Temporal variation and interaction between nutritional and ...

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 137:469–478 (2008)

Temporal Variation and Interaction Between Nutritional and Developmental Instability in Prehistoric Japanese Populations Kara C. Hoover1* and Hirofumi Matsumura2 1 2

Department of Anthropology, University of Alaska Fairbanks, Fairbanks, AK 99775-7720 Department of Anatomy, Sapporo Medical University, S1 W17 Chuoku, Sapporo, 060-8556 Japan KEY WORDS developmental and nutritional stress; enamel hypoplasia; fluctuating asymmetry; Jomon Japan; stress markers

ABSTRACT We examined nutritional and developmental instability in prehistoric Japan, using data from 49 individuals across 13 archaeological sites. Hypoplasia incidence was used as a measure of nutritional stress, and fluctuating asymmetry (of upper facial breath, orbital breadth, and orbital height) as an indirect assessment of developmental instability. Abundant resources due to a stable climate during the Middle Jomon (5,000– 3,000 BP) encouraged population growth, which led to regional cultural homogeneity and complexity. A population crash on Honshu in the Late/Final Jomon (roughly 4,000–2,000 BP) led to regionally divergent subsistence economies and settlement patterns. We find that the nutritional stress was consistent between periods, but developmental instability (DI) decreased in the Late/ Final Jomon. While the DI values were not statistically significant, the higher values for Middle Jomon may

result from sedentism, social stratification, and differential access to resources. On Hokkaido, Jomon culture persisted until the Okhotsk period (1,000–600 BP), marked by the arrival of immigrants from Sakhalin. Nutritional stress was consistent between Middle and Late/Final Jomon, but DI increased in the Late/Final. Nutritional and developmental instability decreased from Late/Final to Okhotsk, suggesting a positive immigrant effect. We expected to find an association between stress markers due to the synergistic relationship between nutrition and pathology. The data support this hypothesis, but only one finding was statistically significant. While high critical values from small sample sizes place limits on the significance of our results, we find that the impact of environmental and cultural change to prehistoric Japanese populations was minimal. Am J Phys Anthropol 137:469–478, 2008. V 2008 Wiley-Liss, Inc.

The most common external disruption to organismal homeostasis is stress, either pathogenic or dietary (Selye, 1973). The immediate result is diminished health and reproductive status as the organism attempts to return to homeostasis. Individual responses to this developmental instability (DI) vary relative to innate resistance and strength of pathogen or severity of malnourishment. Culturally induced stresses, such as differential access to resources or exposure to disease, also contribute to poor health (Goodman and Armelagos, 1989). The metabolic cost of a severe or prolonged stress response during growth and development is high, often a cessation of normal physiological activity (Sapolsky, 1992). The result is permanent markers of developmental stress—shortened stature, poorly formed bones or dental enamel, and asymmetrical development of paired features. These stress markers allow anthropologists to determine the health status of past populations. During the preagricultural periods of Japan, diet and climate varied between periods and regions. The Middle Jomon period (5,000–3,000 BP) enjoyed relative climate stability that allowed a population explosion, social stability, cultural continuity across regions, instances of sedentism, and social complexity in some areas (Habu, 2004; Imamura, 1996). By the Late and Final periods, Jomon culture fractured into regionally divergent subsistence economies and settlement patterns. In particular, the northeastern areas of Honshu increasingly relied on marine resources (Akazawa, 1981, 1982a,b, 1986a,b,c,

1987). During the Late/Final Jomon periods in the inland sea/south central areas of Honshu, dietary subsistence consisted primarily of plant foods (Akazawa, 1981, 1982a,b, 1986a,b,c, 1987). Some archaeological evidence of marine resources exploited in the south indicates a varied diet (Imamura, 1996). Eventually, immigrants from mainland Asia brought with them wet-rice agricultural practices signaling the beginning of a new era, the Yayoi, at roughly 2,300 BP. Populations on Hokkaido experienced a more consistent adaptation throughout the Jomon. The arrival of an immigrant population from modern day Sakhalin marked the beginning of a new archaeological era, the Okhotsk (roughly 1,000–600 BP). These newcomers were not agriculturalists and the transition to farming did not

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WILEY-LISS, INC.

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Grant sponsor: National Science Foundation-Sponsored Japan Society for the Promotion of Science Short-Term Invitational Fellowship. *Correspondence to: Kara C. Hoover, Department of Anthropology, 310 Eielson Building, University of Alaska Fairbanks, Fairbanks, AK 99775-7720, USA. E-mail: [email protected] Received 1 May 2007; accepted 30 May 2008 DOI 10.1002/ajpa.20892 Published online 18 August 2008 in Wiley InterScience (www.interscience.wiley.com).

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occur on Hokkaido until Honshu populations pushed north. During the Okhotsk, archaeological evidence indicates heavy exploitation of maritime resources and adequate nutrition (Aikens and Higuchi, 1982). Major changes in culture, diet, and environment throughout the Jomon (and into the Okhotsk on Hokkaido) would likely upset nutritional and developmental stability during growth and development. In this paper, we test the hypothesis that nutritional stress (via enamel hypoplasia incidence) and developmental instability (via upper facial fluctuating asymmetry) vary between periods on both islands and that instability indicators will increase together. Specifically, we expect to find the lowest hypoplasia incidence and asymmetry values for the Middle Jomon with an increase in the Late and Final periods on both islands. On Hokkaido, we expect to find a decrease during the Okhotsk period.

Dental enamel hypoplasia Dental enamel hypoplasias (hereafter referred to as hypoplasias) result from either temporary or permanent cessation of ameloblast activity (Seow, 1991). The resulting shortened enamel rods create the appearance of lines, furrows, and/or pits on the labial surface of the tooth, incidences of which correlate to developmental age (Hillson, 1996). The etiology of hypoplasia can be genetic or stress-induced. Amelogenesis imperfecta is a genetic disorder that produces the defect in all teeth in the dental arcade (Hart et al., 2003). Sometimes, hypoplasias are symptoms of other inherited systemic disorders (Seow, 1991). The most common etiology is stress-based, the result of external environmental insult(s) during growth and development, such as malnutrition or disease (Goodman and Armelagos, 1985; Seow, 1991; Hillier and Craig, 1992). Malnutrition is a particular focus in the anthropological study of hypoplasias. Hypoplasias are an indirect measure of the childhood nutritional status of an individual (Goodman and Rose, 1991), mainly due to an association between peak hypoplasia incidence and weaning (Katzenberg et al., 1996; Wright, 1997; Wright and Schwarcz, 1998). The introduction of solid food containing pathogens, often bacteria, causes mild to severe diarrhea depending on the level of sanitation in infant food preparation and storage. The diarrhea that ensues impedes adequate absorption of nutrients from food. Research on Chinese famine survivors provides additional support for the nutritional stress etiology of hypoplasia (Zhou and Corruccini, 1998). Malnutrition and disease have a synergistic relationship in which disease weakens the body and prevents adequate absorption of nutrition through a variety of direct (e.g., vomiting and diarrhea) and indirect processes (parasitism). Alternatively, malnutrition weakens the individual, inhibiting an organism’s ability to resist pathogens. On the level of the population, sedentary living conditions and stratified social structures associated with many human societies compound the effects of biological weakness by respectively increasing pathogen exposure and creating differential access to food resources (Goodman and Armelagos, 1985, 1989; Goodman et al., 1988; Leatherman and Goodman, 1997). Hypoplasias with a stress-based etiology exhibit similar patterns across populations and species. The teeth most commonly affected are the anterior dentition, usually the central maxillary incisors and mandibular canAmerican Journal of Physical Anthropology

ines (Goodman and Armelagos, 1985; Hillier and Craig, 1992). Many researchers (e.g., Goodman et al., 1984; Goodman and Armelagos, 1985) attribute differential appearance of hypoplasia within and between tooth classes to tooth-specific resistance factors. The first or polar tooth of a class (e.g., first incisor) is developmentally more stable, but exhibits greater variability in hypoplasia expression. Goodman and Armelagos (1985) suggest that these strongly canalized polar teeth respond to systemic disturbances via variable enamel deposition rather than delayed growth and/or reduced crown size. Some researchers suggest that thickness or surface area of hypoplasia indicates severity (Hutchinson and Larsen, 1988; Ensor and Irish, 1995). Variations in manifestation are also attributable to differing rates of enamel deposition. For instance, a study on great apes (Guatelli-Steinberg and Lukacs, 1999) finds that male canine development takes more time than that of females. As a result, the authors suggest that the male canine is vulnerable to stress over a longer period.

Asymmetry Asymmetry is a deviation from symmetry, the proportional development of paired features. Some deviations from asymmetry are ‘‘normal,’’ such as the lungs and mammalian heart, but some are the result of disturbances during growth and development (Waddington, 1957; Van Valen, 1962). There are actually three types of asymmetry contributing to between-sides differences of paired features: antisymmetry, directional asymmetry (DA), and fluctuating asymmetry (FA). Each type is only meaningful within the context of the population from which the data derive, e.g., they are population parameters (Clarke, 1998). Directional asymmetry. Directional asymmetry (DA) is the consistently greater or lesser development of a trait on one side of the plane of symmetry than the other (Van Valen, 1962). An example is the common occurrence in humans of a smaller left lung. In the anthropological literature, Corruccini et al. (1982) find an association between DA and other stress markers in remains of enslaved Africans, but most reported instances of DA across disciplines are attributed to genetics (e.g., asymmetry of the mammalian heart and lungs), side preferences (e.g., handedness), or remodeling following trauma (Van Valen, 1962). With the exception of dental enamel, the hard tissues of the body undergo natural remodeling through use, wear, and age—each of which may produce or increase DA, inflating overall between-sides variance. Traits heavily implicated in a specific activity are particularly vulnerable. For instance, while under a certain amount of genetic control, craniofacial symmetry is also shaped by strong mechanical loads from mastication (Scheuer and Black, 2000). Energetic dietary mastication remodels the condyles, causing the mandible to lengthen, and places appositional force on the maxillary suture, increasing breadth. Contemporary societies and foragers utilizing softer-textured foods experience a decrease in mechanical load force due to less energetic mastication. This softer diet may result in malocclusion, shorter mandibular arches with subsequent tooth row crowding, and narrower maxillary arches causing cross bite (Hinton and Carlson, 1979; Beecher and Corruccini, 1981; Hinton, 1981a,b, 1982; Ward et al., 1981; Corruccini and Beecher, 1982; Beecher et al., 1983; Corruccini et al., 1983,

NUTRITIONAL AND DEVELOPMENTAL INSTABILITY 1985a,b,c, 1986, 1990a,b; Harris and Corruccini, 1983; Corruccini, 1984a,b, 1987; Corruccini and Choudhury, 1986). DA is detectable if the mean deviates significantly from zero (resulting in a positive or negative distribution) or if the mean asymmetry value for the population deviates. If present, between-sides differences may be attributable to DA as much as FA. Mathematical corrections for DA tend to address data distribution issues but do not eliminate the underlying genetic variance (Palmer, 1994). For DI studies, both a careful selection of traits and statistical tests for DA presence are necessary. Antisymmetry. Antisymmetry is a nondirectional deviation from perfect symmetry around a mean of zero. Graphically, the probability distribution of antisymmetry is either platykurtotic (having a low peak) or bimodal (having two distinct peaks) (see Palmer and Strobeck, 2003). Antisymmetry, like DA, often has an underlying genetic component. If weakly present, a subtle antisymmetry may be difficult to detect. If present to a significant degree, antisymmetry is detectable through a careful analysis of data distributions, skew, and kurtosis statistics (Van Valen, 1962; Palmer, 1994). Unlike attempts to correct for or partition contributions of DA, there are no compensatory methods of proceeding with FA analysis if antisymmetry is present. Fluctuating asymmetry. Fluctuating asymmetry (FA), like antisymmetry, is a nondirectional deviation from perfect symmetry with an equal mean development on both sides and a mean of zero. Graphically, however, FA has a normal probability distribution, which has a more rounded peak (see Palmer and Strobeck, 2003). FA is an indirect marker of decreased developmental stability. Disruptions to homeostasis during growth and development range from external stresses such as temperature to internal stresses such as pathology (Van Valen, 1962; Waddington, 1957). The impact of cultural factors, such as limited access to resources, creates poor health conditions during growth and development leading to increased FA (Bailit et al., 1970; Siegel and Smookler, 1973; Siegel and Doyle, 1975a,b; Potter and Nance, 1976; Doyle and Johnston, 1977; Perzigian, 1977; Sciulli et al., 1979; Sofaer, 1979; Barden, 1980; Harris and Nweeia, 1980; Rose and Pasley, 1980; Townsend and Brown, 1980; Gest et al., 1983; Noss et al., 1983; Boklage, 1987; Livshits and Kobylianski, 1989, 1991; Parsons, 1990; Hershkovitz et al., 1993; Kieser et al., 1997; Kieser and Groeneveld, 1998; Townsend and Farmer, 1998). While there is a heritable component to FA, Naugler and Ludman (1996) argue that this only increases susceptibility to, but does not necessarily predict the presence of FA. If DA and antisymmetry are not present to a significant degree, the remaining between-sides variance is attributable to FA. There are many indices summarizing trait asymmetry for a population. For a review of their pros and cons, see Palmer and Strobeck (2003). The main issue these various indices address is measurement error (ME). This is of particular concern to studies involving archaeological remains, which are subject to differential preservation within and between sites. Statistically rigorous treatments of asymmetry data factor the contribution of ME to between-sides variance (for a worked example using published data, see Palmer and Strobeck, 2003).

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Hypoplasia and FA Previous studies have indicated a weak relationship between increased odontometric FA and hypoplasia presence (Corruccini et al., 2005; Hoover et al., 2005). The results of a recent study (DeLeon, 2007) using threedimensional landmarks of paired craniofacial elements in an early and late phase of the Christian medieval Sudanese Nubians indicate a stress-based etiology for FA. Specifically, individuals from the Early Christian period characterized by poor health (e.g., reduced stature, hypoplasias, cribra orbitalia) have greater overall FA compared to a genetically related group from the Later Christian period. This finding suggests a relationship of some kind between increased FA and other stress markers. Are individuals with greater FA genetically less buffered and thus more prone to additional insult (beyond minor environmental stresses shared by a population, such as temperature)? Or, are individuals who experience a particular biological insult through an accident of culture (inadequate food supply, increased exposure to pathogen) less developmentally stable as a result? Which comes first, weak genetic buffering or a specific insult that reduces systemic stability? Like the synergistic relationship between malnutrition and pathology, the relationship between stress markers and FA is a classic chicken-egg conundrum. Given the large body of research supporting the use of FA to detect DI and hypoplasia to detect malnutrition, we test the hypothesis that subsistence and social changes from the Middle Jomon to the Late/Final and Okhotsk periods result in a differential distribution of hypoplasia frequency and variation in FA. Specifically, we hypothesize that there will be an increase in both measures from the Middle to Late and Final periods and a possible decrease in the Okhotsk. Additionally, we hypothesize that individuals with hypoplasias have greater overall FA.

MATERIALS Named for a distinctive form of cord-decorated pottery, the Jomon period of Japan began in the Late Pleistocene, around 16,500 BP, and ended on the mainland of Honshu with the arrival of agriculture, roughly 2,000 BP. Geological and paleoecological evidence indicate the Jomon experienced climate changes that alternately exposed and covered large amounts of coastline. Archaeological evidence suggests that cultural changes in subsistence, settlement patterns, and social structure coincide with environmental changes (Habu, 2004; Imamura, 1996). The Okhotsk period, marked by the arrival of immigrants from Sakhalin, signals the end of the Jomon on Hokkaido at roughly 1,000 BP, 1,300 years after the end of the Jomon on Honshu. To test for temporal changes in health status, as measured by FA and hypoplasia presence, we used skeletal materials from 13 archaeological sites, dating to the Middle Jomon, Late/Final Jomon, and Okhotsk periods (Table 1). We have a large body of upper facial asymmetry data but, due to the stress interaction hypothesis, we included only individuals for which both hypoplasia and asymmetry data were available. Thus, our final sample consisted of 49 individuals from 13 Japanese prehistoric archaeological sites dating to Middle Jomon, Late/Final Jomon, or Okhotsk. In this final sample, we were not able to collect data for all three variables on each indiAmerican Journal of Physical Anthropology

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K.C. HOOVER AND H. MATSUMURA TABLE 1. Site data for the study

Lab

Period

SMC SMC NSM KUM Middle total

Middle Middle Middle Middle

SMC SMC SMC Hokkaido Late/Final total

Jomon Jomon Jomon Jomon

Site

Province

Location

n

Kotan-Onsen Kitakogane Ebishima Ohta

Oshima Iburi Iwate Hiroshima

SW Hokkaido SW Hokkaido NE Pacific coast Inland sea coast

1 1 9 1 12

Late Jomon Late Jomon Late Jomon

Funadomari Irie Takasago

Soya Iburi Iburi

NE Hokkaido island SW Hokkaido SW Hokkaido

4 6 4 14

NSM NSM KUM Honshu Late/Final total

Latest Jomon Late/Final Jomon Final Jomon

Miyano-Kaisuka Ikawazu Yoshigo

Iwate Aichi Aichi

NE Pacific coast S. Central bay S. Central bay

3 4 8 15

SMC SMC SMC Okhotsk total

Okhotsk Okhotsk Okhotsk

Hamanaka (1 and 2) Utoro-Jinjayama Ohmisaki

Nemuro Nemuro Soya

NE Hokkaido coast NE Hokkaido coast NE Hokkaido coast

2 2 4 8

SMC, Sapporo Medical College, Sapporo; NSM, National Science Museum, Tokyo; KUM, Kyoto University Museum, Kyoto.

vidual. Thus, in analysis, the sample sizes by variable may differ from total sample size. Residential dwellings and pottery indicate that the Middle Jomon experienced significant population expansion following the Early Jomon (starting roughly 6,000 BP), an estimated increase from 105,000 to 260,000 individuals (Imamura, 1996). Ceramic styles diversified as the population expanded. Incipient Jomon ceramic styles, when mapped, form two regions with a clear north–south division. By the Early Jomon, these regions splintered into at least six separate regional zones. This division persisted into the Middle Jomon (Imamura, 1996; Habu, 2004). Dates for the Middle Jomon period vary across geographic locations but roughly span 5,000– 3,000 BP. The Middle Jomon was the peak of cultural prosperity, enjoying a warm, temperate climate with abundant woodland flora and terrestrial fauna. Sea levels were lower, extending settlement areas along the coast, particularly around modern-day Tokyo. Archaeological evidence indicates a balanced dietary exploitation of plants and terrestrial and marine animals (Habu, 2004). Four of our sites date to the Middle Jomon, two from Honshu (Ebishima and Ohta) and two from Hokkaido (Kotan-Onsen and Kitakogane). Because the two Hokkaido samples consisted of one individual each, we grouped Hokkaido and Honshu data together to create a single Middle Jomon pool. During the Late and Final Jomon periods, the prosperity of the settlements declined with the estimated population dropping by 100,000 individuals. Again, dates vary across the islands but roughly span 4,000–2,000 BP. Regional divisions in ceramic styles became less marked, leaving three regions: northern Honshu, the southern islands of Kyushu, and the northern island of Hokkaido. Each had distinctive pottery styles and subsistence activities (Imamura, 1996). On Honshu, the south central regions collapsed earlier than the northern regions. The northern regions intensified production of ritual objects and tool artisanship, particularly specialized fishing implements. In a series of studies on the material culture of subsistence technology (Akazawa, 1981, 1982a,b, 1986a,b,c, 1987), a clear division in northeastern and south central/western subsistence economies American Journal of Physical Anthropology

emerged. Northeastern groups engaged in an increasingly specialized fishing subsistence economy and tended to be comparatively socially simple but maintained stability from the Middle period. The sites from the south central/inland sea area near to mainland Asia (specifically modern day Korea) had heavier concentrations of tools related to plant-based subsistence but also included some freshwater fishing implements. These south central/western groups, for which there are fewer archaeological sites, engaged in a broad-spectrum subsistence economy and were often socially complex (Habu, 2004). Artifacts related to open-sea fishing indicated economic exchange with southern Korea (Imamura, 1996). Ceramic style remained relatively simple and ritual objects were not as abundant in the north. Both males and females in these populations have a high frequency central/lateral ritual tooth ablation, reducing the sample size of our study. We used five archaeological sites from the Late/Final Jomon, analyzing those from Hokkaido (Funadomari, Irie, and Takasago) and Honshu (MiyanoKaisuka, Ikawazu, and Yoshigo) separately. The Okhotsk period was concurrent to the proto historic phase on Honshu, and lasted four centuries starting at about 1,000 BP (Aikens, 1982). The origin of the Okhotsk is not clear, but archaeological evidence suggests continuity with Sakhalin populations across the Okhotsk Sea in modern day Russia. The Okhotsk competed and blended with the local culture, the Satsumon. Okhotsk populations relied heavily on a marine-based food economy and had adequate dietary resources. Eventually, the Okhotsk disappeared from the archaeological record, most likely returning to Sakhalin (Aikens, 1982). We used three Okhotsk sites from Hokkaido: UtoroJinjayama, Hamanaka, and Ohmisaki. Despite temporal and regional fluctuations in cultural components, the sites used in this study are similar in many ways. Burial styles for adults are relatively uniform. The most common interment is the pit burial (Habu, 2004). All populations enjoyed the availability of a variety of seasonal foods. Archaeological evidence supports diverse exploitation of animals and plants and the storage of grains. However, subsistence variation, social structure, and genetic admixing (in the Okhotsk) suggest

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NUTRITIONAL AND DEVELOPMENTAL INSTABILITY variation between periods. In the Late and Final Jomon periods, the division between north and south Honshu also suggest potentially significant variation. Thus, we have grouped all Middle Jomon sites, divided Late/Final Jomon into geographic areas, and grouped Okhotsk sites.

TABLE 2. Hypoplasia frequencies Absent Middle Late/Final Honshu Late/Final Hokkaido Okhotsk

3 3 4 6

(25%) (25%) (23.5%) (75%)

Present 9 9 13 2

(75%) (75%) (76.5%) (25%)

METHODS We collected hypoplasia data on the maxillary and mandibular anterior dentitions. These teeth are developing concurrently with the upper facial bones, and exposed to increased stress throughout infancy and weaning (Goodman and Armelagos, 1985). A hypoplasia is present if both antimeres exhibit the defect, palpable by fingernail, at similar levels on the tooth crown labial surface (Goodman and Rose, 1990; Larsen, 1997). The upper facial metric data consist of three variables. Orbital height (OH) and orbital breadth (OB) for left and right sides follow standard osteological measurement guidelines (Buikstra and Ubelaker, 1994). We modified the standard osteological variable for maximum upper facial breadth (FB), to create right and left sides using the nasion as a midline landmark. We collected data in two trials. Of the 326 skulls examined, 49 individuals met the criteria for inclusion in the study (retaining anterior dentition and preserved and clear cranial landmarks). In this final sample, we were not able to collect data for all three variables on each individual. In the results, sample sizes by variable may be less than the total sample size of each period. Given the nature of differential preservation, local taphonomic processes, and possible confounding effects of ME, we explored the data for outliers to minimize contribution of nonbiological artifacts to variance. Asymmetry data analyses pose a challenge to the researcher. FA values may be inflated if the contributions of antisymmetry and DA to between-sides variation are ignored. This inflation suggests greater population DI than is actually represented by the data. Prior to comparing FA values between periods and groups based on hypoplasia, we followed the FA analysis guidelines presented by Palmer (1994) and Palmer and Strobeck (1986, 2003). First, we examined the data for outliers by visual inspection of various plots. Then we tested trait– size association (which may impact asymmetry index values) by Kendall’s tau b and Spearman’s rho to determine if values required log transformation to reduce the impact of size dependency. Next, we used the template spreadsheet for a two-way mixed-model ANOVA (sides 3 individuals) (http://www2.biology.ualberta.ca/palmer/ asym/FA/FA-Refs.htm#tools, Palmer, 1994; Palmer and Strobeck, 1986, 2003). We input mean squares (MS) values for sides, individuals, and sides 3 individuals interaction into the spreadsheet. The spreadsheet calculates the contribution of ME to asymmetry, the significance of FA after eliminating ME, and the FA10 index (an asymmetry index). Lastly, we tested for significant contributions to overall asymmetry from DA via t tests and antisymmetry via skew and kurtosis statistics. Hypoplasia data in this study are nominal, either present or absent. The nonparametric test for deviations from an expected distribution is the chi-square statistic. Unfortunately, this statistic is partially dependent on sample size. Small sample sizes may affect results. The phi statistic, however, reduces the effect of small sample

sizes by taking the square root of chi-square divided by sample size. Thus, we used the phi statistic in chi square analysis for nominal hypoplasia data to test if nutritional stress changed significantly over time. To test the hypothesis that DI increased from the Middle to Late/Final Jomon on Honshu and Hokkaido, respectively, and from Late/Final to Okhotsk on Hokkaido, we calculated F-statistics using FA10 and compared those results to the critical values (a 5 0.05) of the F-distribution by respective degrees of freedom. We calculated this F statistic from the ratio of FA values for the hypoplasia present and absent groups. Similarly, to test the hypothesis that the presence of hypoplasias is positively association with FA, we calculated the F-statistic to compare to critical values (a 5 0.05) of the F-distribution by respective degrees of freedom.

RESULTS Hypoplasia With the exception of the Okhotsk, where the trend reverses, hypoplasias occurred in roughly 75% of the individuals (Table 2). The phi statistic (0.399; P 5 0.05) suggests that significant differences between periods is likely due to the reversed trend during the Okhotsk. These small sample sizes, however, may not be representative of the population. Still, we expected fewer hypoplasias in the Middle Jomon, but there is no difference in frequency compared to either Honshu or Hokkaido frequencies in the Late/Final periods.

Fluctuating asymmetry An initial inspection of scatterplots did not reveal any suspect values, outliers, or trait–size asymmetries. We assessed trait dependency on overall trait size using Kendall’s tau b and Spearman’s rho correlations between the absolute value of side differences (|R 2 L|) and mean trait size [(R 1 L)/2]. There were no significant associations by period. On the level of the sample as a whole, there was one significant but weak value for OB (tau b 5 20.272; rho 5 20.478). These correlations are negative, however, which is unexpected if between-sides variability increases with trait size. Palmer and Strobeck (2003) found that the proportion of FA attributable to ME in larger individuals and/or traits tends to be smaller, thus making FA smaller overall. In a population where traits and/or individuals vary in size, this phenomenon may create a negative relationship but one that does not need a trait size dependency correction. We tested data for the presence of DA, skew, and kurtosis. Initial results suggested presence of DA in Late/ Final Honshu for FB and OH for Late/Final Hokkaido. After correction for multiple trials, the Bonferroni-corrected values were not significant. There were no significant results for skew or kurtosis. Thus, there is no significant contribution to overall asymmetry from antisymmetry or DA. American Journal of Physical Anthropology

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K.C. HOOVER AND H. MATSUMURA TABLE 3. Mixed-model ANOVA results by period FA [ ME

ME

Trait FB

OB

OH

Period

MS

df

F

P

Bonferronicorrected P value

Middle L/F Honshu L/F Hokkaido Okhotsk Middle L/F Honshu L/F Hokkaido Okhotsk Middle L/F Honshu L/F Hokkaido Okhotsk

0.0234 0.0169 0.0709 0.0290 0.0224 0.0232 0.0229 0.0226 0.0208 0.0219 0.0200 0.0194

18 20 32 16 16 20 28 16 16 18 26 10

45 30 56 32 83 47 179 61 80 26 27 13

0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00

0.01 0.01 0.00 0.03 0.01 0.01 0.00 0.01 0.01 0.02 0.01 0.05

ME % between-sides variance 2.21 3.33 1.79 3.10 1.21 2.11 0.56 1.64 1.25 3.83 3.75 7.67

TABLE 4. F-statistics and FA10 asymmetry indexa FA10 FB FA10 Approx. df OB FA10 Approx. df OH FA10 Approx. df

F-statistics

Middle

L/F Honshu

L/F Hokkaido

Okhotsk

M:LFH

M:LFK

LFK:O

0.5177 8

0.2445 8

1.9441 14

0.4527 7

2.12 CV 5 3.4

3.76* CV 5 3.24

4.29* CV 5 3.53

0.9126 7

0.5377 9

2.0376 13

0.6793 7

1.7 CV 5 3.29

2.23 CV 5 3.55

3 CV 5 3.55

0.8246 7

0.2745 7

0.2561 11

0.1165 3

3 CV 5 3.79

3.22* CV 5 3.01

2.2 CV 5 8.76

CV, critical value. * Significant F-statistics at a 5 0.05. a Palmer and Strobeck, 1986, 2003; Palmer, 1994.

We used the two-way mixed-model ANOVA template (Palmer and Strobeck, 1986, 2003; Palmer, 1994) to test significant between-sides variance after partitioning ME (Table 3). This analysis includes replicate measures to test for ME contributions to FA. The residual variance after partitioning ME was significant and attributable to FA. For all variables and all periods, FA remained significant after Bonferroni correction for multiple tests. A note on the repeatability of FA is appropriate. For most traits across periods, the contribution of ME to the total variance is 4% or less except in the Okhotsk period for OH, where it is just under 8%. This may be due to poor preservation for these materials. Overall, repeatability of FA is good. Testing the multiple hypotheses for significant FA differences (Middle to Late/Final Jomon on Honshu and Hokkaido, respectively, and Late/Final to Okhotsk on Hokkaido), we computed F-statistics using values for FA10 (Table 4) calculated by the two-way mixed-model ANOVA temple. FA 10 is an asymmetry index that removes error variance from overall variance (Palmer and Strobeck, 1986, 2003; Palmer, 1994). Since there were no significant contributions from DA and antisymmetry, all variation after partitioning ME is attributable to FA. On Honshu, FA unexpectedly decreases in the Late/Final Jomon. The F-statistics, however, did not exceed the expected critical value for the F-distribution; so, these trends, while surprising, are not statistically significant. On Hokkaido, FA increases from the Middle American Journal of Physical Anthropology

to Late/Final Jomon for FB and OB, but decreases for OH. Only FB and OH reach statistical significance. From the Late/Final Jomon to the Okhotsk, FA values consistently decrease, but FB is the only significant variable. During this time, the population admixture from Sakhalin may have increased genetic buffering in individuals or positively influenced cultural adaptations. It may also reflect improved environmental conditions or a combination of all these possibilities. Compared to the hypoplasia frequencies, which are consistent across time except for the decreased incidence during the Okhotsk, the FA index as a measure of DI seems to be a better estimate of temporal variation than the nutritional stress data, but only marginally. OH seems to be reflecting different things in many cases.

Hypoplasia and FA The last hypothesis we were interested in testing was the association between hypoplasia and asymmetry. Clearly, they are measuring different things, but given the synergistic relationship between malnutrition and pathology, which both contribute to DI (and vice versa), there may be a positive relationship between the two. Whether the hypoplasia contributes to increased DI or DI increases hypoplasia incidence or susceptibility is beyond the parameters of what we are able to test, but we can test if individuals with hypoplasias have greater FA.

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NUTRITIONAL AND DEVELOPMENTAL INSTABILITY TABLE 5. Mixed-model ANOVA results by hypoplasia FA [ ME

ME

Trait Present Absent

Period

MS

df

F

P

Bonferronicorrected P value

FB OB OH FB OB OH

0.0783 0.0205 0.0219 0.0204 0.0242 0.0200

30 30 22 56 50 48

13 70 29 124 118 39

0.00 0.00 0.00 0.00 0.00 0.00

0.05 0.02 0.03 0.01 0.01 0.01

We assessed trait dependency on overall trait size using Kendall’s tau b and Spearman’s rho correlations between the absolute value of side differences (|R 2 L|) and mean trait size [(R 1 L)/2]. For the group with no hypoplasia, there was one weak but significant negative correlation for OB (tau b 5 20.325). For the group with hypoplasias, there were two weakly significant negative correlations for OB (tau b 5 20.280; rho 5 20.475). In populations where traits and/or individuals vary in size, this may create a negative relationship wherein larger individuals have smaller overall FA relative to ME. Thus, no correction for trait size dependency is warranted. We used the mixed-model ANOVA template to test significant between-sides variation (Table 5). The residual variance after partitioning ME was significant and attributable to FA. For all variables, FA remained significant after Bonferroni correction for multiple tests. The group with hypoplasias had a significant contribution from DA for OH (t 5 20.3736). Normally, data exhibiting a significant amount of DA are excluded from FA studies, because attempts to eliminate DA from a sample affects the data distribution but does not eliminate the underlying genetic and/or environmental contributions. Palmer and Strobeck (2003), however, suggest a general guide for deciding if the DA effect is small enough for the data to be included in analysis. If the DA mean [mean (R 2 L)] is not larger than the value for the FA4a pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi index (0:798 varðR
LÞ, see Table 1 of Palmer and Strobeck, 2003) the effect is small and the data may be retained. For the group with hypoplasias, the OH DA mean (20.454) is smaller than FA4a (0.465). Given the small effect of DA, we retained these data for further analysis. There are no significant results for skew or kurtosis. For the test of association between FA and hypoplasia, we computed the F-statistic using the asymmetry index values for FA10 (Table 6). FA10 is derived from the twoway mixed-model ANOVA and removes error variance from between-sides differences (Palmer, 1994; Palmer and Strobeck, 1986, 2003). FA10 for individuals with hypoplasia for FB and OB is double that for individuals without hypoplasia. Surprisingly, only the F-statistic for FB exceeds its critical value. OB comes close at F 5 2.01. For OH, the difference between groups is slight.

DISCUSSION We hypothesized that the Middle Jomon populations, with adequate resources and balanced dietary intake, would have lower nutritional stress (measured by hypoplasia frequency) and DI (indirectly measured by FA) in comparison to Late/Final Jomon populations on Honshu

ME % between-sides variance 7.85 1.44 3.47 0.81 0.85 2.54

TABLE 6. F-statistics and FA10 asymmetry indexa Trait FB FA10 Approx. df OB FA10 Approx. df OH FA10 Approx. df

Present

Absent

F-statistics

1.25 27

0.46 12

2.73* CV 5 2.48

1.41 24

0.7 14

2.01 CV 5 2.35

0.38 22

0.3 9

1.25 CV 5 2.92

CV, critical value. * Significant F-statistics at a 5 0.05. a Palmer and Strobeck, 1986, 2003; Palmer, 1994.

and Hokkaido, respectively. Contrary to expectations, all Jomon populations had similarly high hypoplasia frequencies. The only possible environmental—as opposed to cultural or genetic—cause of increased hypoplasia frequency is parasitical infection from ingesting fish or through insect vectors in coastal regions (Walker, 1986). This explanation is not completely satisfying for these data. Okhotsk populations have low hypoplasia frequencies and archaeological data indicate lower nutritional stress in this period. Like the Jomon, however, the Okhotsk populations used marine resources—relied heavily on them in fact. If parasitical infections explain the higher than expected Jomon hypoplasia frequencies, why were the Okhotsk populations not suffering chronic and acute parasitical infection? A possible explanation is a hereditary form of hypoplasia (Hoover et al., 2004). Another explanation may be that the higher rates in sedentary Middle Jomon resulted from differential access to resources and social stratification. Perhaps the ritual tooth ablation practiced by central Jomon populations reduced our sample size for hypoplasias and skewed the results. A last explanation may simply be that small and unrepresentative sample sizes per site do not accurately reflect population level nutritional stress. On Honshu, the FA index also shows a trend contrary to our hypothesis that values will increase in the Late/ Final Jomon. Sample sizes are close in size for each period and FA values for the Late/Final period are almost half the Middle Jomon values but the F-statistics do not exceed the critical value and achieve significance. On Hokkaido, the FA indices for FB and OB support the hypothesis of decrease from the Middle to the Late/Final Jonon. The index for OH does not. The F-statistic for FB and OH exceed the critical values—in effect, cancelling each other’s value out. Small sample sizes have higher critical values; so, the lack of statistical significance may simply be the difficulty in exceeding these values. American Journal of Physical Anthropology

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The hypothesis that FA decreases in the Okhotsk is supported. Only FB exceeds the critical value. The standard measure for facial breadth has previously (DeLeon, 2007) been associated positively with other stress markers. Local populations may have benefited from the immigrant population, perhaps due to population admixture enhancing individual genetic buffering or through cultural diffusion of technology and resource exploitation. Another possibility is that local populations crashed and skeletal remains are mostly from immigrant populations. Lastly, we had proposed that the synergistic relationship between malnutrition and pathology might have in a positive relationship between stress markers. All three follow the expected trend that individuals with hypoplasia have higher values for FA10 but only FB exceeds the critical value for the F-statistic. OB comes close, which supports the overall hypothesis, even if weakly. Given the possible effect of DA in the OH data and its consistent discordance with other variable trends, OH may not be a good indicator of stability. Of the three variables, the one most likely to be associated with hypoplasia, based on De Leon’s (2007) research, would have been FB. Given a larger sample size with smaller critical values, the hypothesis might have more support. Overall, our data follow the expected trend and support the hypothesis.

CONCLUSION Throughout prehistoric preagricultural Japan (roughly between 16,500 BP and 300 BP), climate change influenced dietary adaptations and social structure. A stable climate during the Middle Jomon (5,000–3,000 BP) contributed to the availability of consistent and abundant resources on mainland Honshu and the northern island of Hokkaido. A quickly growing population led to a widespread cultural continuity across both islands. By the Late and Final Jomon (roughly 4,000–2,000 BP) on Honshu, population decline led to a fractured culture with regionally divergent subsistence economies and settlement patterns. In this paper, we examined temporal and spatial differences in developmental and nutritional stability using human remains from 13 archaeological sites. We used hypoplasia frequencies as a measure of nutritional stress and fluctuating asymmetry (of upper facial breadth, orbital height, and orbital breadth) as an indirect measure of developmental instability. The Middle Jomon sample consists mostly of individuals from Honshu and two individuals from Hokkaido. We hypothesized that Middle Jomon populations would experience greater nutritional and developmental stability in comparison to their counterparts from the Late/Final periods on Honshu and Hokkaido, respectively. We also hypothesized that Hokkaido Okhotsk (1,000–600 BP) populations would be more stable due to archaeological evidence suggesting adequate nutrition and the possible positive effect of immigrant populations. Lastly, we tested for a positive association between stress markers, given the synergistic relationship between pathology and malnutrition. Interestingly, we found a 75% incidence of hypoplasia throughout the Jomon period on both Honshu and Hokkaido. In the Okhotsk, hypoplasia frequency dropped dramatically to 25%. Certainly, the archaeological data indicate a stable diet for the Okhotsk, but this is true of the Middle Jomon as well. There are two possible explanations for the unexpectedly high incidence in the American Journal of Physical Anthropology

Middle Jomon, parasitical infection from marine resources and differential access to resources. Because the Okhotsk had a similar marine-based diet as the Jomon, parasitical infection does not seem as likely as the differential access to resources that accompanied the increasing social stratification in sedentary Middle Jomon communities. The FA data on Honshu did not support the hypothesis that Middle Jomon populations experienced less developmental stability. Asymmetry index values were lower in the Late/Final Jomon, but no value reached statistical significance. The lack of significant differences between Middle and Late/Final populations is interesting. Despite resource availability, social stratification may have had a significant impact on health in the Middle Jomon. The FA data follow the expected pattern on Hokkaido for two of the three variables (FB and OB) with an increase from the Middle Jomon to the Late/ Final periods. OH data indicate the opposite, a decrease. Both FB and OH test statistics were significant. The OH significant result may be attributable to the small contribution from DA. Of the three variables, we expected FB to yield significant results, as it was a good measure of FA in Nubians (DeLeon, 2007) and it consistently supports the hypotheses with the exception of greater stability in the Middle Jomon. Lastly, we tested the association between hypoplasia and FA. We expected to find that individuals with hypoplasias would have greater FA due to the synergistic relationship between nutrition and pathology. The presence of nutritional defects indirectly suggests those individuals (even those with greater genetic buffering) were more vulnerable to pathogenic infection, which then would disrupt genetic stability. Or, conversely, those infected with pathogens may not be adequately digesting food for proper nutriture, predisposing them to enamel defects. Test statistics for OB approached significance. OB came close to significance. Small sample sizes with higher significance thresholds may be part of the problem. Overall, the data general trend and one significant result support the hypothesis, suggesting that there is an association between nutritional and developmental stability. While the study was limited by small samples sizes, which raised the critical values and significance thresholds, all variables follow the expected trends with the exception of better nutritional and developmental stability in the Middle Jomon on Honshu. This may be the result of differential access to resources resulting from sedentism and ensuing social stratification in the Middle Jomon. Or, perhaps the transition to the Late Jomon was less disruptive to health than it was to culture. The relationship between FA and hypoplasia bears further investigation with larger sample sizes, as our data support the hypothesis that greater asymmetries occur in individuals with nutritionally based enamel defects.

ACKNOWLEDGMENTS We would like to thank the anonymous reviewers of this manuscript, the Sapporo Medical College, National Science Museum, and Kyoto University Museum.

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