ARTICLE IN PRESS

l
l
HOMO — Journal of Comparative
Human Biology 55 (2005) 263–281 www.elsevier.de/jchb

The people of Jabuticabeira II: reconstruction of the way of

life in a Brazilian shellmound
M.M.M. Okumuraa,, S. Eggersb
a
Laboratório de Estudos Evolutivos Humanos, Universidade de São Paulo, Brazil
b
Laboratório de Antropologia Biológica, Universidade de São Paulo, Brazil

Received 9 October 2003; accepted 25 October 2004

Abstract
Sambaquis are huge shellmounds built along almost the entire Brazilian coast between
8000 and 600 years ago. In the present article, 14 osteological markers from 89
individuals excavated at the Sambaqui Jabuticabeira II (2890755/2186760 BP) are
analyzed in order to reconstruct the population0 s health status and way of life. The present
palaeopathological findings (such as lower frequency of degenerative joint diseases in
legs, as compared to arms, and the rarity of traumas) together with archaeological
findings support the idea of nearby resource abundance and infrequent interpersonal
competition. The presence of auditory exostoses mainly in males corroborates
previous findings indicating the importance of marine resources. The low caries
frequency and the high degrees of dental wear point to a diet poor in cariogenic food,
and rich in abrasives such as sand, shell fragments and phytoliths. This suggests a broader
diet, based on marine protein as well as plants, than previously thought. The etiology of
cribra orbitalia could be explained by gastrointestinal parasites or other sources
of physiological stress. These parasites, in turn, could have led to higher frequencies
of infectious diseases, either by the debilitation of the immune system or by the direct
contact with infectious agents. Despite the periods of illness various individuals
experienced, the daily life among the builders of the Sambaqui Jabuticabeira II seems

Corresponding author. Tel.: 55 11 3091 77 25; fax: 55 11 3091 75 53.

E-mail address: okumuram@usp.br (M.M.M. Okumura).

0018-442X/$ - see front matter r 2004 Elsevier GmbH. All rights reserved.
doi:10.1016/j.jchb.2004.10.001
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to have been relatively easy due to the abundance and predictability of resources and the
paucity of violent traumas.
r 2004 Elsevier GmbH. All rights reserved.

Resumo

Sambaquis são sı́tios arqueológicos construı́dos em quase toda a costa brasileira

entre 8000 e 600 anos antes do presente (AP). Neste artigo, foram analisados 14
marcadores osteológicos de 89 indivı́duos exumados no Sambaqui Jabuticabeira II
(2890755/2186760 AP), a fim de obter informações acerca da qualidade de vida
desse grupo. Os achados paleopatológicos (tais como uma menor freqüência de
doenças degenerativas nas articulações dos membros inferiores em comparação aos
superiores e a raridade dos traumatismos), em associação com certas evidências
arqueológicas fornecem suporte à idéia de abundância e proximidade de recursos,
assim como uma baixa competição interpessoal. A presença de exostoses auditivas,
principalmente entre os homens, corrobora estudos prévios que indicam a
importância dos recursos marinhos. A baixa freqüência de cáries e os altos ı́ndices
de desgaste dental apontam para uma dieta pobre em alimentos cariogênicos e ricos
em abrasivos, como areia, fragmentos de conchas e fitólitos. Isso sugere uma dieta
mais ampla, baseada não somente em recursos marinhos como também em vegetais.
A cribra orbitalia nesse grupo seria explicada através da presença de fatores de
estresse, ligados à parasitoses gastrointestinais, que por sua vez, poderiam ser
responsáveis também por doenças infecciosas, como as freqüentes periostites.
Apesar dos perı́odos de saúde debilitada pelos quais muitos dos indivı́duos de
Jabuticabeira II passaram, a vida diária desse grupo não deve ter sido muito árdua,
devido à abundância e previsibilidade de recursos e a baixa competição interpessoal.

Introduction

Sambaquis are archaeological sites associated with populations that intensely

colonized the entire Brazilian coast, specially the Southern regions. The name given
to these sites originates from the tupi words ‘‘tamba’’ (mollusk) and ‘‘ki’’
(accumulation), thus meaning ‘‘shellmound’’ (Prous 1991).
These coastal populations lived from 8000 to 600 years ago (Lima et al 2001).
This long period of time and large area of occupation, associated with the huge
size of many of these sites, suggests that these populations were very well adapted
to the coastal environment. Because of their use for the extraction of lime, the
Portuguese colonists knew the Sambaquis already in the 16th century. But these
sites have only been scientifically studied since the 19th century (Lacerda 1885).
Although about 1000 of these sites have been catalogued and partially analyzed
until the present, there are only a few reports published in international journals
(Gaspar 1998).
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In early Sambaqui studies, two main ideas about their origin predominated. One
of these interpreted Sambaquis as natural structures formed by sea level decline
(Ilhering 1907). The other one stated that they were artificially formed by the
accumulation of food remains left over by prehistoric populations (Bigarella 1951).
However, the fact that some of the Brazilian Sambaquis are so huge (some sites
measure 30 m in height and several hundred meters in diameter) suggests that they
were not incidental structures, but rather the result of the intention to form a well-
visible construction (Gaspar & De Blasis 1992).
The presence of beautiful bone and lithic artifacts in the Sambaquis, along with
findings of recent zooarchaeological and stable isotope studies indicate that the
subsistence of these peoples was mainly based on fishing and gathering of molluscs
(Figuti 1992, 1993, 1994, 1999; Kneip 1994; De Masi 1999). This latter process would
have been the activity that led to the construction of the Sambaquis (De Blasis et al
1998).
The occurrence of pottery in Sambaquis, although used to define pre-ceramic and
ceramic periods (Beck 1974), is limited to a few pieces usually scattered around the
surface of the site, without any other cultural change and no burial associations.
These ceramic fragments might represent occasional trade with surrounding groups
(Gaspar 1996), and appear to indicate that pottery did not play a significant role in
their cooking technology, nor that pottery can be safely associated with high caries
indices (Fish et al 2000; Wesolowski 2000).
Although there are hypotheses that propose the existence of two or three
morphologically distinct populations within the Sambaqui culture (Imbelloni 1956/
1958; Neves 1988) some authors favor the occurrence of a morphological unity of
these groups (Mello e Alvim & Seyferth 1968/1969, 1971). However, more detailed
comparative morphological studies are necessary to test these hypotheses.
Apart from craniometrical studies, most of the research carried out on skeletal
remains is concentrated on the description of oral pathologies (Salles Cunha 1959,
1963a, b; Araujo 1969, 1970; Wesolowski 2000; Neves & Wesolowski 2002), as well
as cribra orbitalia and porotic hyperostosis (Mello e Alvim et al 1991; Mello e Alvim
& Gomes JC de 1992) in single Sambaquis.
Recently, archaeological excavations in the Sambaquis have been more systematic,
and permit the meaningful analysis of population history at specific Sambaquis sites.
The present article focuses on the description of the health status of 89 individuals
buried in the shellmound Jabuticabeira II based on an assessment of 14 osteological
markers.

Archaeological context of Sambaqui Jabuticabeira II

The material reported in this article was excavated from a Sambaqui called
Jabuticabeira II. The excavation of this site is part of a multidisciplinary project
called ‘‘Settlement patterns and formation of Sambaquis from the Santa Catarina
state’’. Its main objective is the systematic approach of a whole series of Sambaquis,
localized around the lake Camacho (Fig. 1), at the southern coast of Brazil, in order
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Fig. 1. Map showing Brazil, the distribution of Sambaquis () on almost the entire coast, the
lake Camacho and the Jabuticabeira II site (arrow).

to obtain understand their construction processes (Gaspar et al 1999; Fish et al

2000).
Besides Jabuticabeira II, there are 22 Sambaquis built between 2000 and 4000
years ago (Fish et al 2000) that are scattered around this lake. In the past this group
of Sambaquis was significantly closer to the coast, due to the decrease in sea level
that began 5100 BP (Bissa et al 2000). Thirty-nine radiocarbon dates for
Jabuticabeira II indicate that it was constructed between 2890755 and 2186760
BP (Laboratory of Isotope Chemistry, Department of Geosciences, University of
Arizona) or over a period of about 700 years (Fish et al 2000). What remained of
this site after mining activities measures approximately 400 m (NW–SE) by 250 m by
6 m height.
The osteological material from Jabuticabeira II derives from profiles as well as
traditional horizontal excavations, which reveal a long and continuous depositional
history involving recurrent burial and mortuary activities and the lack of habitation
structures. The high number and great density of burials, each of which is often
covered over by a layer of sand and shells, suggest that the utilization of this
Sambaqui as cemetery was linked to its construction process (Fish et al 2000).
The burials are distributed over most of the locations excavated, and are
accompanied, in the majority of cases, by hearths, post-holes, as well as lithic
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artifacts, beads, some evidence of food (mainly fish), red pigment and different
ways of interment indicating elaborate funeral rituals (Edwards et al 2001).
Based on the ratio of burials per cubic meter, Fish et al (2000) estimated
an astonishing number of approximately 40 000 persons that must have been
buried during the construction of Jabuticabeira II. Even if this is an overestimate,
it suggests a large number of people living nearby the Sambaqui, sharing a
common social identity and getting together for the construction of this mortuary
monument.

Material and methods

The material described here consists of the remains of a minimum number of 89

individuals excavated from the site Jabuticabeira II during three field campaigns in
1997, 1998 and 1999. The state of conservation of some of the individuals is far from
being ideal. In many cases there are only a few skeletal elements. The curation was
carried out in the laboratory supervised by one of us (SE) according to
internationally accepted criteria.
The minimum number of individuals (MNI) was estimated according to White
(1991). The age at death of the juveniles was based on the degree of epiphiseal
closure (Brothwell 1981), on tooth formation and eruption (Ubelaker 1989) and on
the size of the long bones (Johnston 1962). The adult individuals were sexed based on
pelvic and cranial morphology (Buikstra & Ubelaker 1994), and their age at death
was estimated based on the morphology of the pubic symphysis (Brooks & Suchey
1990) or on the degree of cranial suture closure in cases where the pelvis was absent
(Meindl & Lovejoy 1985). If neither was possible, the individuals were simply
classified as adults.
The estimation of adult stature was carried out based on the maximal length of
complete long bones and on regression formulae for prehistoric Amerindian
populations (Sciulli & Giesen 1993).
The diagnosis of oral and general palaeopathology followed acknowledged criteria
(see below) and was carried out macroscopically, since this is the only method that
allows comparisons with reports on other Sambaquis. Due to the fragmentary
character of the sample, not all individuals were included in every analysis. Therefore
we used the frequency of pathologies per tooth, socket or anatomical unit. For oral
pathology analyses, only individuals presenting more than 50% of teeth or sockets
were included for the estimation of frequency per person, whereas all teeth/sockets
available were considered for prevalence per tooth/socket. Periodontal disease and
dental calculus were recorded as present or absent. Molar dental wear was analyzed
according to Brothwell (1981) and anterior dental wear according to Smith (1984).
Palaeopathological analyses were performed on the criteria established by Ortner &
Putschar (1981) and Aufderheide & Rodrı́guez-Martı́n (1998), and recorded as
present or absent per anatomical unit. The oral, cranial and postcranial pathologies
were evaluated quantitatively, whereas qualitative evaluations were carried out for
infectious disease only.
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Statistical analyses were performed on the SPSS program for Windows in order to
obtain the degree of significance in w2 tests aimed at verifying the differential
frequency of certain traits in subgroups of the population.

Results

Sex and age at death

The estimation of the MNI yielded a total of 89 persons. The distribution

of the age at death is shown in Table 1. Due to their incompleteness (76.4%
of all individuals had less than 50% of all bones) many of the adult skeletons
(simply referred to as Adults in Table 1) lack a more precise age determination.
That is why the sample of adults was not divided into age categories when analyzed.
The same problem of incompleteness prevented sex determination in 63% of
the adults.

Stature

The average stature of the population from Jabuticabeira II is 1.51 m. The mean
stature of males (n ¼ 6) was estimated to be 1.56 m (s ¼ 0.074, s ¼ 0.067), whereas
that of females (n ¼ 5) was 1.46 m (s ¼ 0.042; s ¼ 0.039).

Oral pathologies

The distribution of age at death of the 24 individuals included in the oral

pathology analyses (Table 2) consists of one adolescent (4.2%), two young adults
(8.3%), nine middle adults (37.5%), one old adult (4.2%) and 11 adults (45.8%). As
shown in Table 2, periodontal disease was observed in the great majority of the
individuals, and in two-thirds of the teeth. Abscessing was present in almost half of
the population, but affected only a small number of alveoli per individual. A similar
pattern was observed for antemortem tooth loss: one-third of the population was

Table 1. Age at death and sex distribution in Jabuticabeira II

Age class Age-at-death (years) N % N females N males

Juveniles 0–20 26 29.2 — —

Young adults 21–35 10 11.2 2 1
Middle adults 36–49 11 12.4 4 7
Old adults 450 1 1.1 1 0
Adults 421 41 46.1 3 4
Total — 89 100.0 10 12
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Table 2. Frequency distribution of oral pathologies in Jabuticabeira II

Oral N Available N Affected Frequency N Available N Affected Frequency

Markers Individuals Individuals of Affected Teeth or Teeth or of Affected
Individuals Sockets Sockets Teeth or
(%) Sockets
(%)

Peridontal disease 21 19 90.5 336 222 66.07

abscesses 16 7 43.7 336 12 3.57
AMTL 16 6 37.5 359 23 6.41
Caries 24 1 4.2 452 2 0.44

affected, but one individual presented an edentulous mandibula, whereas the rest of
the affected persons lost only very few teeth. Finally, a low caries incidence
was found in this population (4.2% of individuals and 0.44% of teeth affected),
in which only one adult individual presented the two (occlusal molar) caries
lesions found in this sample. All adults presented a pronounced dental wear.
The mean degree of dental wear for incisors, canines and premolars is x ¼ 4.763
(following Smith 1984) and x ¼ 3.649 for molars (following Brothwell 1981).
No evidence of the use of teeth as tools was found in this sample. All individuals
were affected with dental calculus. However, only very few presented them
intact (two out of 23 available individuals), and in these cases the calculus was
remarkably extensive, reaching the maximum degrees in Brothwell’s classification
(1981). Due to the small sample size, statistical analyses of dental pathologies were
not carried out.

Auditory exostoses

Auditory exostoses was observed in four adult males and one adult female
(out of nine males, seven females and five adults of undetermined sex with at
least one meatus preserved), leading to a figure of 23.8%. In males, in two cases
the exostosis was observed in both meati and with symmetric grades of severity,
but in one case, the right meatus was more affected than the left one. The female
had just one meatus affected. Six out of 34 (17.7%) meati presented auditory
exostoses.

Cribra orbitalia

The occurrence of cribra orbitalia was verified in five individuals in a total of 17

eligible crania (eight females, six males, one non-sexed adult and two juveniles with
at least one preserved orbit), yielding a figure of 29.4%. Four of these lesions were
healed and belonged to adult females; one was still active at the time of death and
belonged to a three-year-old child. Eight among 27 orbits (29.6%) showed evidence
of cribra orbitalia.
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Infectious diseases

The distribution of infectious diseases, considered here as periostitis and

osteomyelitis, is given in Table 3. The bone significantly most often affected was
the tibia (37%) (w2 ¼ 11.24; po 0.01), whereas the rib was the bone with the lowest
frequency observed. All infections matched the diagnostic criteria of periostitis,
except a distal humerus with osteomyelitis and the case of a pair of tibiae and one
fibula with gummatous lesions (Fig. 2) that belonged to an adult of undetermined
sex. The right tibia was more affected than the left one, the former being a typical
saber shin tibia. The X-ray of both tibiae showed a slight reduction of the diameter
of the medullary cavity (Fig. 3).

Table 3. Frequency distribution of periostitis and osteomyelitis per anatomical unit in

Jabuticabeira II

Bone N available bones N affected bones Affected bones (%)

Clavicula 43 4 9.30
Scapula 45 4 8.89
Humerus 61 6 9.84
Radius 56 8 14.29
Ulna 56 5 8.93
Femur 55 9 16.36
Tibia 49 18 36.73
Fibula 38 4 10.53
Long bone (fragment) 30 6 20
Rib 34 1 2.94

Fig. 2. Saber Shin tibia from one adult individual.

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Fig. 3. X-ray of the pathological tibiae shown on Fig. 2 (on the left and in the middle) in
comparison with a normal one (on the right).

An interesting palaeopathological finding refers to a double burial of a six-month

old infant and a three-year-old child. Both were buried together in an undoubtedly
secondary burial, with many beads and a carved shell positioned near their
heads. Although the bones were very fragile (due to their tiny size, their patho-
logies and the very bad weather conditions during the excavation), both skele-
tons were more than 50% complete and well preserved. All their long bones
presented about 2 mm thick detachable new bone formation (periostitis) on
both, metaphysis and diaphysis (Fig. 4). The X-ray of these bones revealed
no alteration in the medulary cavity (Fig. 5). The older child presented active
cribra orbitalia.
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Fig. 4. Periostitis on tibia of a three-year-old child.

Fig. 5. X-ray of long bones belonging to six-month- and three-year-old children.

Degenerative joint disease (DJD)

Among the adults (n ¼ 34 individuals), almost all (n ¼ 33) were affected by

degenerative joint disease. It must be kept in mind that due to the small sample size
only presence and absence of DJD was considered. Nevertheless, it was possible to
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Table 4. Distribution frequency of degenerative joint disease per anatomical unit and joint in
Jabuticabeira II

Bone N N Affected Affected Upper limbs and

available affected bones joints (%) lower limbs (%)
bones bones (%)

Sternal end of 14 11 78.57 78.57 —

clavicula
Acromial end of 14 10 71.43 47.17 88/147 ¼ 59.86
clavicula
Scapula 18 12 66.67
Proximal humerus 21 3 14.29
Distal humerus 29 17 58.62 59.46
Radius/ulna 21 13 61.90
Proximal ulna 24 14 58.33
Distal radius 18 3 16.67 20.37
Distal ulna 14 5 35.71
Carpii 22 3 13.64
Metacarpii 27 3 11.11 14.81
Phalanges (hand) 27 5 18.52
Acetabulum 11 1 9.09 6.67 26/165 ¼ 15.76
Proximal femur 19 1 5.26
Distal femur 10 0 0 18.92
Patella 20 7 35.00
Proximal tibia 7 0 0
Proximal fibula 10 2 20.00 20
Distal tibia 14 1 7.41 17.65
Distal fibula 13 2 15.38
Tarsii 24 6 25.00
Metatarsii 16 3 18.75 16.22
Phalanges (foot) 21 3 14.29
Vertebrae 531 220 41.44 41.43 —

Upper limbs: considered from acromial clavicula to phalanges of the hands. Lower limbs: considered from
acetabulum to phalanges of the feet.

observe that the degenerative changes affected both men and women equally, but the
distribution of bones affected (Table 4) shows that the upper limbs (37% of them
arthritic) were significantly (w2 ¼ 21.77; po0.01) more affected than the lower ones
(16% of them arthritic). Despite the high prevalence of DJD, no eburnation was
observed.
Degenerative joint changes were also observed in the vertebral column. However,
since none of the spines were complete and all of the vertebrae were badly damaged,
no attempt could be made to analyse the differential degree of articular changes in
the cervical, thoracic and lumbar segments. Degenerative joint disease was found in
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41.4% of the vertebral body facets (220 out of 531 facets affected) and in 22 out of 28
(78.6%) adult individuals (data not shown).

Trauma

Out of 14 adults (six males and eight females) only two of the females presented
trauma, against three of the males. Moreover two out of seven adults (28.6%) of
undetermined sex presented traumas. They were localized on one femur, two
vertebrae, one ulna, one elbow and also on one skull. Most of them were not severe
and presented no evidence of interpersonal violence. Furthermore they were in the
process of healing at the time of death.

Discussion

Skeletal markers are among the most powerful tools used to reconstruct the
biological features of ancient populations. A more complete reconstruction of their
way of life can be made if there is an integration of the study of these markers with
data obtained from other sources such as zooarchaeology, palaeobotany, material
culture and settlement patterns. According to more recent studies, Sambaqui
populations were fisher-gatherers (Figuti & Klökler 1996), who used a wide variety
of plants for food, fuel, artifact production and construction (Scheel-Ybert 1999)
and engaged in elaborated mortuary rituals (Edwards et al 2001). They possibly
shared a common identity with neighboring Sambaqui peoples and used their often
huge mounds for purposes as diverse as habitation, cemetery and as a place for tool
production (Gaspar 1998).

Sex and age at death

The data obtained from Jabuticabeira II revealed that approximately one-third

of the buried individuals were juveniles. This high proportion of juveniles has
been observed in most prehistoric cemeteries and in accordance with Waldron
(1994), this indicates that burial rituals were not altering the natural demo-
graphic composition. This statement was corroborated by the fact that the sexes
were evenly distributed and that the age at death of adults ranged from 21 to more
than 50 years.

Stature

The average stature for the population of Jabuticabeira II (1.51 m) and

other Sambaquis (Mello e Alvim & Uchôa 1976; Kneip et al 1995; Mendonça
de Souza 1995) is at the lower end of the range, especially for women, when
compared with other prehistoric and extant Amerindian populations (Storto et al
1999).
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Oral pathologies

The study of dental pathologies allows some inferences about the resources
consumed by this coastal population. The high degree of dental wear detected on the
occlusal surface of all studied teeth from Jabuticabeira II was exclusively due to
masticatory stress. The high degree of dental wear in all Sambaqui populations
studied, as already pointed out by many authors (Salles Cunha 1959, 1963a, b;
Araujo 1969, 1970; Mendonça de Souza 1995; Wesolowski 2000), was probably
caused by sand, tiny shellfish fragments and phytoliths (Reinhard et al 2001) present
in the food consumed.
The large quantity of abrasive material present in the diet of the Jabuticabeira
population possibly caused an increase in the frequency of periodontal disease
(90.5% of the individuals and 66.07% of the sockets). High degrees of dental wear
result in the loss of contact between adjacent teeth and irritation of nearby soft
tissues, followed by inflammation and subsequent infection (Ortner & Putschar 1981;
Alt et al 1998). However, this disease can also be the result of dental calculus
(Brothwell 1981), a trait which affects all adults and that is extremely large in the
Jabuticabeira II sample, when preserved. Only 4.2% of the individuals and 0.44% of
the teeth were affected by caries. In spite of the fact that high degrees of dental wear
reduce the substrate for occlusal caries, and this might account for the low frequency
of caries (Maat & van der Velde 1987) observed in many Sambaqui populations
(Salles Cunha 1959, 1963a, b; Araujo 1969, 1970; Mendonça de Souza 1995), the low
frequency might also be related to a combination of the following factors: diet poor
in cariogenic substances (Larsen 1997), low genetic predisposition to caries and
cariostatic habits (Hillson 1996).
Coastal populations usually show high levels of dental wear and low frequencies of
caries, calculus, abscesses and antemortem tooth loss (Littleton & Frohlich 1993).
All of these features, except for high frequencies of dental calculus, were also
observed in Jabuticabeira II and other Sambaquis (Salles Cunha 1963a; Mendonça
de Souza 1995). A higher calculus frequency in other non-agricultural populations
was reported to be due to the alkaline mouth environment caused by the ingestion of
large quantities of fats and proteins (Pedersen 1947).

Auditory exostosis

Auditory exostosis can be interpreted as an indicator of sex specific activities in the

Jabuticabeira II population. A higher frequency of auditory exostoses in men than
women was observed in this and other Sambaqui populations (Mendonça de Souza
1995). This type of exostoses is reported to be caused by frequent dives in cool
(Chaplin & Stewart 1998; Kennedy 1986) or salty water (Peixoto 1989) and may
therefore be related to the people’s subsistence strategies. In several other
populations, high frequencies of this trait are found in the sex which is responsible
for the capture of aquatic resources (Kennedy 1986; Standen et al 1997). This might
also be true for the Sambaqui people.
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Cribra orbitalia

Once interpreted as one of the best palaeopathological markers, cribra orbitalia

reached figures of almost 30% of orbits in Jabuticabeira II. Since it does not stand as
a proxi for anemia anymore, this relatively high percentage suggests that
physiological stressors (Wapler et al 2004) must have affected them in probably
different ways. According to the high prevalence of general infections (see below),
the most parsimonious hypothesis on the origin of those stressors are parasitic
infections.

Infectious diseases

Among all chronic diseases, only some result in bony changes. Periostitis and
osteomyelitis do lead to bony changes but may be a consequence of several different
causes, including metabolic disorders and infectious agents (Ortner & Putschar
1981). Periostitis is due to infections and inflammations of the periosteum
(Mensforth et al 1978; Ortner & Putschar 1981; Goodman et al 1984) and might
be due to local infection or systemic infection. Osteomyelitis is the result of the
introduction of bacteria into the bone marrow either by direct infection through
trauma, by extension from adjacent infections or by hematogeneous spread
(Steinbock 1976; Ortner & Putschar 1981; Goodman et al 1984). Among the
infectious agents, there are many different bacteria. One of them is Treponema sp.,
which besides venereal syphilis also causes pinta, yaws and endemic syphilis. These
four diseases together are known as treponematoses.
The gummatous lesions found in the tibiae of one adult in Jabuticabeira II suggest
treponematosis (Brothwell, personal communication). However, it is not possible to
fully confirm this diagnosis because of the incompleteness of the skeleton, which also
prevented us to apply criteria for differential diagnosis, such as those developed by
Rothschild & Rothschild (1995).
The juvenile skeletal remains of the double secondary burial presenting severe
systemic periostitis suggest four possible diagnoses. Since they presented the same
type, distribution and severity of bone modifications, the same disease probably
affected both of them. Possible diagnoses include congenital syphilis, yaws, scurvy or
hematogenous osteomyelitis.
Congenital syphilis was excluded, despite the fact that deposition of subperiosteal
bone on the shafts of long bones can be diagnostic of congenital syphilis (Ortner &
Putschar 1981), because no other typical feature was found, such as the ‘‘saw-
toothed’’ metaphysis or the pathognomonic dental lesions (Aufderheide &
Rodrı́guez-Martı́n 1998).
The diagnosis of yaws was excluded due to the young age of the children (six
months and three years old), since this disease usually affects the skeleton several
years after the initial infection (Aufderheide & Rodrı́guez-Martı́n 1998; Buckley
2000).
Scurvy, the result of chronic vitamin C deficiency, was also ruled out. In scurvy,
there is a new bone formation at the periosteum, and usually these changes are
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M.M.M. Okumura / HOMO — Journal of Comparative Human Biology 55 (2005) 263–281 277

bilateral, involve multiple bones, and in children affect mostly costochondral

junctions and metaphyses (Ortner & Putschar 1981). Additionally, other osseous
changes may be present due to scurvy such as bony growth on the jaws, orbits and
along the lines of the temporalis muscle (Ortner 1984; Roberts 1987). Excluding
metaphyseal periostitis, none of these features were observed in the two children.
Furthermore, scurvy is unlikely to occur where fruits like guava and other Myrtacea
seem to have been abundant (De Masi 1999) and at least the small child would
probably still have been nursed with vitamin-rich milk from the mother.
Most cases of infection and hematogenous osteomyelitis in particular, are caused
by bacteria such as Staphylococcus aureus. Besides causing mastitis and pneumonia,
S. aureus is responsible for osteomyelitis, which, in pre-antibiotic times, would have
led to septicemia with rapid and fatal outcomes. This bacterium can be found in a
large range of environmental conditions and easily adapts to temperatures that range
between 15 and 45 1C, to environments with high degrees of salinity, as well as
aerobic and anaerobic conditions (Todar 2004). Hematogeneous osteomyelitis
caused by S. aureus seems to be the most plausible diagnosis of the disease which
affected the two children because this diagnosis can be reached even with the lack of
typical osteomyelitic features, since in children cloacae and sequestra are rarely
observed and pus can exude directly through the periosteum (Ortner & Putschar
1981; Aufderheide & Rodrı́guez-Martı́n (1998)). Furthermore, the multiple bones
affected in the two children are consistent with reports of several bones being
affected in up to 40% of the juvenile cases (Bullough 1992).
Poor sanitary conditions such as those presumed for people living on shellmounds
can account not only for hematogeneous osteomyelitis, but also for gastrointestinal
infections that may lead to anemia or other sources of physiological stress (Wapler
et al 2004) as is indicated by the cribra orbitalia observed in the older child (Buckley
2000).

Degenerative joint diseases (DJD)

The higher prevalence of DJD in the upper (60%) as compared to the lower limbs
(16%) of the people from Jabuticabeira II has also been observed in other
Sambaquis (Neves 1986) and was associated with activities like swimming, diving,
rowing, throwing of fishing nets and carrying baskets full of seafood (Mendonça de
Souza 1995). On the other hand, the minimal stress load observed in the lower limbs
can be interpreted as indicating the short walking distances needed for resource
procurement. This suggests both resource abundance and predictability.

Trauma

Besides its benign nature, the low frequency of traumas observed in Jabuticabeira
II is not unexpected, since this has also been observed at other Sambaqui sites
(Mendonça de Souza 1995; Lessa & Medeiros 2001). The broad temporal and
geographic distribution of Sambaquis and especially the use of multiple concomitant
neighboring sites sharing the same territory, suggest that the Sambaqui populations
 ARTICLE IN PRESS
278 M.M.M. Okumura / HOMO — Journal of Comparative Human Biology 55 (2005) 263–281

may have been peaceful, showing little interpersonal violence. This is consistent with
a high resource availability being shared by many peoples (Larsen 1997) and with the
paleoenvironment of this region (Scheel-Ybert 1998).

Conclusion

These data support the idea of resource abundance, already indicated on the
basis of the high number, density and size of the Sambaquis scattered around
the lake Camacho (Fish et al 2000). Despite the periods of illness various
individuals experienced, the daily life among the Sambaqui dwellers from
Jabuticabeira II seems to have been relatively easy due to the abundance and
predictability of marine and plant resources and the rarity of traumas, be they
violent or not.

Acknowledgements

The human skeletal remains used in this article derive from archaeological
excavations undertaken by several specialists under the joint coordination of P. De
Blasis, M.D. Gaspar, S. Fish and P. Fish and the financial support of Wenner Gren
Foundation, FAPESP and USP. Financial support was received further from
CEPID/ FAPESP. We would also like to specially thank: M.M. Lahr for help and
contacts, C.B. Simões, C. Storto Frochtengarten and I. Fazzio for providing us with
additional literature on Sambaquis and a helping hand during the curation process,
D. Brothwell for valuable discussions regarding treponematosis, UNIORT for
kindly providing the X-rays, and finally the Martinez-Okumura family for all their
caring support. We would also like to thank the referees P. Caselitz, I. Hershkovitz
and M.A. Costa for comments and suggestions that significantly improved this
article.

References
Alt KW, Rösing FW, Teschler-Nicola M (1998) Dental Anthropology: Fundamentals, Limits and
Prospects. Springer, Wien.
Araujo EM (1969) Análise do material ósseo humano do Sambaqui do rio Lessa. An Inst Antrop 2:
141–211.
Araujo EM (1970) Afecções dentárias: hipercementose e abrasão das populações do litoral de Santa
Catarina. An Mus Antrop UFSC 3: 71–90.
Aufderheide AC, Rodrı́guez-Martı́n C (1998) The Cambridge Encyclopedia of Human Paleopathology.
Cambridge University Press, Cambridge.
Beck AM (1974) O Sambaqui de Enseada I—SC LN 71: um estudo sobre a tecnologia pré-histórica Tese
de livre-docência. UFSC, Florianópolis.
Bigarella JJ (1951) Contribuição ao estudo dos Sambaquis do estado do Paraná. II Regiões adjacentes à
baı́a de Guaratuba. Arq Biol Tecnol (Curitiba) 5/6: 293–314.
Bissa WM, Ybert J-P, Catharino ELM, Kutner M (2000) Evolução paleoambiental na planı́cie costeira do
baixo Ribeira durante a ocupação Sambaquieira. Rev Mus Arqueol Etnol 10: 89–102.
 ARTICLE IN PRESS
M.M.M. Okumura / HOMO — Journal of Comparative Human Biology 55 (2005) 263–281 279

Brooks ST, Suchey JM (1990) Skeletal age determination based on the Os Pubis: a comparison of the
Acsádi-Nemeskéri and Suchey-Brooks Methods. Hum Evol 5: 227–238.
Brothwell DR (1981) Digging up Bones. Cornell University Press, New York.
Buckley H (2000) Subadult health and disease in prehistoric Tonga, Polynesia. Am J Phys Anthrop 113:
481–505.
Buikstra JE, Ubelaker DH (1994) Standards for data collection from human skeletal remains. Arkansas
Archeological Survey Research Series No. 44.
Bullough PG (1992) Atlas of Orthopedic Pathology with Clinical and Radiologic Correlations. Gower
Medical Publishers, New York.
Chaplin JM, Stewart IA (1998) The prevalence of exostoses in the external auditory meatus of surfers. Clin
Otolaryngol 23 (4): 326–330.
De Blasis PAD, Fish SK, Gaspar MD, Fish PR (1998) Some references for the discussion of complexity
among the Sambaqui moundbuilders from the southern shores of Brasil. Rev Arqueol Am 15: 75–105.
De Masi MAN (1999) Prehistoric hunter-gatherer mobility on the southern Brazilian Coast: Santa
Catarina island. PhD dissertation, Department of Anthropology, Stanford University.
Edwards HGM, Farwell DW, de Faria DLA, Monteiro AMF, Afonso MC, De Blasis P, Eggers S (2001)
Raman spectroscopic study of 3000 year-old human skeletal remains from a Sambaqui, Santa
Catarina, Brazil. J Raman Spectrosc 32: 17–22.
Figuti L (1992) Les Sambaquis COSIPA (4200 à 1200 ans BP): Ètude de la subsistance chez les peuples
préhistoriques de pêcheurs-ramasseurs de bivalves de la côte centrale de l’état de São Paulo, Brézil.
PhD dissertation, Musée National d’Histoire Naturelle, Institut de Paléontologie Humaine, Paris.
Figuti L (1993) O homem pré-histórico, o molusco e o Sambaqui: considerações sobre a subsistência dos
povos Sambaquieiros. Rev Mus Arqueol Etnol 3: 67–80.
Figuti L (1994) Os Sambaquis COSIPA (4200 a 1200 anos AP): estudo da subsistência dos povos
pescadores coletores pré-históricos da Baixada Santista. Ver Arqueol (São Paulo) 8: 167–283.
Figuti L (1999) Economia/alimentação na pré-história do litoral de São Paulo. In Tenório MC (ed)
Pré-História da Terra Brasilis. UFRJ, Rio de Janeiro, 197–203.
Figuti L, Klökler DM (1996) Resultados preliminares dos vestı́gios zooarqueológicos do Sambaqui
Espinheiros II (Joinville, SC). Rev Mus Arqueol Etnol 6: 169–187.
Fish SK, De Blasis P, Gaspar MD, Fish P (2000) Eventos incrementais na construção de Sambaquis,
litoral sul do Estado de Santa Catarina. Rev Mus Arqueol Etnol 10: 69–87.
Gaspar MD (1996) Datações, construção de Sambaqui e identidade social dos pescadores, coletores e
caçadores. Anais da VIII Reunião da Soc Arqueol Brasileira 1: 811–820.
Gaspar MD (1998) Considerations of the Sambaquis of the Brazilian coast. Antiquity 72: 592–615.
Gaspar MD, De Blasis PAD (1992) Construção de Sambaquis. Anais da VI Reunião da Soc Arqueol
Brasileira 2: 811–820.
Gaspar MD, Afonso M, De Blasis PAD, Eggers S, Figuti L, Fish P, Fish S, Klokler DM, Lahr MM,
Moeley E (1999) Uma breve história do projeto de pesquisa ‘‘Padrão de assentamento e formação de
Sambaquis: arqueologia e preservação em Santa Catarina’’. Rev Centro Estudos Pesquisas Arqueol 23:
108–117.
Goodman AH, Martin DL, Armelagos GJ, Clarck G (1984) Indications of stress from bones and teeth.
InCohen MN, Armelagos GJ (eds) Paleopathology at the Origins of Agriculture. Academic Press,
Orlando, 13–49.
Hillson S (1996) Dental Anthropology. Cambridge University Press, Cambridge.
Ilhering H von (1907) A antropologia do estado de são Paulo. Ver Mus Paulista 7:202–257.
Imbelloni J (1956/1958) Las reliquias del Sambaqui. Rev Mus Paulista (Nova Série) 10: 243–281.
Johnston FE (1962) Growth of the long bones of infants and young children at Indian Knoll. Hum Biol
33: 66–81.
Kennedy GE (1986) The relationship between exostoses and cold water: a latitudinal analysis. Am J Phys
Anthrop 71 (4): 401–415.
Kneip LM (1994) Sı́ntese final. InKneip LM (ed) Cultura material e subsistência das populações pré-
históricas de Saquarema, RJ. Doc Trabalho, Série Arqueol 2. Museu Nacional, Rio de Janeiro, 61–70.
Kneip LM, Machado LC, Crancio F (1995) Ossos humanos trabalhados e biologia esqueletal do
Sambaqui de Saquarema, RJ. Documento de Trabalho, Série Arqueologia 3. Museu Nacional, Rio de
Janeiro, 13–31.
Lacerda JB (1885) Nota sobre os crânios dos Sambaquis de Santos (Passa-Mirim). Bol Comis Geog Geol
São Paulo 9: 89–90.
Larsen C (1997) Bioarchaeology: interpreting behaviour from the human skeleton. Cambridge University
Press, Cambridge.
 ARTICLE IN PRESS
280 M.M.M. Okumura / HOMO — Journal of Comparative Human Biology 55 (2005) 263–281

Lessa A, Medeiros JC (2001) Reflexões preliminares sobre a questão da violência em populações

construtoras de Sambaquis: análise dos sı́tios Cabeçuda (SC) e Arapuan (RJ). Rev Mus Arqueol Etnol
11: 77–94.
Lima TA, Macario KD, Anjos RM (2001) Datações antigas em Sambaquis do Rio de Janeiro: um
problema que se reapresenta. Resumos do XI Congresso da Sociedade de Arqueologia Brasileira,
135–136
Littleton J, Frohlich B (1993) Fish-eathers and farmers: dental pathology in the Arabian Gulf. Am J Phys
Anthrop 92: 427–447.
Maat G, van der Velde E (1987) The caries attrition competition. Int J Anthrop 2: 281–292.
Meindl RS, Lovejoy CO (1985) Ectocranial suture closure: a revised method for the determination of
skeletal age at death based on the lateral–anterior sutures. Am J Phys Anthrop 68: 57–66.
Mello e Alvim MC, Seyferth G (1968/1969) Estudo morfológico do úmero na população do Sambaqui de
Cabeçuda (Laguna, Santa Catarina). Rev Mus Paulista (Nova Série) 18: 119–126.
Mello e Alvim MC, Seyferth G (1971) O fêmur da população do Sambaqui de Cabeçuda (Laguna
Estado de Santa Catarina, Brasil): estudo morfológico e comparativo. Rev Mus Nac (Nova Série) 24:
1–14.
Mello e Alvim MC, Uchôa DP (1976) Contribuição ao estudo das populações de Sambaquis: Os
construtores do Sambaqui de Piaçaguera. Série Pesquisas do Instituto de Pré-História (USP) 1: 1–32.
Mello e Alvim MC, Uchoa DP, Gomes JCO (1991) Cribra orbitalia e lesões cranianas congêneres em
populações pré-históricas da costa meridional do Brasil. Rev Mus Arqueol Etnol 1: 21–53.
Mello e Alvim MC, Gomes JC de O (1992) Hiperostose porosa: anemia malárica? Ìndios Guajajara—
estudo de um caso. InAraújo AJG, Ferreira LF (eds) Paleopatologia e paleoepidemiologia. Estudos
multidisciplinares. Escola Nacional de Saúde Pública, Rio de Janeiro, 141–157.
Mendonça de Souza SMF (1995) Estresse, doença e adaptabilidade: estudo comparativo de dois grupos
pré-históricos em perspectiva biocultural. PhD thesis. Fundação Oswaldo Cruz, Rio de Janeiro.
Mensforth RP, Lovejoy CO, Lallo JW, Armelagos GJ (1978) The role of constitutional factors diet and
infectious disease in the etiology of porotic hiperostosis and periosteal reactions in prehistoric infants
and children. Med Anthropol 2: 1–59.
Neves WA (1986) Incidência e distribuição de osteoartrites em grupos coletores do litoral do Paraná: uma
abordagem osteobiográfica. Clio (Série Arqueológica 1) 6: 47–62.
Neves WA (1988) Paleogenética dos grupos pré-históricos do litoral sul do /Brasil (Paraná e Santa
Catarina). Pesquisas (Antropologia) 43: 1–178.
Neves WA, Wesolowski V (2002) Economy, nutrition, and disease in prehistoric coastal Brazil: a case
study from the state of Santa Catarina. In Steckel RH, Rose JC (eds) The backbone of history: health
and nutrition in the Western hemisphere. Cambridge University Press, Cambridge, 376–400.
Ortner DJ (1984) Bone lesions in a probable case of scurvy from Metlatavik, Alaska. MASCA J 3: 79–81.
Ortner DJ, Putschar WGJ (1981) Identification of pathological conditions in human skeletal remains.
Smithsonian Contributions to Anthropology, vol. 28. Smithsonian Institution Press, Washington.
Pedersen P (1947) Dental investigations of Greenland Eskimos. Proc R Soc Med 40: 726–736.
Peixoto MV (1989) Avaliação radiológica do torus auditivus nos grupos formadores de Sambaquis do
litoral meridional brasileiro: contribuição ao estudo dos traços não métricos em populações pré-
históricas do Brasil. MSc thesis. Depto de Anatomia Humana, Universidade Federal do Rio de
Janeiro.
Prous A (1991) Arqueologia brasileira. Universidade de Brası́lia.
Reinhard KJ, Souza SMF, Rodrigues C, Kimmerle E, Dorsey-Vinton S (2001) Microfossils in dental
calculus: a new perspective on diet and dental disease. In Williams E (ed) Proceedings of the
Conference: Human Remains, Conservation, Retrieval and Analysis. BAR International Series 934.
Williamsburg, November 1999, 113–118.
Roberts CA (1987) Case Report 9: Scurvy. Paleopathol Assoc Newslett 57: 14–15.
Rothschild BM, Rothschild C (1995) Treponemal disease revisited: skeletal discriminators for yaws, bejel,
and venereal syphilis. Clin Infec Dis 20: 1402–1408.
Salles Cunha E, de M (1959) Patologia odonto-maxilar no homem dos Sambaquis. Rev Brasileira Odontol
17: 532–541.
Salles Cunha E, de M (1963a) Afecções alvéolo-dentárias da população do Sambaqui de Cabeçuda. Rev
Mus Paulista (Nova Série) 14: 523–529.
Salles Cunha E de M (1963b) Sambaquis e outras jazidas arqueológicas: paleopatologia dentária e outros
assuntos. Cientı́fica, Rio de Janeiro.
Scheel-Ybert R (1999) Paleoambiente e paleoetnologia de populações Sambaquieiras do Sudeste do
Estado do Rio de Janeiro. Rev Mus Arqueol Etnol 9: 43–59.
 ARTICLE IN PRESS
M.M.M. Okumura / HOMO — Journal of Comparative Human Biology 55 (2005) 263–281 281

Sciulli PW, Giesen MJ (1993) Brief communication: An update on stature estimation in prehistoric native
Americans of Ohio. Am J Phys Anthrop 92: 395–399.
Smith BH (1984) Patterns of molar wear in hunter-gatherers and agriculturalists. Am J Phys Anthrop 63:
39–56.
Standen VG, Arriaza BT, Santoro CM (1997) External auditory exostosis in prehistoric chilean
populations: a test of the cold water hypothesis. Am J Phys Anthrop 103: 119–129.
Steinbock RT (1976) Paleopathological Diagnosis and Interpretation. CC Thomas, Springfield.
Storto C, Eggers S, Lahr M (1999) Estudo preliminar das paleopatologias da população do Sambaqui
Jabuticabeira II, Jaguaruna, SC. Rev Mus Arqueol Etnol 9: 61–71.
Todar K (2004) Staphylococcus. Bacteriology at University of Wisconsin-Madison, Department of
Bacteriology. Bacteriology Todar’s online textbook of bacteriology—http://textbookofbacteriology.
net/staph.html. Date of access: 29-9-2004.
Ubelaker DH (1989) Human Skeletal Remains. Taraxacum, Washington DC.
Waldron T (1994) Counting the dead: the epidemiology of skeletal populations. John Wiley & Sons: New
York.
Wapler U, Crubézy E, Schultz M (2004) Is cribra orbitalia synonymous with anemia? Analysis and
interpretation of cranial pathology in Sudan. Am J Phys Anthrop 123: 333–339.
Wesolowski V (2000) A prática da horticultura entre os construtores de Sambaquis e acampamentos
litorâneos da região da Baı́a de São Francisco, Santa Catarina: Uma abordagem bio-antropológica.
MSc thesis. FFLCH, USP, São Paulo.
White TD (1991) Human Osteology. Academic Press, San Diego.