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Patterns of systemic stress during the agricultural transition in prehistoric Japan.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 142:112–124 (2010)
Patterns of Systemic Stress During the Agricultural
Transition in Prehistoric Japan
Daniel H. Temple*
Department of Anthropology, University of Missouri, Columbia, MO 65211-1440
KEY WORDS
enamel hypoplasia; cribra orbitalia; Jomon; Yayoi; bioarchaeology
ABSTRACT
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 142:112–124, 2010. V 2009 Wiley-Liss, Inc.
This study documents and interprets systemic stress
patterning during the agricultural transition in prehistoric Japan using linear enamel hypoplasia (LEH) defects
and cribra orbitalia (CO) lesions. LEH defects and CO
lesions were utilized because these nonspecific indicators
of stress represent independent reactions to environmental stimuli and provide a broad perspective on health outcomes between behaviorally and ecologically diverse people (Huss-Ashmore et al., 1982; Goodman et al., 1984;
Larsen, 1997). LEH defects are horizontal pits or grooves
observable on tooth surfaces caused by disrupted enamel
production during infancy and early childhood (Goodman
and Rose, 1991). When enamel production is disrupted,
shortened enamel prisms are deposited on the dentine by
ameloblasts (enamel producing cells) (Hillson, 1996). Disruption of enamel production is associated with a variety
of conditions including malnutrition, acute and chronic
infection, trauma, and hereditary anomalies (Goodman
and Rose, 1991). There is general consensus, based on
observations among living communities and individuals
from known environments, that the prevalence of teeth/
individuals affected by LEH defects reflects systemic
stress levels (Goodman et al., 1991; May et al., 1993; Zhou
and Corruccini, 1998).
CO lesions occur when blood producing bone marrow
in the cranium expands, increasing red blood cell production (Stuart-Macadam, 1985). Marrow expansion
through the cortex of the orbital roof produces sieve-like
lesions. CO is associated with a variety of anemic conditions, rickets, scurvy, and inflammation (Wapler et al.,
2004; Walker et al., 2009). Many of these nutritional
deficiencies are associated with parasite exposure and
diarrheal disease (Walker, 1985, 1986; Walker et al.,
2009).
The agricultural transition represents one of the most
pivotal phases of biocultural evolution for modern
humans (Larsen, 1987, 1995, 2002). Mutual reliance
between humans and plants characterizes this behavioral shift and suggests humans became dietarily dependent on agricultural products (Rindos, 1984). Such
relationships differ from foraging or food procurement
economies where domestication of plants (plant reliance
on humans) often occurs in the absence of human
reliance on cultigens (Harris, 1989; Smith, 2000). Agricultural economies formed the basis for expansions in
population density and urbanization.
Bioarchaeological research has questioned the extent
to which modern humans benefited from the transition
to food producing economies (Cohen and Armelagos,
1984; Larsen, 1987, 1995, 2002, 2006; Cohen and CraneKramer, 2007). Percentages of teeth and individuals
with LEH defects increased significantly in response to
dietary stress and infectious disease levels in the Western Hemisphere and Southwest Asia following the transition to intensive agriculture (Cook, 1980, 1981, 1984;
C 2009
V
WILEY-LISS, INC.
C
Grant sponsor: Wenner Gren Foundation for Anthropological
Research.
*Correspondence to: Daniel H. Temple, Department of Anthropology, University of Missouri-Columbia, Columbia, MO 65211-1440.
E-mail: templedh@missouri.edu
Received 5 February 2009; accepted 3 September 2009
DOI 10.1002/ajpa.21208
Published online 1 December 2009 in Wiley InterScience
(www.interscience.wiley.com).
113
JOMON AND YAYOI STRESS
TABLE 1. Jomon and Yayoi sample data
Site
Kitamura
Ota
Tsukumo
Yosekura
Hobi
Inariyama
Nakazuma
Yoshigo
Doigahama
Kanenokumac
Koura
Nagaoka
Date
5000–3000
5000–4000
3000–2300
4000–3000
3000–2300
3000–2300
4000–3000
3400–2400
2500–1900
2500–1900
1900–1700
2100–1900
Group
BP
BP
BP
BP
BP
BP
BP
BP
BP
BP
BP
BP
b
Inland Jomon
Western Jomon
Western Jomon
Western Jomon
Eastern Jomon
Eastern Jomon
Eastern Jomon
Eastern Jomon
Yayoi
Yayoi
Yayoi
Yayoi
Curation
Na
Nagano
Kyoto University
Kyoto University
Tokyo University
Tokyo University
Kyoto University
Kyoto University
Kyoto University
Kyushu University
Kyushu University
Kyushu University
Kyushu University
93
42
67
59
66
34
103
181
143
68
53
20
a
Approximate numbers of individuals available for study. The number of teeth and orbital vaults available for each sample differs
from these numbers.
b
Inland Jomon diet was likely similar to those from western regions (Akazawa, 1986; Minagawa and Akazawa, 1992).
c
A skeleton from this sample was dated to 2350 BP using AMS 14C methods with correction for the marine reservoir effect
(Tanaka et al., 2005).
Kennedy, 1984; Rose et al., 1991; Lukacs, 1992; Larsen
et al., 2002; and others). CO prevalence increased
among maritime foragers and following the transition to
agriculture in many regions, reflecting the interaction of
infectious disease loads with nutritional homeostasis
(El-Najjar, 1976; Walker, 1985, 1986; Walker et al.,
2009).
The biological impact of wet rice dependent economies
in Southeast Asia differs from that observed in other
regions. Increases in LEH defects and CO prevalence are
not reported in Thailand or Vietnam (Pietrusewsky and
Douglas, 2002a,b; Oxenham, 2004; Domett and Tayles,
2007; Douglas and Pietrusewsky, 2007). Continued reliance on broad-based economies and stasis in frequencies
of infectious diseases are likely responsible for these
trends in Thailand (Pietrusewsky and Douglas, 2002a,b;
Douglas and Pietrusewsky, 2007; Domett and Tayles,
2007), though increases in the prevalence and variety of
infectious diseases are reported in regions such as
Vietnam (Oxenham et al., 2005). These findings suggest
that the transition to wet rice economies may not have
produced the types of nutritional stressors associated
with intensive agriculture in other regions of the globe,
though chronic infection related to population aggregation and migration is noted (Larsen, 2002, 2006).
In Japan, Jomon subsistence economies were broadbased, regionally variable, and terminated with the
introduction of wet rice agriculture during the Yayoi period (2500–1700 BP) (Akazawa, 1981, 1982, 1986; Akazawa and Maeyama, 1986; Imamura, 1996a,b; Habu,
2004). Geographic distributions of tools indicate that
Jomon foragers from eastern Japan had more sophisticated systems for maritime and terrestrial mammal food
procurement than those from western and inland
regions (Akazawa, 1986; Akazawa and Maeyama, 1986).
Eastern Jomon economies were supported by a forest–
estuary ecosystem that included coastal embayments,
long-spanning coastlines, and diluvial uplands (Akazawa, 1986). Forest–estuary ecosystems likely provided
year-round access to foods such as finfish and mollusks,
terrestrial mammals, and plant products suggesting that
calorically dense foods were available for much of the
year (Akazawa, 1986, 1999; Minagawa and Akazawa,
1992).
In contrast, western and inland Jomon sites were situated in forest–freshwater ecosystems that exist as transitional zones between rivers, lakes, and forests (Aka-
zawa, 1999). Tools related to plant procurement discriminate sites from these regions (Akazawa, 1986; Akazawa
and Maeyama, 1986). Plant availability in this region
was subject to seasonal fluctuations and may not have
been available at certain times of the year (Akazawa,
1986; Hudson, 1999). Nevertheless, recent stable isotope
analysis of human skeletal remains suggests significant
consumption of marine finfish by inland/western compared to eastern Jomon people (Minagawa, 2001; Yoneda
et al., 2004; Kusaka, personal communications). Finfish
consumed by these groups was, however, seasonal in
availability (Kobayashi, 2005). Fallback foods exploited
by western Jomon people were nutritionally poor, particularly when compared with those consumed by eastern
Jomon communities (Akazawa, 1986). Fallback foods are
defined as resources consumed during periods when primary/preferred foods are unavailable (Marlowe and
Berbesque, 2009). These fallback foods included acorns,
leafy greens, roots, tubers, and walnuts in western Japan (see: Akazawa, 1986 Table 1) and terrestrial mammals combined with seasonal roots/tubers in eastern Japan (Akazawa, 1999). Greater frequencies of teeth and
individuals with LEH defects are observed among Jomon
people from western and inland sites compared to eastern regions (Shigehara, 1994; Temple, 2007a). These
studies suggest western and inland Jomon people experienced greater systemic stress due to narrow food availability and nutritional quality (Shigehara, 1994; Temple,
2007a).
Previous research explored frequencies of teeth with
LEH defects and CO between Jomon, Yayoi, Kofun, and
historic Japanese people as well as the relationship of
these lesions to Harris lines (Koga, 2003). Similar CO
and lower LEH prevalence is observed among Yayoi compared to Jomon samples. Jomon groups were, however,
compared as pooled data sets to Yayoi samples (Koga,
2003), despite variable economies between regions (Akazawa, 1981, 1982, 1986, 1999).
Three (3) specific hypotheses associated with the biological impact of agricultural economies in prehistoric
Japan are tested by this study. These hypotheses are
developed in concert with previous research that suggests little change or improvement in nutritional status
following the transition to wet rice agriculture in Southeast Asia (Pietrusewsky and Douglas, 2002a,b; Oxenham, 2004; Domett and Tayles, 2007; Douglas and Pietrusewsky, 2007), and more specifically, Japan (Koga,
American Journal of Physical Anthropology
114
D.H. TEMPLE
2003). First, it is predicted that the introduction of wet
rice economies will be associated with a reduction in systemic stress in western Japan. Frequencies of teeth and
individuals with LEH defects will significantly decline
among prehistoric Yayoi compared to western Jomon
communities. This decline will be associated with the
introduction of a predictable, renewable resource base
and exploitation of more nutritionally adequate dietary
alternatives. Second, the hypothesis that a similar prevalence of teeth and individuals with LEH defects will be
observed between Yayoi agriculturalists and Jomon foragers from eastern Japan is also tested. This prediction
expects similar stress patterns between these two groups
because both cultures practiced intensive subsistence
strategies focused on high yield, reliable food sources,
and consumed more nutritious fallback foods. Finally,
the hypothesis that CO frequencies remained static following the transition to agriculture in prehistoric Japan
is tested. This study predicts stasis in CO prevalence
between Jomon and Yayoi period samples as each group
thrived in contexts associated with elevated CO prevalence, specifically sedentary agricultural and maritime
environments. Jomon samples from eastern and western
Japan are combined to test this third hypothesis because
similar rates of CO are observed between the two groups
(Suzuki, 1998).
BIOCULTURAL CONTEXT
Jomon
Jomon period (13,000–2300 BP in eastern Japan) cultures were part of a 10,000 year foraging tradition in the
Japanese Islands (Imamura, 1996a). Jomon foragers were
the descendents of Pleistocene nomads who migrated to Japan around 20,000 BP and subsumed preexisting ‘‘knifeblade’’ cultures (Kobayashi, 2005). These later groups were
associated with a ‘‘microblade’’ technology that first
appeared in Hokkaido, likely in relation to the expansion
of cultural networks from eastern Siberia (Imamura,
1996a; Kobayashi, 2005). Microblade Paleolithic industries
diversified from Hokkaido into Tohoku around 14,000 BP,
evolved into Mikoshiba tradition, and formed the basis for
the earliest spread of Jomon culture (Imamura, 1996a).
One set of hypotheses surrounding the earliest migrations to the Japanese Islands suggest that the ancestors
of Jomon people migrated from Sundaland (Turner,
1990; Hanihara, 1991). These hypotheses are based on a
dental morphological complex (i.e., Sundadonty)
observed in Jomon people and shared with the early
inhabitants of Sundaland (Turner, 1990, 1992; Matsumura and Hudson, 2005; and others). Multivariate analyses of cranial and dental measurements also find similarities between the Paleolithic foragers of Japan, Jomon
people, and individuals from Sundaland (Hanihara,
1991; Baba et al., 1998; Hanihara and Ishida, 2005).
Other multivariate analyses of cranial and dental traits
suggest a Northeast Asian ‘‘point of origin’’ for the Pleistocene ancestors of Jomon foragers (Doi et al., 1997; Dodo et
al., 1998; Pietrusewsky, 2005; Seguchi et al., 2007; Hanihara and Ishida, 2009; and others). Cold-derived body size
among Jomon foragers and the Pleistocene occupants of
the Japanese Islands suggest that this region was initially
populated by foragers from a colder environment such as
Northeast/Central Asia (Temple et al., 2008). Analysis of
classic loci and Y-chromosomes derived from the Ainu suggest a Northeast/Central Asian ‘‘point of origin’’ for the
ancestors of Jomon people dating to 20,000 BP (Omoto
American Journal of Physical Anthropology
and Saitou, 1997; Hammer et al., 2006). More recently, ancient DNA analysis of Jomon period skeletal remains from
Hokkaido indicate that the Pleistocene ancestors of Jomon
people migrated to the Japanese Islands from Northeast
Asia (Adachi et al., 2009).
There is some disagreement regarding the use of the
term ‘‘forager’’ to categorize the subsistence economies of
Jomon people (Imamura, 2006; Underhill and Habu,
2006). It is, however, important to point out that the
term ‘‘forager’’ does not describe a static subsistence
framework. In fact, many ‘‘foraging’’ societies domesticate considerable numbers of plant species and are characterized by variation in mobility and social complexity
(Binford, 1981; Harris, 1989; Smith, 2000). In this sense,
Jomon people are encompassed within the foraging subsistence spectrum (Ikawa-Smith, 1986; Tsude, 2001;
Matsui and Kanehara, 2006; Underhill and Habu, 2006).
Broad consumption of cariogenic cultigens is reported
during the Jomon period, despite variation in resource
availability (Turner, 1979; Fujita, 1995; Todaka et al.,
2003; Temple, 2007a). Spikes in carious tooth frequencies
are observed following climatic oscillations around 4300
BP indicating a shift in diet across eastern and western
Japan (Fujita, 1995; Temple, 2007a). Dietary changes
among prehistoric Jomon people are related to the ubiquitous exploitation of a cariogenic food source such as
taro or yams and resulted in elevated caries prevalence
among Late/Final compared to Middle Jomon people
(Fujita, 1995; Temple, 2007a) with exceptions reported
on Hokkaido Island (Oxenham and Matsumura, 2008).
Increased consumption of these products did not precipitate agricultural economies per se, as the types of energy
expenditure, social organization, and caries prevalence
expected in agricultural economies are not observed until
the subsequent Yayoi period (Sanui, 1960; Inoue et al.,
1986; Imamura, 1996a,b; Oyamada et al., 1996; Tsude,
2001; Todaka et al., 2003; Temple and Larsen, 2007).
Yayoi
Yayoi period (2500–1700 BP) were the first wet rice dependent communities in the Japanese Islands (Imamura,
1996a, b). Cranial and dental size and shape varied
between Jomon and Yayoi people in association with
environment and gene flow (Brace and Nagai, 1982; Mizoguchi, 1986; Hanihara, 1991; Turner, 1992; Nakahashi,
1993; Pietrusewsky, 2006). Yayoi period agriculturalists
were the descendents of people from modern-day Korea
or northern China who migrated to Japan and interbred
to varying degrees with indigenous Jomon foragers
around 2500 BP (Brace and Nagai, 1982; Hanihara,
1991; Nakahashi, 1993; Omoto and Saitou, 1997; Hammer et al., 2006; Pietrusewsky, 2006). Migrants from
continental Asia during the Yayoi period introduced wet
rice agriculture to the Japanese Islands (Imamura,
1996a,b; Hudson, 1999; Tsude, 2001).
The earliest dates for migrant arrival correspond with the
earliest dates for wet rice production in Northern Kyushu
and Southern Honshu Island, specifically those obtained
from the Doigahama, Itatzuke, and Notame sites (Imamura,
1996b). Tool types and irrigation systems that closely resemble those found at farming sites from southern China and
Korea also suggest that wet-rice agriculture was brought to
Japan by migrant people (Tsude, 2001). For example, the
paddy field excavated at the Itatzuke site is remarkably
similar to wet rice fields found in southern China and North
Korea between 4000 and 3000 BP (Tsude, 2001).
115
JOMON AND YAYOI STRESS
Significant energy expended on the care of domesticated plants is recorded during the Yayoi period in the
form of large-scale agricultural ecosystems based around
wet rice farming (Imamura, 1996b; Hudson, 1999; Tsude,
2001). Precipitous increases in carious tooth frequencies
follow this economic shift and bear further testament to
the importance of carbohydrate-heavy crops during the
Yayoi cultural horizon (Sanui, 1960; Inoue et al., 1986;
Oyamada et al., 1996; Todaka et al., 2003; Temple and
Larsen, 2007). This increase in caries prevalence is associated with the consumption of a starch-heavy carbohydrate, variation in food preparation techniques (i.e., boiling and processing rice), and increased malocclusion
among Yayoi compared to Jomon people (Temple and
Larsen, 2007). General variation in cranial morphology
between historic Japanese compared to Yayoi people suggest in situ behaviorally-related changes in morphology
after the arrival of these migrants to the Japanese
Islands (Mizoguchi, 1986).
MATERIALS
All bioarchaeological data (LEH, CO) were collected by
the author (DHT). Human skeletal remains recovered
from eight Jomon period sites (Fig. 1; Table 1) represent
the foraging component of this study. These sites are
dated from the Middle (5000–4000 BP), Late (4000–3300
BP), and Final (3300–2500 BP) Jomon period and
include remains from the eastern and western regions of
Honshu island. Human skeletal materials recovered
from four Yayoi period archaeological sites represent the
agricultural component of this study (Fig. 1; Table 1).
These sites yielded the largest numbers of skeletal
remains for all early agricultural sites in the Japanese
Archipelago. Wet rice dependence among these groups is
supported by archaeological and isotopic studies (Imamura, 1996a,b; Chisholm and Koike, 1999). All sites
were dated using pottery chronology and/or radiocarbon
methods. The use of pottery chronology is an accurate
method to estimate site occupations in prehistoric Japan
because these methods have achieved significant precision over many years of description and comparison to
absolute dating methods (Aikens, 1995; Imamura, 1996a;
Habu, 2004; Tanaka et al., 2005).
This study compares Yayoi assemblages recovered
from western Japan to Jomon assemblages recovered
from eastern Japan. Eastern Yayoi skeletal collections
are fragmentary and small in sample size due to highly
acidic soil. Those in western Japan were preserved in
sand-dunes, while those from eastern locations were
interred in soil (Imamura, 1996a). Soil in Japan has a
low pH level and is responsible for fragmentation and
disintegration of skeletal materials interred outside of
shell mounds or sand dunes (Imamura, 1996a).
Comparing these two groups could be problematic as
these comparisons may not measure a ‘‘direct’’ biological
impact of wet rice agriculture in eastern Japan. These
comparisons are, however, important because Yayoi samples from western Japan represent the earliest wet rice
farmers in the Japanese archipelago. In this sense, comparisons between eastern Jomon communities with the
earliest wet rice farmers from western Japan will
enhance knowledge of the more immediate differences/
impacts in stress associated with this transition.
Fig. 1. Map indicating site locations. Jomon: 1) Nakazuma,
2) Kitamura, 3) Yoshigo, 4) Hobi, 5) Inariyama, 6) Tsukumo, 7)
Ota, 8) Yosekura; Yayoi: A) Koura, B) Doigahama, C) Kanenokuma, D) Nagaoka.
METHODS
Age estimation
CO prevalence was compared between age groups. Age
was estimated on the basis of long bone epiphyseal
fusion (Scheuer and Black, 2000) tooth development/
eruption stages (Smith, 1991), and tooth wear scores
obtained from premolar and molar teeth (Scott, 1979).
Samples were then divided into two age groups based on
these estimations. Age Group 1 includes individuals
younger than 15 years, while Age Group 2 includes individuals aged 15 years and older.
LEH defects
LEH defects were recorded as deficiencies in enamel
thickness appearing as horizontal grooves or pits on
mandibular and maxillary anterior, permanent one of
these teeth for both adults and subadults with at least
one tooth. LEH defect presence was determined by macroscopic observation aided by the use of a magnifying
glass (103), natural fluorescent lighting, and a 100-W
Toshiba desk lamp. Identification of LEH defects follow
Skinner et al. (1995) and Guatelli-Steinberg (2003),
where adjacent perikymata were compared to possible
LEH defects to prevent confusing normal variation in
tooth morphology with disrupted enamel production. The
minimum limit for LEH defect identification was set at
the point where horizontal grooves appeared larger than
adjacent perikymata under 103 magnification. The maximum limit includes LEH defects that were clearly visible as furrows of enamel deficiency in the absence of
magnification. Methods for documenting intraobserver
error in LEH defect recognition are reported in Temple
(2007a,b). These methods determined a level of ‘‘substantial agreement’’ between two rounds of observation.
American Journal of Physical Anthropology
116
D.H. TEMPLE
TABLE 2. Overall prevalence of anterior, permanent teeth with
LEH defects
TABLE 3. Percentages of individuals with at least one anterior,
permanent tooth expressing an LEH defect
Group
N Teeth
% LEH
(Y:) P a
Group
N individualsa
% LEH
(Y:) P Yayoi (Y)
Eastern Jomon (EJ)
Western Jomon (WJ)
965
559
495
30.3
36.8
56.7
–
0.05
0.001
Yayoi (Y)
Eastern Jomon (EJ)
Western Jomon (WJ)
182
164
122
63.1
48.2
64.8
–
0.05
NSb
a
Probability values for Yayoi compared to eastern and western
Jomon.
It is important to note that LEH defects are most
objectively identified by increased perikymata spacing
using microscopic measurements (Hillson and Bond,
1997). Since this study relies on macroscopic identification, the prevalence of LEH defects reported here represents a minimum estimate. LEH prevalence is first
reported using individual and overall frequencies. These
frequencies were calculated using the following methods:
Number of anterior, permanent teeth with at least one
LEH defect divided by the total number of observed anterior, permanent teeth (overall prevalence); number of
individuals with at least one observable LEH defect on
an anterior, permanent tooth divided by number of individuals with at least one anterior, permanent tooth (individual prevalence).
LEH defects arising from disrupted physiological homeostasis following severe traumatic injuries may bias
interpretations by mimicking hypoplastic lesions normally attributable to stress (Hillson, 1996). LEH defects
associated with traumatic injuries are rare in archaeological contexts (Goodman and Rose, 1991). Nevertheless, LEH defects associated with systemic stress are
possible to differentiate from those arising as a consequence of physical trauma by chronological matching:
LEH defects associated with systemic stress are observable at similar chronological positions on tooth antimeres, whereas trauma-induced LEH defects are generally observed on isolated teeth (Hillson, 1996). Antimere
refers to side-specific identical structures in bilaterally
symmetric organisms (e.g., right and left mandibular
canines). In an attempt to offset the potential for including trauma-induced LEH defects in the study, LEH
defect prevalence on maxillary first incisor (MxFI) and
mandibular canine (MaC) tooth antimeres were calculated. MxFI and MaC teeth were selected in association
with previous observations that suggest these teeth are
most susceptible to LEH defect formation (Goodman and
Armelagos, 1985). Numbers of mandibular canine (MaC)
and maxillary first incisor (MxFI) antimeres with at
least one observable LEH defect on both teeth divided by
the total number of observed MaC and MxFI antimeres,
respectively were used to calculate the prevalence of
antimeres affected by LEH defects.
Cribra orbitalia
CO lesions were identified using a 103 magnifying
lens under florescent lighting and a 100-W desk lamp.
CO was identified as sieve-like lesions on the orbital
roof. The presence of marrow hyperplasia through the
orbital cortex and/or remodeling on the borders of sievelike lesions helped differentiate this condition from postmortem damage. CO was scored following methods
reported by Steckel et al. (2002) and described by Temple
(2007b). Prevalence of this condition was compared as
the total number of individuals with at least one orbital
American Journal of Physical Anthropology
a
Number of individuals with at least one anterior, permanent
tooth.
b
Does not reflect a statistically significant result compared to
Yayoi samples.
roof with evidence of CO divided by the total number of
individuals with at least one orbital roof.
Statistical methods
The G-statistic with continuity correction is a more
conservative version of the chi-square test in assessing
the independence of nominal data (Sokal and Rohlf,
1995). The G-statistic with continuity correction compares the goodness-of-fit between observed and expected
cell frequencies and corrects for greater than expected
Type I errors (Sokal and Rohlf, 1995). The G-statistic is
applied to data where the observed minus expected cell
frequencies are greater than the expected cell frequencies or studies that rely on limited sample sizes—small
samples conflate the numerator in the chi-square calculation and produce unusually large degrees of difference
between data sets (Sokal and Rohlf, 1995). G-tests for independence are employed by previous studies using similar sources of data (Temple, 2007a; Temple and Larsen,
2007).
RESULTS
LEH defects
Overall prevalence of teeth with at least one observable LEH defect is significantly greater among eastern
(G 5 6.9; P 0.05) and western (G 5 95.6; P 0.001)
Jomon foragers compared to Yayoi agriculturalists (Table
2). G-values for the overall prevalence of anterior, permanent teeth with at least one LEH defect are elevated
for the western Jomon and Yayoi comparison in relation
to a 26% difference in teeth affected by LEH defects.
Differences in the frequencies of anterior, permanent
teeth affected by LEH defects between eastern Jomon
and Yayoi samples are less extensive at 6%.
Eastern Jomon foragers have significantly fewer individuals with at least one anterior, permanent tooth
affected by at least one LEH defect compared to Yayoi
agriculturalists (G 5 7.91; P 0.05) (Table 3). No significant differences in individuals with at least one anterior, permanent tooth affected by at least one LEH defect
are observed between the western Jomon and Yayoi samples (G 5 0.077).
No significant differences are observed in MxFI antimeres affected by LEH defects between the eastern
Jomon and Yayoi samples (G 5 3.2), while significantly
greater frequencies of MxFI antimeres affected by LEH
defects are observed among western Jomon compared to
Yayoi groups (G 5 5.5; P 0.05) (Table 4). No significant
difference in MaC antimeres affected by LEH defects are
observed between the eastern Jomon and Yayoi samples
(G 5 0.644). Significantly greater frequencies of MaC
antimeres are affected by LEH defects among western
Jomon compared to Yayoi people (G 5 7.8; P 0.05).
117
JOMON AND YAYOI STRESS
TABLE 4. Percentage of antimeric tooth pairs expressing LEH defects on both teeth
Group
N MxFI antimeresa
%LEHb
(Y:) P N MaC antimeresc
% LEH
(Y:) P Yayoi (Y)
Eastern Jomon (EJ)
Western Jomon (WJ)
77
47
28
35.1
21.2
60.7
–
NS
0.05
76
23
39
34.2
56.5
61.5
–
NSd
0.01
a
Number of maxillary first incisor antimeres.
Percentage of antimeres expressing LEH defects.
c
Number of mandibular canine antimeres.
d
Does not reflect a statistically significant result compared to Yayoi samples.
b
Several significant differences in the prevalence of teeth
affected by LEH defects between Yayoi and western
Jomon people support the first hypothesis of this study.
Few differences in teeth affected by LEH defects
between Yayoi and eastern Jomon people confirm the
second hypothesis.
Cribra orbitalia
TABLE 5. CO prevalence by age group and time period
Age group 1a
Jomon
Yayoi
Age group 2b
Jomon
Yayoi
a
Comparisons of CO prevalence are reported for Age
Groups 1 and 2 in Table 5. CO prevalence is not significantly different between the Middle to Final Jomon and
Yayoi agriculturalists from Age Group 1 (G 5 0.013) or 2
(G 5 0.014). These results are consistent with the third
hypothesis of this study that predicted similar frequencies of CO would be observed between Jomon and Yayoi
period people.
DISCUSSION
LEH defect prevalence
Several significant differences in the prevalence of
teeth affected by LEH defects were observed between
western Jomon and Yayoi samples. Assuming a decline
in stress between the western Jomon and Yayoi samples,
these results may be related to variation in resource
availability and nutritional quality. LEH defects reflect
inadequate intake of proteins, vitamins, and iron (Wolbach and Howe, 1933; Mellanby, 1939; Schour et al.,
1944). Poor intake of these nutrients is associated with
atrophy of the enamel organ (Wolbach and Howe, 1933;
Schour et al., 1944) and damage to the Tomes’ process
(enamel producing organ) of ameloblasts (Witzel et al.,
2006). The enamel organ is a condensation of cells that
differentiate into ameloblasts (Ten Cate, 1998). Nutritional deprivation causes enamel organ atrophy through
vasoconstriction (Mellanby, 1939; Schour et al., 1944).
Poor organizational capacity for the differentiation of
ameloblasts and odontoblasts from the enamel organ
combined with LEH defect formation follows (Mellanby,
1939; Schour et al., 1944). Tomes’ process damage
impairs the capacity for the ameloblast to produce
enamel (Witzel et al., 2006) and also results in the production of LEH defects.
Similar findings are reported among children in developing countries. Prevalence of children in Guatemala
with teeth affected by LEH defects and overall frequencies of teeth affected by LEH defects were increased
among groups that lacked adequate nutritional supplementation (i.e., protein and vitamin fortifications)
(Goodman et al., 1991; May et al., 1993). These findings
suggest that poor consumption of essential nutrients is
associated with the formation and greater prevalence of
LEH defects.
b
N individuals
% Cribra
24
33
50.0
50.1
209
111
8.6
8.8
Age Group 1 includes individuals less than 15 years.
Age Group 2 includes individuals aged 15 years and greater.
Teeth and individuals with LEH defects are also
observed in great prevalence from a variety of contexts
with presumably elevated levels of malnutrition, and
especially, regions with resource limitations such as famine-era China and the Protohistoric American Southwest
(Zhou and Corruccini, 1998; Stodder et al., 2002).
Hunter-gatherer people from Southwest Asia have elevated LEH defect frequencies for teeth and individuals
in association with seasonal food scarcity (Lukacs and
Pal, 1993). These findings suggest that nutritionally
inadequate food and seasonal scarcity were responsible
for the elevated prevalence of LEH defects among western Jomon compared to Yayoi people.
It is also possible that increased population density
during the Late/Final Jomon period may have added
pressure on resource availability in western Japan. Population density declined in eastern and central Japan
during the Late to Final Jomon period; western Japan
did, however, experience significant increases in population density during this same time period (Koyama,
1978). This population expansion appears to be part of a
broader response to climatic cooling, where migrations
into northern and western Japan combined with dietary
change are noted, rather than increased reproductive
output within a stressed community (Hudson, 1999;
Habu, 2004; Temple, 2007a).
Age compositions of deer hunted by Jomon people
changed to include large quantities of younger animals
during the Late/Final Jomon period suggesting that
increased population density was associated with overuse of environmental resources (Koike and Ohtaishi,
1985; Koike, 1992). Similar trends are observed in gastropod exploitation patterns, where range of shell
heights expanded to include smaller organisms during
the Late/Final Jomon period (Koike, 1986). Finfish consumed by western Jomon people were subjected to seasonal depletion (Kobayashi, 2005), while fallback foods
were nutritionally poor (Akazawa, 1986). This suggests
that increased population density during the Late/Final
Jomon period in western Japan may have encroached on
the carrying capacity of an already limited environment
and exacerbated nutritional status.
American Journal of Physical Anthropology
118
D.H. TEMPLE
In contrast, Yayoi people were reliant on a predictable
and renewable source of food in the form of wet rice
economies (Imamura, 1996a,b) and consumed nutrient
rich fallback foods (Chisholm and Koike, 1999; Takahashi, 2009). The earliest form of wet rice produced in prehistoric Japan was resistant to cold weather and able to
survive drastic seasonal shifts in temperature (Tsude,
2001). In addition, the form of paddy-field agriculture
imported to the Japanese Islands was at an advanced
stage, having evolved in Northeast Asia over 3,000 years
before arriving in this region (Tsude, 2001). Yayoi people
also supplemented this diet with maritime resources
(Chisholm and Koike, 1999; Takahashi, 2009) and even
cultivated various species of freshwater fish (Nakajima
et al., 2009). It is, therefore, likely that the lower prevalence of teeth with LEH defects among Yayoi people is
attributable to resource stability and nutritional quality.
Similarity in systemic stress prevalence between the
Yayoi and eastern Jomon people is associated with exploitation of consistently available subsistence bases and
wide dietary breadths. Hypotheses by Yesner (1994) predict that resource abundance and dietary breadth are
associated with systemic stress patterns among prehistoric foragers and incipient agriculturalists. For example, patterns of LEH defects in Southeast Asia indicate
continuity between foragers and agriculturalists in association with continued broad-spectrum subsistence
economies following the transition to wet rice agriculture
(Pietrusewsky and Douglas, 2002a,b; Douglas and Pietrusewsky, 2007). Eastern Jomon people relied on a wide
dietary breadth with consistently available, calorically
dense resources (Akazawa, 1999). Yayoi people continued
this trend, incorporating maritime and terrestrial game
into agricultural economies (Terasawa and Terasawa,
1981; Chisholm and Koike, 1999; Nakajima et al., 2009).
To be certain, Jomon people from eastern Japan and
Yayoi groups relied on different foods and resource procurement/production systems. Both groups were, however, active participants in economies characterized by
intensive subsistence behavior and the exploitation of
calorically dense resources.
Cribra orbitalia and parasite infection
Similar frequencies of lesions associated with CO are
observed between Jomon and Yayoi samples in both age
groups. Prevalence of CO was originally thought to form
a straightforward relationship with diet, specifically iron
status (El-Najjar et al., 1976). These relationships were
later questioned on the basis of various parasites found
in the coprolites of prehistoric North Americans (Reinhard, 1990). Cranial porosity also reached significant
levels among maritime foragers from the California coast
(Walker, 1986) and densely populated desert agriculturalists (Walker, 1985) further indicating that dietary factors are only loosely associated with CO. These lesions
are, in populous maritime and agricultural environments, associated with iron deficiency anemia stemming
from parasitic infection, prolonged weaning due to poor
resource availability, and diarrhea caused by the use of
contaminated water supplies (Walker, 1985, 1986, 2006).
A recent survey does, however, suggest that iron deficiency anemia alone will not produce the hypertrophic
marrow expansion observed in cases of CO and that
these lesions are more likely attributable to other nutritional deficiencies or infectious conditions of the eye orbit
(Walker et al., 2009). Primary diseases contributing to
American Journal of Physical Anthropology
the development of CO include scurvy, rickets, megaloblastic anemia (MA), and trachoma (Schultz, 2001;
Wapler et al., 2004; Walker et al., 2009). It is difficult to
differentiate these conditions without histological
(Schultz, 2001) or radiographic (Ortner, 2003) sections.
It is, however, possible to ‘‘infer’’ specific conditions associated with CO based on environmental context and
lesion distribution (Larsen and Sering, 2000).
Rickets is a pathological condition associated with a
lack of vitamin D intake (Ortner, 2003). Humans cannot
independently synthesize vitamin D and must obtain
this nutrient from environmental surroundings. Vitamin
D is available in a variety of foods, but in most cases,
humans directly synthesize adequate amounts of this
nutrient from sun exposure (Ortner, 2003). Under circumstances where sun exposure is negligible, for
instance among indigenous foragers of Siberia and
Northern North America, consumption of maritime products provide an adequate source of vitamin D (Jablonski
and Chaplin, 2000). The climate of Japan is temperate
(Honshu Island and regions south) and continental
microthermal (Hokkaido) (Fukui, 1977). These regions
experience adequate sunlight for vitamin D synthesis
outside the context of industrialized or urban environments (Lips, 2007). This suggests rickets arising from dietary/climatic factors was an unlikely contributor to the
observed patterning of CO lesions. Rickets is, however,
observed in cases of parasite infection (Walker et al.,
2009), and therefore, cannot be effectively ruled out as a
contributor to these lesions.
Scurvy is another diagnostic option for these lesions.
Scurvy is a pathological condition attributed to insufficient levels of vitamin C (Aufderheide and RodriguezMartı́n, 1998). Considerable levels of vitamin C are
found in citrus fruits, vegetables, and shellfish (Rivers,
1987). Significant consumption of shellfish as well as a
wide variety of vegetables is reported among Jomon people (Koike, 1986; Crawford, 1992, 2006; Matsui and
Kanehara, 2006). Some level of caution is, however, necessary in ruling out scurvy as a diagnostic option. Surprisingly elevated frequencies of scurvy were observed in
early historic Florida—a region with abundant access to
citrus fruits (Ortner et al., 2001). Underlying infection
by parasites and infant diarrheal disease may also significantly deplete vitamin C and result in scurvy (Walker
et al., 2009). As a consequence, scurvy cannot be effectively rejected as a diagnostic option for the observed
lesions.
The marrow hyperplasia of CO is also attributable to
megaloblastic anemia (MA) (Walker et al., 2009). MA is
associated with inhibited DNA production in red blood
cells and produced by poor levels of vitamin B-12 or folic
acid (Antony, 1995). This condition is rare in adults, but
children lacking significant stores of vitamin B-12 are
particularly susceptible to the disease as are individuals
exposed to parasitic infection (Walker et al., 2009). This
suggests that MA also contributed to the patterning of
CO observed by this study.
It is important that parasites specific to prehistoric Japan be considered as contributing factors to cranial porosity induced by MA, rickets, or scurvy. These conditions include but are not limited to schistosomiasis, trichuriasis, roundworm (Ascaris), and Diphyllobothrium
infections. In Asia, schistosomiasis is a disease associated with infection by the cercariae of Schistosoma japonica that survive on snails living in brackish water,
depart this vector during daylight hours, penetrate
119
JOMON AND YAYOI STRESS
human skin, and disseminate to various organ systems
(Mascie-Taylor and Mohamed, 1995). Eggs of Schistosoma japonica are re-released into surrounding environments by urination, mature into cercariae, reattach to
snails, and perpetuate new rounds of infection. Environmentally, Schistosoma japonica infections increase in
concert with the square acreage of wet rice fields in rural China suggesting a link between paddy field agriculture and schistosomiasis (Yi-Xin and Manderson, 2005).
Schistosomiasis inducing parasites are also spread
through contact with or consumption of unsanitary
water (Mascie-Taylor and Mohamed, 1995).
Trichuriasis is a pathological state caused by the consumption of eggs laid by Trichuris trichiura or Trichocephalus trichiuris in dry areas, specifically those found
associated with stored rice and other grains (Stephenson
et al., 2000). The disease is also related to accidental
ingestion of soil contaminated by the eggs of Trichuris
(Stephenson et al., 2000). These eggs hatch in the small
intestine, with larvae and mature worms moving into
various regions of the digestive system (Crompton and
Nesheim, 2002). Subsequent spread through contact
with stool is reported (Stephenson et al., 2000; Crompton
and Nesheim, 2002).
Roundworms are another potential contributor to
nutritional depletion and CO distribution among the
Jomon and Yayoi people. Parasitic roundworms include
members of the genus Ascaris. Ascaris infection occurs
when pigs consume the meat of infected rats and
humans consume the meat of infected pork, especially in
circumstances where meat is raw or undercooked (Aufderheide and Rodriguez-Martin, 1998). Immature larvae
are deposited into the small intestine with later migration into the large intestine by mature parasites. Mature
parasites then reproduce in the large intestine, depositing larvae into the intestinal mucosa.
Finally, infection by the Diphyllobothrium genus of
maritime parasite is reported in a variety of coastal contexts (Reinhard, 1990; Bathurst, 2005a,b). In Japan,
Diphyllobothrium latum and nihonkaiense infect hosts
following consumption of raw or undercooked fish, with
mature organisms migrating to the small intestine
(Scholtz et al., 2009).
Parasite loads are particularly heavy among maritime
foragers, where contact with contaminated, stagnant
water and consumption of undercooked fish provide vectors for infection and reinfection (Reinhard, 1990; Bathurst, 2005a,b; Walker, 2006). Jomon people occupied
coastal, populous environments and procured maritime
resources on the open water (Koyama, 1978; Imamura,
1996a). Fishing behavior, maritime resource consumption, and exposure to contaminated water supplies likely
acted as a primary source of Diphyllobothrium and
Schistosoma infection. Jomon people also consumed pig
meat (Hongo et al., 2006), and as a consequence, were
likely exposed to Ascaris parasites. In addition, Jomon
people stored foods including various acorns and walnuts
in underground storage units (Imamura, 1996a). Food
storage may have placed Jomon people at risk for infection by Trichuris. In fact, whipworms (Trichuris) were
observed in coprolites from the Jomon period Sannai
Maruyama site (Matsui et al., 2003). The totality of
these findings indicate that CO patterning among Jomon
people reflect nutrient deficiencies brought about by parasite infection, with specific reference to Trichuris species.
Yayoi people stored wet rice as dry grain (Imamura,
1996a,b), continued to rely on maritime resources, and
consumed pigs (Aikens and Akazawa, 1992; Chisholm
and Koike, 1999). These behaviors likely exposed Yayoi
people to Ascaris, Diphyllobothrium, Schistosoma, and
Trichuris infection. It is also possible that infection by
parasites such as Schistosoma japonica were transmitted
through contact with stagnant water in wet rice fields.
More specifically, however, whipworms (Trichuris) and
roundworms (Ascaris) were found in coprolites recovered
from the Ikegami-Sone Yayoi site (Matsui et al., 2003).
This suggests that the patterning of CO observed among
Yayoi people was associated with parasite infection, particularly Trichuris and Ascaris species.
It is also important to consider trachoma as a possible
contributor to these lesions (Wapler et al., 2004; Walker
et al., 2009). Trachoma is an infectious disease of the eye
caused by direct contact with the bacteria Chlamydia
trachomitis (Wright et al., 2008). Elevated frequencies of
trachoma are reported in dense populations lacking
access to sanitary bathing and drinking facilities as well
as those where young people lack access to clean water
for proper facial cleansing and sleep near infected individuals (Wright et al., 2008).
Access to sanitary bathing and drinking facilities were
a major environmental hazard for prehistoric coastal
communities, particularly those with dense populations
(Walker, 2006). Both Jomon and Yayoi people occupied
regions of high population density (Koyama, 1978). Poor
sanitation among these groups is indicated by reports of
fecal material within water sources around settlements
(Matsui et al., 2003). In this sense, both Jomon and
Yayoi people occupied environments where trachoma
was a likely environmental hazard and an additional
contributor to the CO lesions observed by this study.
Stress and the agricultural transition
The results presented here differ from previous
research addressing patterns of systemic stress during
the agricultural transition (i.e., Cohen and Armelagos,
1984; Larsen, 1987, 1995, 1997, 2002, 2006; Cohen and
Crane-Kramer, 2007), but are consistent with reports
from Southeast Asia (Oxenham, 2000; Domett, 2001; Pietrusewsky and Douglas, 2002a,b; Domett and Tayles,
2007; Douglas and Pietrusewsky, 2007). A general
decline/continuity in systemic stress is noted with regard
to prevalence of teeth with LEH defects, while CO frequencies remained static. Two major reasons for these
systemic stress patterns are important to note. Wet rice
agriculture arrived in Japan as a fully functioning subsistence strategy and was supplemented by a sophisticated system of maritime exploitation. The development
of agricultural ecosystems implies a fairly long-term process of human/environmental interaction with early systems subjected to failure due to climatic or other environmental fluctuation (Harris, 1989, 1996). The earliest
wet rice fields in Japan best resemble those from China
and have significantly more complex features than the
earliest paddy sites such as Caoxieshan (6000 BP) (Imamura, 1996a,b; Tsude, 2001). In fact, Yayoi paddy fields
post-date the earliest development of wet rice paddies in
China by 3,000 years (Takahashi, 2009) and exemplify
modified versions of these earlier sites (Imamura, 1996b;
Tsude, 2001). It is, in this sense, likely that Yayoi period
agriculturalists did not experience stressors associated
with poor control over environmental resources. Instead,
these early agricultural people enjoyed the benefit of a
well developed subsistence system. It should be noted
American Journal of Physical Anthropology
120
D.H. TEMPLE
that systemic stress experienced as a consequence of
introducing this behavioral strategy into new landscapes
may have been experienced, though stress prevalence
among Yayoi people still did not exceed levels reported
for eastern or western Jomon people.
In addition, Yayoi period agriculturalists continued to
exploit maritime products following the agricultural
transition. Maritime resources provide an excellent
source of nutrition, particularly when mixed with cereal
products (Layrisse et al., 1968; Larsen, 2003; Murphy
and Allen, 2003; Rivera et al., 2003). Prehistoric foragers
reliant on terrestrial mammals experienced an increase
in the frequency of teeth affected by LEH defects after
the transition to intensive plant-based agriculture, in
part due to dietary stress (Cook, 1980, 1981, 1984;
Lukacs, 1992; Larsen et al., 2002; Hutchinson et al.,
2007).
In contrast to dietary shifts experienced during the agricultural transition in the New and Old World, there is
ample evidence suggesting continued reliance on the procurement of maritime resources among Yayoi people.
Similarities in fishing tool kits are noted between Jomon
people from eastern Japan and a number of Yayoi period
sites (Aikens and Akazawa, 1992; Imamura, 1996a,b;
Takahashi, 2009). Stable isotopic analysis of human
remains indicates that Yayoi people consumed greater
amounts of maritime products than early agricultural
people from North America (Chisholm and Koike, 1999).
Additionally, previously mentioned studies report evidence that Yayoi people actually cultivated some species
of fresh-water fish (Nakajima et al., 2009).
CONCLUSIONS
Jomon foragers from western Japan had significantly
greater frequencies of teeth with LEH defects than Yayoi
agriculturalists. Reduction in the prevalence of teeth
with LEH defects following the agricultural transition is
likely related to the introduction of a predictable, renewable subsistence base into western Japan combined with
a system of exploiting more nutritious fallback foods.
More specifically, Jomon foragers from western Japan
were reliant on calorically dense finfish, but consumed
nutritionally poor fallback foods. The introduction of wet
rice agriculture provided this region with an economic
base that was high yield, renewable, cold resistant, and
supplemented by maritime foods.
Similar frequencies of teeth with LEH defects were
observed between Jomon foragers from eastern Japan
and Yayoi agriculturalists. The similar prevalence of systemic stress observed between these two groups is attributable to the fact that eastern Jomon and Yayoi people
both had significant control over environmental resources and relied on nutritionally rich fallback foods that
included terrestrial mammals and maritime resources.
Finally, CO prevalence between the two groups
remained stable. Both Jomon and Yayoi people were
exposed to environments that were hospitable to organisms such as Schistosoma japonica, Trichuris, Diphyllobothrium, and roundworms (Ascaris). Trichuris and
Ascaris parasites were, in fact, observed in Jomon and
Yayoi coprolites. In addition, both groups occupied environments where exposure to bacteria such as Chlamydia
trachomitis was likely significant. This suggests parasite
induced malnutrition and bacterial infection was responsible for the observed pattern of CO among Jomon and
Yayoi people.
American Journal of Physical Anthropology
These results depart from general models of PostPleistocene human evolution that suggest increases in
systemic stress followed the agricultural transition. Two
primary reasons for the trend in Japan are reported.
First, wet rice agriculture was based on a well developed
system of paddy farming that evolved over 3,000 years
before arriving in the Japanese Islands. Second, Yayoi
people continued to rely on maritime products as a dietary source. In contrast, early agricultural people from
other regions of the globe relied upon newly developed
subsistence systems and nutritionally inadequate cultigens. It is also important to note that Jomon and Yayoi
people represent distinct biological groups with unique
migratory histories (see references above). Variation in
systemic stress between these groups may also represent
differences in genetic capacity to buffer against environmental perturbations (see: Hoover and Matsumura,
2008). Research addressing finite aspects of stress
including chronology, duration, and periodicity may further resolve this issue (see: Temple, 2008).
ACKNOWLEDGMENTS
Masato Nakatsukasa, Kazumichi Katayama, Naomichi
Ogihara, and Wataru Yano provided access to and assistance with the Jomon skeletal material housed at Kyoto
University. Gen Suwa, Souichiro Mizushima, and Aiko
Saso provided access to and assistance with the Jomon
skeletal material housed at the University Museum of the
University of Tokyo. Takahiro Nakahashi, Yoshiyuki
Tanaka, Shozo Iwanaga, Yuji Mizoguchi, and Kenji Okazaki provided access to and assistance with the Yayoi skeletal material housed at Kyushu University. Yoshitaka
Miyauchi and Reiko Oomi from Toride Maizobunkazai and
Masatsugu Hashimoto from Tokyo Dental College provided the access to and assistance with the Nakazuma
Jomon skeletal material. Tamotsu Kawasaki provided
access to and assistance with the Kitamura Jomon skeletal
material housed at the Nagano Historical Museum. Clark
Spencer Larsen, Paul Sciulli, Debbie Guatelli-Steinberg,
Sam Stout, and Kristen Gremillion, all from The Ohio
State University, provided initial support and important
comments on early versions of this work. Special thanks to
Takao Suzuki from the Tokyo Metropolitan Institute of
Gerontology for advisement and logistical support. Discussions with Soichiro Kusaka (Kyoto Univ.) provided new
perspectives on western Jomon diet, though any errors in
interpretation rest entirely with the author. Comments
from Chris Ruff and three anonymous reviewers greatly
improved the content of this manuscript.
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