dietary variation and stress among prehistoric jomon foragers from japan -temple 2007

8/10/2019 Dietary Variation and Stress Among Prehistoric Jomon Foragers From Japan -Temple 2007

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Japan, where dietary behavior was comparable toherbivorous ungulates and Yosekura in western Japan,where dietary behavior was primarily reliant on plantresources (Akazawa, 1999). Stable isotopic evidence forplant consumption is, however, reported from coastalsites in eastern Japan, while evidence of marine con-sumption is recorded among some inland Jomon sites

indicating some dietary variability within regions (Mina-gawa and Akazawa, 1992; Yoneda et al., 2004).

On a global scale, the level of contrast in diet betweenthe eastern and western Jomon is more often observedduring the agricultural transition, where greater fre-quencies of enamel hypoplasia and carious teeth arereported among many plant dependent agriculturalists(see Larsen, 1987, 1995). These declines in health andwell-being are associated with a continuum of environ-mental changes that include increased sedentism andpopulation density as well as the consumption of foodswith poor micronutrient availability and heavy carbohy-drate loads (Larsen, 1987, 1995, 2002).

Plant-based diets are associated with general growthdisruption and poor nutritional status if they are not

diverse and representative of the necessary micronu-trients essential to growth and development (Murphyand Allen, 2003). These findings have, for example, beendemonstrated in a clinical setting where animalsdeprived of vitamin A more frequently experienced dis-rupted enamel formation (May et al., 1993). Furthermore,many of the plant foods consumed by the western/inlandJomon were seasonal, and shortages may have ex-acerbated health during periods of resource scarcity(Akazawa, 1999). This paper, therefore, tests the hypoth-esis that the dietary choices of the western/inland Jomonwere associated with greater levels of systemic stressand oral disease. This hypothesis will be tested by com-paring frequencies of enamel hypoplasia and cariousteeth between the eastern and western Jomon.

Other indications of behavioral plasticity among theprehistoric Jomon are revealed through reactions to cli-mate change. Climatic cooling is evidenced by retreatingoak forests dated to c. 5,000 years BP with intensifica-tion of this trend recorded around 4,400 years BP(Koyama, 1978; Tsukada, 1986). This environmentalchange is associated with depopulation in inland andeastern Japan during the Late and Final Jomon period(Koyama, 1978). One interpretation of this populationdecline is that food plants were unable to adapt to colderenvironments resulting in diminished food returns forplant dependent Jomon foragers. Diminished foodreturns accelerated stress among local groups causingthem to seek out alternative resources from differentenvironments. Evidence supporting this idea has, how-ever, not been reported (Habu, 2004: 253254). Instead,studies of Jomon dispersal patterns suggest the possibil-ity of dietary change and migrations to less denselypopulated areas.

This paper, therefore, tests two additional hypotheses.First, it is hypothesized that foragers from the Middle toLate Jomon period will have greater evidence of systemicstress than Late to Final Jomon people. This hypothesiswill be tested by comparing frequencies of enamel hypo-plasia between Middle to Late and Late to Final Jomonforagers from western/inland Japan. Alternatively, evi-dence for a dietary shift associated with a behavioralresponse to climate change will be observed between theMiddle to Late and Late to Final Jomon periods. The al-ternative hypothesis differs from the first by suggesting

that Jomon foragers were able to respond to climatechange through shifting dietary foci and mitigating

stress levels. This hypothesis will be tested by comparingproportions of carious teeth between Middle to Late andLate to Final Jomon foragers.

MATERIALS AND METHODS

This paper uses the term eastern Japan as a geo-graphic and subsistence designation for marine foragersfrom Tokai and Kanto. Western/inland Japan is a geo-graphic and subsistence designation for Jomon gatherersfrom the Chubu and Chugoku regions, where dietarychoices were more often based around plant gatheringand cultivation. The temporal focus of this paper is theMiddle to Final Jomon period (5,0002,300 years BP).

The skeletal samples from which data were collectedwere recovered from the Hobi, Inariyama, Nakazuma,and Yoshigo archaeological sites in eastern Japan andthe Kitamura, Ota, Tsukumo and Yosekura archaeologi-cal sites from western/inland Japan (Fig. 1). All of thesites were dated using pottery-based chronology andradiocarbon methods. The use of pottery chronology isan accurate method to estimate site occupations in pre-historic Japan because of the preponderance of system-atic studies on the chronology of Jomon pottery (seereviews by Aikens, 1995; Imamura, 1996a; Habu, 2004).The approximate locations, dates, and site-specific num-ber of dental remains from which data were collected arelisted in Figure 1, and Table 1.

The Middle, Late, and Final Jomon periods are datedbased on radiocarbon analysis of pottery cultures.

Fig. 1. Map of Japan illustrating the approximate locationsof the sites used by this study. (1) Ota (W/I); (2) Yosekura (W/I);(3) Tsukumo (W/I); (4) Inariyama (E); (5) Yoshigo (E); (6) Hobi(E); (7) Kitamura (W/I); (8) Nakazuma (E). E, Eastern location.W/I, Western/inland location.

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Pottery-based chronologies date the Middle Jomon from5,000 to 4,000 years BP, Late Jomon from 4,000 to 3,000years BP, and the Final Jomon from 3,000 to 2,500 yearsBP in southern Honshu and 2,300 years BP northernHonshu (Habu, 2004). Climatic periods according tobotanical and pollen analysis vary from cultural periodsand include an RII period from 7,000 to 4,000 years BP(Tsukada, 1986). This period is considered a climatic

optimum, where warm temperatures are found through-out the Japanese Islands and dates from the Initial toMiddle Jomon periods (Tsukada, 1986). The climaticoptimum is characterized by \prosperous" Jomon cul-tures. Such prosperity is revealed by large scale popula-tions with complex social networks and subsistenceregiments found throughout Honshu (Imamura, 1996a).The RIIIa period (4,0001,500 years BP) is characterizedby a general cooling trend observed in central, eastern,and northern Japan and corresponds to the Late andFinal Jomon periods (Tsukada, 1986). Depopulation ofChubu and Kanto as well as increased density in Tohokuand Chugoku began during the RIIIa period (Koyama,1978).

Regional comparisons for enamel hypoplasia and cari-

ous tooth frequencies were made between sites listed aseastern and western/inland in Figure 1 and Table 1.Overall frequencies of enamel hypoplasia were com-pared. Temporal comparisons of enamel hypoplasia werelimited to sites within the western/inland region ofJapan because these areas had similar dietary patterns;any differences in enamel hypoplasia observed betweenthese groups would, therefore, likely be attributable tothe impact of climate change.

Systemic stress

Observation and recording of enamel hypoplasia andcarious teeth are used by this study to understand varia-tion in systemic stress and dietary patterns among the

prehistoric Jomon. Hypoplastic defects are grooves orpits observable on tooth surfaces caused by disruptedenamel production associated with periods of systemicstress during infancy and childhood (Goodman and Rose,1991) (Fig. 2). Hypoplastic defects were recorded as defi-ciencies in enamel thickness appearing as horizontalgrooves or pits on tooth surfaces. Presence of enamel hy-poplasia was determined by macroscopic observationaided by the use of a magnifying glass (103), naturalfluorescent lighting, and a 100 W Toshiba desk lamp.

Approximately 50% or more of the crown height was pre-sent on all examined teeth. The identification of enamelhypoplasia follow Skinner et al. (1995) and Guatelli-Steinberg (2003), where adjacent perikymata were com-pared to possible enamel defects to prevent confusingnormal variation in tooth morphology with enamel hypo-plasia. Enamel hypoplasia ranged in severity from mac-roscopically apparent to those that could not be viewedwithout the assistance of a magnification device. Fre-quencies of enamel hypoplasia are reported according tothe proportion of teeth with at least one defect dividedby the total number of teeth observed.

TABLE 1. Dates, locations, and curatorial locations for material used by this study

Sites Region Period Dates Curator

Inariyama Eastern Japan Late to Final 30002300 Kyoto Univ.a

Hobi Eastern Japan Final 30002300 UMUTb

Nakazuma Eastern Japan Late 40003300 Toride Boardc

Yoshigo Eastern Japan Late to Final 34002400 Kyoto Univ.

Kitamura Inland Japan Middle to Late 40003000 Chi. His. Soc.

d

Ota Western Japan Middle 50004000 Kyoto Univ.Tsukumo Western Japan Late to Final 30002300 Kyoto Univ./UMUTYosekura Western Japan Late 40003000 UMUT

a Laboratory of Physical Anthropology, University of Kyoto.b University Museum, University of Tokyo.c Toride Board of Cultural Assets.d Chikuma City Historical Society.

Fig. 2. Enamel hypoplasia on the right canine of a prehis-toric Jomon male from the Yoshigo site.

TABLE 2. Distribution of linear enamel hypoplasiason antimeric maxillary first incisors and mandibular

canines for eastern and western/inland Jomon foragers

Group NAa % LEH

Eastern Jomon Ia 47 21.2

Western Jomon I

a

28 60.7Eastern Jomon C 23 56.5Western Jomon C 39 61.5

a Number of individuals with antimeric pairs of canines orincisors.

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Problems in the interpretation of enamel hypoplasiafrequencies such as the under-enumeration of lesions arereported in the absence of microscopic analysis (Bertiand Mahaney, 1995; Hillson and Bond, 1997). Enameldefects identified by this study, therefore, represent aminimum estimate of teeth with evidence of stress epi-sodes. Other difficulty in enamel hypoplasia interpreta-

tion arises because defects associated with localizedtrauma appear similar to those from systemic stress(Hillson, 1996). Recording defects at similar developmen-tal locations on antimeres or other adjacent teeth helpsdefine the etiology of an enamel hypoplasia becausedefects arising from localized trauma appear on onetooth. The mandibular canines and maxillary first inci-sors most frequently display evidence of enamel hypopla-sia (Goodman and Armelagos, 1985). This study recordedfrequencies of enamel hypoplasia on antimeric pairs ofmaxillary first incisors and mandibular canines tounderstand if significant differences in hypoplasia fre-quencies exist between the overall distribution of enameldefects and those observed on different tooth types. Anti-meric enamel hypoplasia frequencies were calculated as

the sum of mandibular canine and maxillary first incisorpairs with evidence of enamel hypoplasia on both teethdivided by the total number of antimeric maxillary firstincisors and mandibular canines.

Enamel hypoplasia was also compared by individual tounderstand if interregional patterns of stress experi-enced at the individual level were similar to that sug-gested by cumulative tooth counts and antimeric toothpairs. Individuals with at least one observable toothwere included in the analysis; those with enamel hypo-plasia on at least one tooth were grouped into theenamel hypoplasia present category, while those lackinghypoplastic defects were grouped into the hypoplasiaabsent category. Individual comparisons of enamel hypo-plasia frequency were divided into adults and subadultsfrom eastern and western/inland Japan. Age groupswere divided on the basis of third molar eruption; suba-dults lacked a fully erupted third molar, whereas adultshad fully erupted third molars.

Oral health

Dental caries is a disease process associated with focalenamel demineralization by organic acids (Larsen, 1997:65) (Fig. 3). Organic acids are produced by bacteria thatconsume food particles in the oral cavity. Carious lesionswere recorded according to their presence on a specifictooth and identified based on enamel demineralization instages that ranged in size from destruction of more thanone half of a total tooth to pin-prick sized lesions. Thefrequency of carious teeth observed by this study is con-servative because high powered microscopy often identi-fies carious lesions that are unobservable through mac-roscopic examination (Hillson, 2000). Carious lesionswere identified under the same lighting described abovewith a 103 magnifying glass and dental mirror. Overallfrequencies of carious teeth were calculated as the totalnumber of teeth with observable carious lesions dividedby the total number of teeth observed.

Dental caries is an age-progressive process more fre-quently involving individuals in older age classes(Hillson, 2001). Additionally, carious lesions involvemolar teeth more often than the anterior dentition orpremolars (Larsen et al., 1991). A subset of teeth was di-vided according to age and tooth class. Age classes were

arranged according to first molar wear using the scoringprocedures described by Buikstra and Ubelaker (1994).Carious tooth frequencies between regional and temporalgroups were then compared for the anterior teeth (inci-sors and canines), premolars, and molars. Differences incarious teeth between males and females are anothermajor component to studies of dental caries and dietarybehavior (see Larsen et al., 1991). This study was notable to explore sex-based variation in carious teethamong Jomon skeletal samples because of poor cranialand pelvic preservation that limited the number of indi-viduals who could be assigned to a sex.

Statistical methods

Intraobserver error in the recording of hypoplasticlesions is a potential methodological shortcoming of mac-roscopic studies of enamel defects. Intraobserver errorwas addressed using observations recorded from 72 teethcurated by the University of Kyushu. The teeth werescored for the absence of enamel hypoplasia (1), presenceof one enamel hypoplasia (2), or presence of more thanone enamel hypoplasia (3). The teeth were then rescored2 weeks later using the same scoring criteria. A kappastatistic was applied to these observations to identify dif-ferences between the observed and expected levels of ob-server agreement (Cohen, 1960). Some researchers noteproblems with the kappa statistic because of variation intrait frequencies between populations that cause confu-sion in recognizing the same trait in different groups(Thompson and Walter, 1988). However, errors caused byconfusing enamel hypoplasia with other anomalous fea-tures are not expected because the perikymata in thearea of the enamel defects were observed for abnormalityof size. The kappa statistic generated for the observa-tions made by this study was 0.63 suggesting \substan-tial agreement" (0.610.80) between the actual andexpected results (Landis and Koch, 1977). The use ofthis terminology to classify these results is decidedly ar-bitrary (Landis and Koch, 1977: 165); however, the pur-pose here is to provide a \benchmark" to identify the

Fig. 3. Massive carious lesion involving the left first andsecond mandibular molars of a prehistoric Jomon female from

the Hobi site.

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strength of agreement associated with the kappa statis-tic. Previously reported kappa statistics regarding intra-observer error in enamel hypoplasia observation arecloser to 0.80 (see Guatelli-Steinberg, 2003). However,the series of teeth used to score this statistic was fromthe Yayoi period, where enamel hypoplasia frequencyand expression were less severe than the Jomon sample,

so the degree of correspondence in the current study,where enamel hypoplasia was generally more marked, islikely greater.

Overall frequencies of carious teeth and enamel hypo-plasia were compared between geographic and temporalgroups using 95% confidence intervals. Here, 95% confi-dence intervals around the overall frequencies of enamelhypoplasia and carious teeth from different geographiclocations and temporal periods are not expected to over-lap if these frequencies are different; similarity isimplied if overlap in 95% confidence intervals isobserved. Overall carious tooth frequencies are comparedfor anterior, premolar, and molar tooth groups, whileoverall frequencies of enamel hypoplasia are comparedfor all teeth. Confidence intervals were calculated using

the standard equations published in Zarr (1997).The G-statistic was applied as a measure of independ-

ence for individual and antimeric tooth pair frequenciesof enamel hypoplasia between geographic and temporalgroups, as opposed to the v2 test, because of the smallnumber of individuals yielding antimeric tooth pairs.The G-statistic is more appropriately applied to datawhere the observed minus expected cell frequencies aregreater than the expected cell frequencies (Sokal andRohlf, 1995; Gotelli and Ellison, 2004). Under these cir-cumstances low expected values are often calculated andthese values may greatly increase the v2 statistic (Sokaland Rohlf, 1995; Gotelli and Ellison, 2004). The v2 test issensitive to these circumstances because the expected

frequency is used as the denominator in the likelihoodratio that generates the v2 statistic.

RESULTS

Enamel hypoplasia

Frequencies of enamel hypoplasia observed on anti-meric maxillary incisors were significantly greateramong the western/inland Jomon than those from east-ern Japan (P 0.001) (Table 2). Statistically significantdifferences of enamel hypoplasia frequencies betweeneastern and western Jomon were not observed on anti-meric mandibular canines (Table 2). The lack of statisti-cally significant differences in enamel hypoplasia fre-quency of antimeric mandibular canines between easternand western/inland Jomon groups is attributed to a sam-pling bias associated with ritual tooth ablation. Antemor-tem extraction of the mandibular canines and incisors isroutinely observed among the prehistoric Jomon and isassociated with achieved social identities (Temple andSciulli, 2005). The differences between enamel hypopla-sia frequencies observed on maxillary first incisors are,

therefore, more representative of trends in systemicstress between the eastern and western Jomon.

The 95% confidence intervals for the overall frequen-cies of enamel hypoplasia between eastern (95% CI 0.3280.409) and western (95% CI 0.5300.611) Jomonpeople did not overlap (Table 3). In addition, the west-ern/inland Jomon cumulative (P 0.01) and adult (P 0.01) groups have statistically significantly greater fre-quencies of individuals with at least one hypoplastic epi-sode than those from eastern Japan (Table 4). Frequen-cies of individuals with at least one hypoplastic episodeamong subadult groups from these regions were not stat-istically significantly different (Table 4). The lack of dif-ference in individual frequencies of enamel hypoplasiaamong the subadult groups from eastern and western/

inland Japan is likely associated with a small samplesize. More data should, however, be collected for thispossibility to be further explored.

The Middle to Late Jomon had significantly less evi-dence of enamel hypoplasia on antimeric maxillary firstincisors than those from the Late to Final Jomon period(P 0.01) (Table 5). The confidence intervals for overallenamel hypoplasia frequencies between Middle to Late(95% CI 0.5110.620) and Late to Final (95% CI 0.4990.637) Jomon foragers overlapped.

Dental caries

Fewer carious teeth were observed among the west-ern/inland Jomon when compared to those from eastern

Japan (Table 6), with deviations in dental caries preva-lence observed at the Tsukumo and Yosekura sites when

TABLE 3. Regional enamel hypoplasia frequencies

Nteeth NLEH % LEH

Eastern Jomon sitesa

Inariyama 51 33 64.7Hobi 76 20 26.3Nakazuma 135 20 14.8Yoshigo 297 133 44.7Pooled Eastern 559 206 36.8

Western/Inland Jomon SitesKitamura 232 125 53.8Ota 98 62 63.2Tsukumo 136 84 61.7Yosekura 29 10 34.5Pooled Western/Inland 495 281 56.7

a

Number of teeth observed for enamel hypoplasia (combinedright and left sides from mandible and maxilla).

TABLE 4. Regional frequencies of enamel hypoplasia by individual

Location Nindividualsa % LEHb Nsubadultsc % LEH Nadultsd % LEH

Eastern Jomon 164 48.2 34 52.9 106 48.1Western/Inland Jomon 122 64.8 22 68.2 90 64.4P 0.01 NSe 0.01

a Total number of individuals with at least one observable tooth.b Percentage of individuals with at least one observable hypoplastic episode.c Total number of subadults with at least one observable tooth (aged 015 years).d Total number of adults with at least one observable tooth (age


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compared with the other sites from western/inlandJapan (Table 6). However, when these data are exam-ined within a temporal context a more significant pat-tern becomes evident: Middle to Late Jomon foragershad fewer carious teeth than Late to Final Jomon forag-

ers (Table 7); statistical analysis was not performed onthese data because they represent biased estimates ofcaries prevalence without regard to age or tooth type.These patterns are also evident in all three age groupsbetween Middle to Late and Late to Final Jomon people(Table 8). Statistical analysis was performed on the Mid-dle to Late vs. Late to Final Jomon caries data that wasdivided into age and tooth groups (Table 8). It is signifi-cance tests that were not performed. The confidenceintervals for molar and overall carious tooth frequenciesbetween Middle to Late and Late to Final Jomon did notoverlap in any age category (Table 9). Carious tooth fre-quencies in the anterior and premolar tooth classes of allthe three age groups overlapped (Table 9).

DISCUSSION

Evidence for nutritional variation

Population density increases are recorded in westernJapan between the Middle and Late Jomon period(Koyama, 1978). Rises in chronic and acute infection aswell as greater parasite loads are recorded in sedentarypopulations of increased density, where greater exposureto and transmission of pathogens is recorded. Greaterpathogen exposure and transmission is related toincreases in host-contagen ratios, contact with infectedpeople, contaminated water supplies, and waste disposalissues (Armelagos, 1990; Jackson, 2000). Clinical studiesreport a relationship between enamel hypoplasia and in-

fectious diseases. Experimental results, for example,found that sheep with elevated parasite loads were likelyto form an enamel hypoplasia (Suckling and Thurley,1984; Suckling et al., 1986). These findings are sup-ported by bioarchaeological evidence for increasedenamel hypoplasia frequencies among hunter-gathererswho had recently undergone population expansions(Walker and Lambert, 1989; Lambert, 1993; Stodder,1997). A comparison of enamel hypoplasia frequenciesbetween two western Jomon groups from time periodswith different population densities (Ota and Tsukumo),however, shows no significant change in systemic stresslevels. These results suggest that the gradual elevationof population density in western Japan is not character-ized by variation in enamel hypoplasia frequencies.

Dietary choices were the primary environmental dif-ference between the prehistoric Jomon from easternJapan and those from western and inland locations. Thesubsistence economy of the western and inland Jomonwas more focused on plant based resources, whereas thedietary choices of eastern coastal Jomon included greatermarine consumption.

Dietary reliance on plant foods is associated with thesubstandard synthesis of proteins, minerals, and vita-mins, particularly iron, vitamin A, and zinc (Murphyand Allen, 2003). Poor iron, vitamin A, and zinc intakeare, for example, associated stunted growth in childrenwith limited access to animal source foods (Rivera et al.,2003). This stunting occurs because of the importance ofzinc, iron, and vitamin A in the development of insulin-

like growth factor I, plasma concentration levels, andhuman growth hormone receptors. Additionally, pooriron mobilization and hemoglobin synthesis caused by alack of vitamin A and riboflavin intake among plantdependent people act as contributing factors to iron defi-ciency anemia and scurvy (Murphy and Allen, 2003).These difficulties are demonstrated by greater enamelhypoplasia frequencies in famine period Chinese (Zhouand Corruccini, 1998) and undernourished people fromGuatemala (Goodman et al., 1991; May et al., 1993). Pre-historic foragers who were reliant on terrestrial mam-mals also experienced an increase in enamel hypoplasiafrequencies after the transition to plant-based agricul-ture (Cook, 1980, 1981, 1984; Lukacs, 1992; and others).

Another possible contributor to the elevated frequencyof enamel hypoplasia among the western/inland Jomoncompared to those from eastern Japan is seasonalresource depletion. The majority of the plant foods con-sumed by these groups were seasonally available(Koyama, 1978; Akazawa, 1999). It is possible that thewestern/inland Jomon suffered seasonal periods of stressduring times when resources were unavailable andstored food became scarce. Similar findings are reportedfrom the American Southwest where greater indicatorsof stress are associated with seasonal resource depletion(Stodder et al., 2002; and others). These findings do notdownplay the role of infectious disease and populationdensity on the development of enamel hypoplasia; rather,the goal here is to interpret these lesions within the con-text of the prehistoric Jomon environment. In this con-

TABLE 5. LEH frequencies among Middle to Late andLate to Final Jomon

Group

Middle to Latea Late to Finalb

NAc 14 (50.0)d 14 (71.4)Nteethe 330 (56.7) 165 (56.9)

a Middle to Late Jomon sample consists of the Kitamura andOta sites.b Late to Final Jomon sample consists of the Tsukumo and Yose-kura sites.c Number of individuals with antimeric first maxillary incisors.d Values in parentheses indicate % LEH.e Total number of teeth (i.e., incisors and canines).

TABLE 6. Regional differences in carious tooth frequencies

Nteeth Ncarious % carious

Eastern Jomon sitesInariyama 330 18 5.4Hobi 416 39 9.4Nakazuma 615 69 11.2Yoshigo 1,181 135 11.4Pooled Eastern 2,542 261 10.3

Western/Inland Jomon SitesKitamura 943 35 3.7Ota 505 19 3.8Tsukumo 675 65 9.6Yosekura 204 18 8.8Pooled Western/Inland 2,327 137 5.9

TABLE 7. Temporal differences in carious tooth frequencies

Time period Nteeth % carious

Middle to Late Jomon 1,448 3.7Late to Final Jomon 2,746 10.1

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text, the differences in enamel hypoplasia frequenciesbetween the eastern and western Jomon likely reflect

stress variation associated with dietary choices and foodavailability.

Evidence for collapse

Evidence for climate change and population collapseduring the later part of the Middle Jomon period is notsupported by episodes of systemic stress. Of particularinterest is the even distribution of enamel hypoplasiafrequencies overall, as well as the random distributionacross samples and time periods of any observed differ-ences in enamel hypoplasia (Tables 5 and 6). If the cli-mate changes of the Middle to Late Jomon periodresulted in significant resource depletion and subsequentcollapse, it is expected that the combination of plant de-pendent diets and scarcity of food would be associatedwith significantly greater frequencies of enamel hypopla-sia among the Middle to Late Jomon sample. Theseresults suggest that the foragers from the Middle to LateJomon period did not undergo a nutritional crisis duringthe climatic shift of approximately 5,000 years BP.

In contrast, elevated systemic stress is documented inthe American Southwest where climate changes areassociated with seasonal resource depletion (Stodderet al., 2002). Similarly, people exposed to the Chinesefamine show marked increases in enamel hypoplasia fre-quencies (Zhou and Corruccini, 1998). Bioarchaeologicalstudies of enamel hypoplasia, stature, porotic hyperosto-sis, and population collapse in the Mayan lowlands, how-ever, failed to provide evidence for intensive systemic

stress during the Post Classic period (Wright and White,1996). Instead, regional differences in stress patterns

reflective of social and environmental variation arereported. Similar patterns are observed among the pre-historic Jomon, where variation in systemic stress indi-cators fail to support a demographic collapse associatedwith a nutritional crisis.

Other regions such as Tokai and eastern Kanto alsoexperienced sharp population declines and climatic cool-ing during the Middle to Late Jomon period (Koyama,1978). Elevated stress episodes are not recorded amongthese groups. Instead, depopulation in the Chubu,Kanto, and Tokai regions was associated with migrationsto other areas such as Tohoku or western Japan. Grad-ual increases in density are recorded in both Tohoku andwestern Japan during the Middle to Late Jomon period(Koyama, 1978). These results are consistent witharchaeological hypotheses that suggest the climatechanges of the Middle to Late Jomon period were associ-ated with adjustments in subsistence regiments and pop-ulation dispersals into surrounding ecological zones(Habu, 2004: 254255).

Evidence for subsistence changeand dietary choices

Greater caries prevalence among the Late to FinalJomon suggests a cultural/behavioral shift following theMiddle to Late Jomon period. Evidence for dietarychange is illustrated following climatic oscillations inNorthern China, where greater masticatory stress andsex-based differences in calculus are recorded during

TABLE 8. Observed frequencies of carious teeth within each age and tooth group

Ant Na % carious Pre Nb % carious Mol Nc % carious Nteethd % carious

Age Group 1Middle to Late 84 0 77 2.6 118 5.0 279 2.9Late to Final 77 1.3 134 5.2 216 18.8 427 8.1

Age Group 2

Middle to Late 105 0.0 134 2.2 218 4.1 457 2.6Late to Final 184 3.8 375 2.9 474 11.1 1,033 6.9Age Group 3

Middle to Late 105 1.9 121 6.0 212 6.1 438 4.1Late to Final 110 1.8 183 4.4 285 19.3 578 11.2

a Number of anterior teeth.b Number of premolar teeth.c Number of molar teeth.d Total number of teeth.

TABLE 9. Confidence intervals for carious tooth frequencies

Group ANT 95% CIa PRE 95% CIb MOL 95% CIc Overall 95% CId

Age Group 1Middle to Late Jomon 0.0030.119 0.0190.134 0.0130.068Late to Final Jomon 0.00030.179 0.0260.103 0.1540.249* 0.0600.112*

Age Group 2Middle to Late Jomon 0.0040.100 0.0130.091 0.0140.045Late to Final Jomon 0.0160.058 0.0150.060 0.0900.146* 0.0560.086*

Age Group 3Middle to Late Jomon 0.0020.181 0.0240.120 0.0340.114 0.0250.064Late to Final Jomon 0.0020.119 0.0190.107 0.1710.243* 0.0940.146*

a 95% confidence intervals for carious tooth frequencies in anterior tooth group.b 95% confidence intervals for carious tooth frequencies in premolar tooth group.c 95% confidence intervals for carious tooth frequencies in molar tooth group.d 95% confidence intervals for carious tooth frequencies in cumulative tooth groups.




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networks of prehistoric Jomon had a great impact on bio-logical variation before the arrival of the Yayoi. This con-clusion is supported here by variation in systemic stressindicators observed among Jomon foragers from differentenvironmental contexts, and by evidence of a dietaryshift, possibly in response to environmental change.

Interregional environmental heterogeneity is, however,

also documented among these prehistoric people. Geo-graphic, seasonal, and temporal fluctuations in socialcomplexity, sedentism, and population density are allcharacteristic of Jomon foragers (Koyama, 1978; Ima-mura, 1996a; Habu, 2004; Yoneda et al., 2004). Thesefindings suggest that the degree of biological variationattributable to environmental variables and behavioralchoices reported by this study is modest. Few data havebeen collected from human skeletal remains recovered atsmaller Jomon sites from the eastern and western/inlandregions of Japan. Bioarchaeological inquiries that con-sider samples of skeletal remains from single regions(i.e., western/inland Japan or eastern Japan) are, there-fore, an integral component to further understanding theenvironmentally directed biological variation of the pre-

historic Jomon people. It is expected that interregionalvariation in systemic stress patterns also played a signif-icant role in directing the biological and cultural evolu-tion of prehistoric Jomon people.

The findings of this paper also support a resource-stress model regarding the swift adoption of agriculturein prehistoric western Japan. Yayoi migrants entered Ja-pan around 2,500 years BP (Imamura, 1996a). A popula-tion boom associated with these migrations is reportedfirst in western Japan (Koyama, 1978; Hanihara, 1987).

Agriculture was quickly adopted in western Japan, spe-cifically in the regions of southwestern Honshu andnorthern Kyushu compared to a period of behavioral con-tinuity among the eastern Jomon (Akazawa, 1981, 1982).One reason for this swift adoption of wet rice agricultureamong the western Jomon was a hypothesized broadbased plant dependent economy in western Japan whichcontrasted with the more marine focused economy ineastern Japan. Here, the significant population increaseduring the Yayoi period (see Koyama, 1978; Hanihara,1987) is hypothesized to have resulted in reducedresource predictability within the broad based subsist-ence regiment of the western Jomon (Akazawa, 1981,1982). While the results of this study do not support aresource related collapse among the Late to Final Jomonpeople, a greater degree of systemic stress is observed inwestern Japan. Under these conditions, prehistoric peo-ple are hypothesized to change their subsistence strat-egies in an effort to moderate environmental constraints(Goodman and Armelagos, 1989). The greater degree ofsystemic stress observed among the western Jomon

likely reflect an environment where the swift adoption ofagriculture helped combat the stresses of broad basedplant dependent diets and possibly mitigated the impactof large-scale Yayoi migrations on resource predictability.

CONCLUSIONS

The results of this study support two hypothesesregarding environmental interactions among the prehis-toric Jomon. First, differences in enamel hypoplasia fre-quencies suggest variation in systemic stress patternsamong the prehistoric Jomon, with greater stress levelsrecorded among western/inland plant gatherers. These

differences support archaeological studies of subsistencechoices among the eastern and western/inland Jomon.Here, greater evidence of systemic stress among west-ern/inland plant gatherers is consistent with the stressesassociated with plant dependent economies and season-ally based resource depletion. However, frequencies ofenamel hypoplasia fail to support wide-spread systemic

stress associated with a resource crisis during the Mid-dle to Late Jomon period. Instead, greater frequencies ofcarious teeth were observed among Late to Final Jomonforagers compared with those from the Middle to LateJomon period. These changes suggest a subsistence shiftafter the climatic changes of the Middle to Late Jomonperiod. The presence of a dietary shift after a significantclimate change follow the model of culturally inducedstress of Goodman and Armelagos (1989), where behav-ioral decisions in response to environmental constraintoften carry biological consequences. Here, these conse-quences are illustrated by a rise in carious teeth follow-ing climatically induced dietary change.

The results of this study also have important anthro-pological implications because they support the existence

of environmentally directed biological variation amongprehistoric foragers. Such variation is rarely documentedin the bioarchaeological literature because the dietarychoices and living conditions of most prehistoric foragerswere confined to specific environments. Additionally,studies of biological variation among the prehistoricJomon often focus on the origin of modern Japanese orthe impact of Yayoi migrations on the spread of Jomontraits. Such questions are geared towards a genetic con-text. In contrast, this study documents an underlyingtheme of variation in systemic stress experiences and di-etary behavior before the arrival of Yayoi migrants.Finally, the results of this study indicate that the swiftadoption of wet rice agriculture by the western Jomonwas likely facilitated by environmental constraints, asindicated by the greater degree of systemic stressrecorded in the teeth of these foragers. The findings ofthis study suggest that both behavioral choices and thenatural environment contributed significantly to evolu-tionary processes in Japan, crossing large portions of ge-ographic and temporal space.

ACKNOWLEDGMENTS

I thank Clark Larsen, Paul Sciulli, Debbie Guatelli-Steinberg, Kris Gremillion, and Sam Stout, from TheOhio State University, for their helpful comments andsupport of this study. I am also grateful to MasatoNakatsukasa, Kazumichi Katayama, Wataru Yano, andShiori Fujisawa (Kyoto University), Takao Suzuki (TokyoGerontology Research Institute), Gen Suwa, SoichiroMizushima, and Aiko Sasao (University Museum,Tokyo), Masatsugu Hashimoto (Tokyo Dental College),

Yoshitaka Miyauchi and Reiko Omi (Toride Board ofCultural Assets), Hiroko Hashimoto (Nara Institute forthe Study of Cultural Properties), Nobuo Shigehara(Kyoto Primate Research Institute), Tamotsu Kawasaki(Nagano Historical Museum), Takahiro Nakahashi, KojiMizoguchi, Yoshiyuki Tanaka, Shozo Iwanaga, and KenjiOkazaki (Kyushu University) for allowing me access toand providing me assistance with the collections used bythis study. I thank Kara Hoover (Temple University) forallowing me to use her camera while she was at KyotoUniversity in 2004 and for helpful resources on enamel




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hypoplasia. I would also acknowledge Patricia Lambertand two anonymous reviewers whose thoughtful com-ments greatly improved this manuscript.

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