutritional stress. Previous reports indicate that females had higher incidence of osteomalacia. If so, female nutritional stress may explain the extreme mesiodistal reduction and minimal sexual dimorphism in this group.     

Health status among prehistoric Eskimos from Point Hope,Alaska

Using the protocol outlined in The Backbone of History: Health and Nutrition in the Western Hemisphere (BBH) (Steckel and Rose. 2002a. The backbone of history: health and nutrition in the Western Hemisphere. Cambridge: Cambridge University Press), this project compares the Mark I Health Index (MIHI) scores of the Ipiutak (n = 76; 100BCE–500CE) and Tigara (n = 298; 1200–1700CE), two samples of North American Arctic Eskimos excavated from Point Hope, Alaska. Macroscopic examination of skeletal remains for evidence of anemia, linear enamel hypoplasias (LEH), infection, trauma, dental health, and degenerative joint disease (DJD) was conducted to assess differences in health status resulting from a major economic shift at Point Hope. These data demonstrate that despite differences in settlement pattern, economic system, and dietary composition, the MIHI scores for the Ipiutak (82.1) and Tigara (84.6) are essentially equal. However, their component scores differ considerably. The Ipiutak component scores are suggestive of increased prevalence of chronic metabolic and biomechanical stresses, represented by high prevalence of nonspecific infection and high frequencies of DJD in the hip/knee, thoracic vertebrae, and wrists. The Tigara experienced more acute stress, evidenced by higher prevalence of LEH and trauma. Comparison of overall health index scores with those published in BBH shows the MIHI score for the Ipiutak and Tigara falling just above the average for sites in the Western Hemisphere, adding support to the argument that the human capacity for cultural amelioration of environmental hardships is quite significant. Am J Phys Anthropol, 2011. © 2011 Wiley‐Liss, Inc.     

Plasticity and constraint in response to early‐life stressors among late/final jomon period foragers from Japan: Evidence for life history trade‐offs from incremental microstructures of enamel

This study evaluates two hypotheses that address how Late/Final Jomon period people responded to early‐life stress using linear enamel hypoplasia (LEH) and incremental microstructures of enamel. The first hypothesis predicts that Jomon people who experienced early‐life stressors had greater physiological competence in responding to future stress events (predictive adaptive response). The second hypothesis predicts that Jomon people traded‐off in future growth and maintenance when early investment in growth and survival was required (plasticity/constraint). High resolution tooth impressions were collected from intact, anterior teeth and studied under an engineer's measuring microscope. LEH were identified based on accentuated perikymata and depressions in the enamel surface profile. Age of formation for each LEH was estimated by summing counts of perikymata and constants associated with crown initiation and cuspal enamel formation times. The relationship between age‐at‐first‐defect formation, number of LEH, periodicity between LEH, and mortality was evaluated using multiple regression and hazards analysis. A significant, positive relationship was found between age‐at‐death relative to age‐at‐first‐defect formation and a significant, negative relationship was found between number of LEH relative to age‐at‐first‐defect formation. Individuals with earlier forming defects were at a significantly greater risk of forming defects at later stages of development and dying at younger ages. These results suggest that Late/Final Jomon period foragers responded to early‐life stressors in a manner consistent with the plasticity/constraint hypothesis of human life history. Late/Final Jomon period individuals were able to survive early‐life stressors, but this investment weakened responses to future stress events and exacerbated mortality schedules. Am J Phys Anthropol 155:537–545, 2014. © 2014 Wiley Periodicals, Inc.     

The neolithic demographic transition and oral health: The Southeast Asian experience

The purpose of this article is to present new oral health data from Neolithic An Son, southern Vietnam, in the context of (1) a reassessment of published data on other Neolithic, Bronze, and Iron Age Southeast Asian dental series, and (2) predictions of the Neolithic Demographic Transition (NDT). To this end, frequencies for three oral conditions (caries, antemortem tooth loss, and alveolar lesions) were investigated for seven Southeast Asian adult dental series from Thailand and Vietnam with respect to time period, age‐at‐death and sex. A clear pattern of elevated rates for oral disease in the Neolithic followed by a marked improvement in oral health during the Bronze and Iron Ages was observed. Moreover, rates of caries and antemortem tooth loss for females were almost without exception higher than that for males in all samples. The consensus view among Southeast Asian bioarchaeologists that oral health did not decline with the adoption/intensification of agriculture in Southeast Asia, can no longer be supported. In light of evidence for (1) the low cariogenicity of rice; (2) the physiological predisposition of females (particularly when pregnant) to poorer oral health; and (3) health predictions of the NDT model with respect to elevated levels of fertility, the most plausible chief explanation for the observed patterns in oral health in Southeast Asia is increased levels of fertility during the Neolithic, followed by a decline in fertility during the subsequent Bronze and Iron Ages. Am J Phys Anthropol 152:197–208, 2013. © 2013 Wiley Periodicals, Inc.     

禄丰古猿牙齿釉质发育不全的观察研究

对出自禄丰石灰坝的26个禄丰古猿下颌齿列的246枚恒齿进行了观察研究,发现禄丰古猿具有普遍的带状釉质发育不全（LEH）现象,个体LEH比例为100%,恒齿LEH比例为85%。乳齿几乎没有LEH现象,第一恒臼齿的LEH比例也很低仅57%。根据牙齿萌出顺序及现代大猿的牙齿发育年龄特征,作者推断2—3岁之前的幼儿古猿很少出现釉质发育不全现象,这可能与母体的营养关照有关。禄丰古猿的LEH的发生频率具有明显的季节性,结合中新世晚期气候变化特征、古猿的生态环境、生活习性及食性特征分析,作者推测：季节性营养不良可能是造成禄丰古猿釉质发育不全的主要原因。     

Contact in the Andes: bioarchaeology of systemic stress in colonial Mórrope, Peru

The biocultural interchange between the Eastern and Western Hemispheres beginning in the late fifteenth century initiated an unprecedented adaptive transition for Native Americans. This article presents findings from the initial population biological study of contact in the Central Andes of Peru using human skeletal remains. We test the hypothesis that as a consequence of Spanish colonization, the indigenous Mochica population of Mórrope on the north coast of Peru experienced elevated systemic biological stress. Using multivariate statistical methods, we examine childhood stress reflected in the prevalence of linear enamel hypoplasias and porotic hyperostosis, femoral growth velocity, and terminal adult stature. Nonspecific periosteal infection prevalence and D(30+)/D(5+) ratio estimations of female fertility characterized adult systemic stress. Compared to the late pre-Hispanic population, statistically significant patterns of increased porotic hyperostosis and periosteal inflammation, subadult growth faltering, and depressed female fertility indicate elevated postcontact stress among both children and adults in Mórrope. Terminal adult stature was unchanged. A significant decrease in linear enamel hypoplasia prevalence may not indicate improved health, but reflect effects of high-mortality epidemic disease. Various lines of physiological, archaeological, and ethnohistoric evidence point to specific socioeconomic and microenvironmental factors that shaped these outcomes, but the effects of postcontact population aggregation in this colonial town likely played a fundamental role in increased morbidity. These results inform a model of postcontact coastal Andean health outcomes on local and regional scales and contribute to expanding understandings of the diversity of indigenous biological variation in the postcontact Western Hemisphere.     

Linear enamel hypoplasia as an indicator of physiological stress in great apes: reviewing the evidence in light of enamel growth variation

Physiological stress, such as malnutrition or illness, can disrupt normal enamel growth, resulting in linear enamel hypoplasias (LEHs). Although ecological factors may contribute to LEH expression, other factors, such as surface abrasion and enamel growth variables, are also likely to be involved. Attention to these other factors is necessary before we can begin to understand what LEH might signify in terms of ecological sources of physiological stress in non-human primates. This study focuses on assessing the contribution of these other factors to variation in LEH expression within and across great ape taxa. Here, we present LEH data from unabraded crown regions in samples of seven great ape species. We analyze these data with respect to lateral enamel formation time and the angles that striae of Retzius make with the enamel surface, as these variables are expected to affect variation in LEH expression. We find that although the duration of enamel formation is associated with sex differences in LEH expression, it is not clearly related to taxonomic variation in LEH expression, and does not explain the low frequency of LEH in mountain gorillas found in this and a previous study. Our data on striae of Retzius angles suggest that these influence LEH expression along the tooth crown and may contribute to the consistently high frequencies of LEH seen in Pongo in this and previous studies. We suggest that future work aimed at understanding species variation in these angles is crucial to evaluating taxonomic patterns of LEH expression in great apes.     

Missing defects? A comparison of microscopic and macroscopic approaches to identifying linear enamel hypoplasia

Linear enamel hypoplasia (LEH), the presence of linear defects of dental enamel formed during periods of growth disruption, is frequently analyzed in physical anthropology as evidence for childhood health in the past. However, a wide variety of methods for identifying and interpreting these defects in archaeological remains exists, preventing easy cross‐comparison of results from disparate studies. This article compares a standard approach to identifying LEH using the naked eye to the evidence of growth disruption observed microscopically from the enamel surface. This comparison demonstrates that what is interpreted as evidence of growth disruption microscopically is not uniformly identified with the naked eye, and provides a reference for the level of consistency between the number and timing of defects identified using microscopic versus macroscopic approaches. This is done for different tooth types using a large sample of unworn permanent teeth drawn from several post‐medieval London burial assemblages. The resulting schematic diagrams showing where macroscopic methods achieve more or less similar results to microscopic methods are presented here and clearly demonstrate that “naked‐eye” methods of identifying growth disruptions do not identify LEH as often as microscopic methods in areas where perikymata are more densely packed. Am J Phys Anthropol 153:463–472, 2014. © 2013 Wiley Periodicals, Inc.     

Novel genetic sex markers reveal high frequency of sex reversal in wild populations of the agile frog (Rana dalmatina) associated with anthropogenic land use

Populations of ectothermic vertebrates are vulnerable to environmental pollution and climate change because certain chemicals and extreme temperatures can cause sex reversal during early ontogeny (i.e. genetically female individuals develop male phenotype or vice versa), which may distort population sex ratios. However, we have troublingly little information on sex reversals in natural populations, due to unavailability of genetic sex markers. Here, we developed a genetic sexing method based on sex‐linked single nucleotide polymorphism loci to study the prevalence and fitness consequences of sex reversal in agile frogs (Rana dalmatina). Out of 125 juveniles raised in laboratory without exposure to sex‐reversing stimuli, 6 showed male phenotype but female genotype according to our markers. These individuals exhibited several signs of poor physiological condition, suggesting stress‐induced sex reversal and inferior fitness prospects. Among 162 adults from 11 wild populations in North‐Central Hungary, 20% of phenotypic males had female genotype according to our markers. These individuals occurred more frequently in areas of anthropogenic land use; this association was attributable to agriculture and less strongly to urban land use. Female‐to‐male sex‐reversed adults had similar body mass as normal males. We recorded no events of male‐to‐female sex reversal either in the laboratory or in the wild. These results support recent suspicions that sex reversal is widespread in nature, and suggest that human‐induced environmental changes may contribute to its pervasiveness. Furthermore, our findings indicate that sex reversal is associated with stress and poor health in early life, but sex‐reversed individuals surviving to adulthood may participate in breeding.