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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 132:558–567 (2007)

Auditory Exostoses as an Aquatic Activity Marker:


A Comparison of Coastal and Inland Skeletal Remains
From Tropical and Subtropical Regions of Brazil
Maria Mercedes M. Okumura,1 Célia H.C. Boyadjian,2 and Sabine Eggers2*
1
Laboratório de Estudos Evolutivos Humanos, Depto. de Genética e Biologia Evolutiva,
Instituto de Biociências, Universidade de São Paulo, 05422-970 São Paulo, SP, Brazil
2
Laboratório Antropologia Biológica, Depto. de Genética e Biologia Evolutiva, Instituto de Biociências,
Universidade de São Paulo, 05422-970 São Paulo, SP, Brazil

KEY WORDS shellmound; Paleoindian; Botocudo; Brazilian archaeology; bioarchaeology

ABSTRACT Auditory exostoses are bone masses lo- temperatures in conjunction with wind effects. In areas
cated in the external auditory canal. Currently, most re- with mild atmospheric temperatures and wind chill fac-
searchers agree that the environment (especially water tors, the coastal populations analyzed do not show high
temperature, but also atmospheric temperature and wind frequencies of auditory exostoses. However, high frequen-
action) plays a pivotal role in the development of this cies of auditory exostoses develop where cold atmospheric
trait. This article discusses whether the presence of audi- temperatures are further lowered by strong wind chill.
tory exostoses can be used as an aquatic activity marker Therefore, the association between aquatic activities, low
in bioarchaeological studies, especially in groups that atmospheric temperature, and wind chill is strongly corre-
inhabited tropical and subtropical regions. We analyzed lated with the presence of auditory exostoses, but where
676 skeletons (5,000 years BP to historical times) from 27 these environmental factors are mild, the frequencies of
coastal and inland native Brazilian groups. Very low fre- auditory exostoses are not necessarily high. Concluding,
quencies of auditory exostoses were found in the inland auditory exostoses should be cautiously used as a marker
groups (0.00–0.03), but the expected high frequency of au- of aquatic activity in bioarchaeological studies in tropical
ditory exostoses in the coastal groups was not always and subtropical regions, since these activities do not
observed (0.00–0.56). These differences might be ex- always result in the presence of this trait. Am J Phys
plained by the combination of water and atmospheric Anthropol 132:558–567, 2007. V 2007 Wiley-Liss, Inc.
C

Auditory exostoses are bone anomalies mainly located From the 19th century until recently, the cause of au-
on the floor of the external auditory canal, medial to the ditory exostoses was thought to be genetic (Blake, 1880;
sutures of the tympanic plate (for a complete review of Hartmann, 1893; Berry, 1975). However, an exclusively
this trait, see Hauser and De Stefano, 1989). Auditory genetic origin of this trait has recently been rejected,
exostoses have an extensive base and can be bilateral because ancestry has not been shown to be significantly
and multiple (Sheehy, 1982; Hyams et al., 1988) (Fig. 1). related to the prevalence of auditory exostoses (Kroon
Auditory exostoses have been recorded in ancient skele- et al., 2002). Furthermore, several researchers who sup-
tal remains worldwide: Mesolithic Yugoslavians, pre-His- ported the genetic hypothesis have also cited chemical or
panic individuals from the Canary Islands (1,700– mechanical stimuli that lead to irritation of the auditory
540 years BP), Chileans (7000 B.C. to 1450 A.D.), pre- canal as possible underlying causes of the development
Columbian South American mummies, Lithuanians (from of auditory exostoses (Hrdlicka, 1935; Berry and Berry,
the Neolithic to the 17th–18th century A.D.), and individ-
uals from Imperial Rome (1st–3rd century A.D.) (Frayer,
1988; Manzi et al., 1991; Sakalinskas and Jankauskas, Grant sponsor: FAPESP: Grant numbers: 02/13441-0, 04/11038-0;
1993; Standen et al., 1997; Gerszten et al., 1998; Velasco- Grant sponsor: CNPq; Grant sponsor: FAPESP-CEPID; Grant num-
Vazquez et al., 2000). Auditory exostoses have also been ber: 98/14354-2; Grant sponsor: PIBIC-CNPq.
observed in Neanderthals and some European Middle
Pleistocene individuals excavated at Sima de los Huesos *Correspondence to: Sabine Eggers, Laboratório de Antropologia
(Boule, 1911–1913; Trinkaus, 1983:70, 411; Pérez et al., Biológica, Depto. de Genética e Biologia Evolutiva, Instituto de Bio-
ciências, Universidade de São Paulo, CP 11461, 05422-970 São
1997). Today, this trait is common in individuals who prac- Paulo, SP, Brazil. E-mail: saeggers@usp.br
tice aquatic sports (Van Gilse, 1938; Adams, 1951; Dettman
and Reuter, 1964; DiBartolomeo, 1979; Scrivener, 1981; Present address of Maria Mercedes M. Okumura: Leverhulme
Filipo et al., 1982; Kemink and Graham, 1982; Fabiani Centre for Human Evolutionary Studies, The Henry Wellcome Building,
et al., 1984; Kennedy, 1986; Umeda et al., 1989; Deleyiannis University of Cambridge, Fitzwilliam Street, Cambridge CB2 1QH, UK.
et al., 1996; Kroon et al., 2002), and prevalence of auditory
exostoses and degree of canal obstruction are positively cor- Received 31 January 2006; accepted 7 November 2006
related with intensity and number of years involved in
aquatic sports (Fowler and Osmun, 1942; Umeda et al., DOI 10.1002/ajpa.20544
1989; Deleyiannis et al., 1996; Kroon et al., 2002; Altuna Published online 22 January 2007 in Wiley InterScience
Mariezkurrena et al., 2004). (www.interscience.wiley.com).

C 2007
V WILEY-LISS, INC.
AUDITORY EXOSTOSES AS AQUATIC ACTIVITY MARKER 559
The purpose of this study is to investigate whether au-
ditory exostoses are an accurate aquatic activity marker
in tropical and subtropical regions. We seek to answer
two related questions: (1) are auditory exostoses indica-
tors of activities associated with the aquatic environ-
ment? and (2) do environmental factors such as atmos-
pheric and water temperature, as well as wind chill,
affect the frequencies of auditory exostosis?
These questions are approached using the frequencies
of exostoses among prehistoric and extant inhabitants of
inland and coastal regions of Brazil. This is the first sys-
tematic multisite study of auditory exostosis in tropical
and subtropical regions we are aware of. The inland
groups (Paleoindians and Botocudo) based their subsist-
ence on terrestrial game and plants, whereas the coastal
groups (shellmound builders) subsisted on fish and ma-
rine mollusks.
Regarding the first question, inland groups are ex-
pected to present little or no auditory exostosis, whereas
groups adapted to aquatic environments should show
higher frequencies of auditory exostosis. To answer the
Fig. 1. Auditory exostosis as observed in skeletal material. second question, we considered the variation not only of
sea water temperature, but also of atmospheric tempera-
ture and wind chill. Coastal groups are divided according
1967; Berry, 1975; Hutchinson et al., 1997). Currently, to geographic location, which coincides with increasing
most researchers agree that auditory exostoses are prob- latitude and consequently decreasing water and atmos-
ably caused by environmental factors, and genetic predis- pheric temperature, and increasing wind chill. If these
position has only a minor role in the development of this environmental factors influence the frequency of audi-
trait (Field, 1878; Van Gilse, 1938; Fowler and Osmun, tory exostosis, low water temperature, low atmospheric
1942; Harrison, 1962; Fabiani et al., 1984; Kennedy, 1986; temperature, and high wind chill will coincide with
Peixoto, 1989; Standen et al., 1997; Chaplin and Stewart, higher frequency of this trait in the coastal groups of the
1998; Velasco-Vazquez et al., 2000; Kroon et al., 2002). highest latitudes.
While water salinity (Peixoto, 1989) and wind effect
(Fabiani et al., 1984) are among the environmental fac- MATERIALS AND METHODS
tors reported to cause auditory exostoses, low water tem- Materials
perature is the most frequently cited factor. Although
the exact temperature necessary to trigger the develop- The geographic distribution of the groups studied is
ment of auditory exostoses has not been established, con- shown in Figure 2.
siderable physiological changes occur in the human ear
canal when exposed to water temperatures below 198C Inland sites. Brazilian inland skeletal remains are usu-
(Van Gilse, 1938; Fowler and Osmun, 1942). Signifi- ally scarce because of acidic tropical soil, which prevents
cantly higher prevalence of auditory exostoses has been the preservation of organic remains. With the exception
reported in individuals in contact with cold water (Van of two fairly large collections, Lagoa Santa and Boto-
Gilse, 1938; Fowler and Osmun, 1942; Harrison, 1962; cudo, no other inland collections are available.
Kennedy, 1986; Standen et al., 1997; Chaplin and Stew- The skeletal series of Paleoindians from Lagoa Santa
art, 1998; Ito and Ikeda, 1998; Velasco-Vazquez et al., (Minas Gerais State) comprises a large number of pre-
2000). Additionally, cold-water athletes are more likely historic inland individuals in a reasonable state of pres-
to develop auditory exostoses than are warm-water ath- ervation. Most of these hunter-gatherer groups inhabited
letes (Ito and Ikeda, 1998; Kroon et al., 2002). Lagoa Santa from 11,000 to 8,000 BP. Several studies
Inland populations, which lack intense contact with have been performed on the skeletal remains from this
water, present very low frequencies of auditory exostoses. region since the work of Peter Lund in the 19th century,
This is the case among the inland Salish, with a fre- and these remains are the most significant evidence that
quency of 0.03 (Finnegan, 1972), the central highlanders the New World was first colonized by a non-Mongoloid
from Gran Canaria with a frequency of 0.01 (Velasco-Vaz- population (Powell and Neves, 1999; Neves et al., 2004).
quez et al., 2000), and inhabitants of Chilean valleys and Although megafauna was contemporaneous with Paleo-
highlands with 0.02 and 0.00, respectively (Standen et al., indian groups in Lagoa Santa (Neves and Piló, 2003),
1997). Similarly, participants of nonaquatic sports were their diet was based on small animals (Araujo et al.,
found to have no auditory exostoses (Fabiani et al., 1984). 2002). A high frequency of dental caries (9%) at two
However, the association of low frequencies of exosto- Paleoindian sites from Lagoa Santa (not included in our
ses in inland groups and high frequencies in coastal pop- study) suggests a plant-based diet rich in carbohydrates
ulations is not always straightforward. Development of (Neves and Cornero, 1997; Neves and Kipnis, 2004).
auditory exostosis also appears to depend on the use of The other inland group used in this analysis is a
ear protection in the form of earplugs and/or hoods, recent (postcontact) group of Brazilian natives called
which mitigate wind chill or low atmospheric tempera- Botocudo (also known as Krenák). They were hunter-
tures or both, therefore, preventing the auditory canal to gatherers with a clear sexual division of labor: men
cool off (Deleyiannis et al., 1996; Timofeev et al., 2004; hunted and women were responsible for gathering. The
Zoltan et al., 2005). original territory of the Botocudo was the Atlantic Rain

American Journal of Physical Anthropology—DOI 10.1002/ajpa


560 M.M.M. OKUMURA ET AL.

Fig. 2. Map of Brazilian regions studied. Legend: Botocudo and Lagoa Santa are inland groups, all others are coastal groups. RJ, Rio
de Janeiro; SP, São Paulo; PR, Paraná; NSC, Northern Santa Catarina; ISC, Island of Santa Catarina; SSC, Southern Santa Catarina.

Forest. They were expelled from the coast by another 1999; De Masi, 1999, 2001). Consumption of plants, how-
native group, the Tupi, and occupied a parallel stretch of ever, was more common than was believed until recently
forest between the Atlantic Rain Forest and the edge of (Scheel-Ybert, 1998, 2001; Wesolowski, 2000, Scheel-Ybert
the Brazilian Plateau. In the 19th century, the Botocudo et al., 2003). Intense dental wear in these skeletal
groups moved south. This vast and scattered inland dis- remains is attributed to the admixture of sand, shellfish
tribution was a response to the European conquest as fragments, and phytoliths present in the food (Reinhard
well as wars between the Botocudo and their native ene- et al., 2001). Although the coastal Brazilian shellmound
mies (Paraı́so, 1991, 1992). In 1939, the tribe numbered builders were of relatively low stature, they were within
fewer than 100 individuals (IBGE, 2002). The osteologi- the range of variation of prehistoric and extant Native
cal series analyzed derives from the last half of the 19th Americans (Storto et al., 1999). Frequent nonspecific
century and encompasses individuals from three neigh- infections in many shellmound dwellers are attributed to
boring states: Bahia, Espı́rito Santo, and Minas Gerais. the intense contact with animal remains and pathogens
typical of tropical coastal areas (Mendonça de Souza,
Coastal sites. Shellmounds, common archaeological sites 1995). There is also evidence of communicable infectious
scattered along most of the 8,000 km of the Brazilian coast, diseases in some of the sites, suggesting high demo-
represent an excellent opportunity for the study of audi- graphic density, and although many neighboring sites are
tory exostoses. More than 1,000 sites are mapped (Gaspar, contemporaneous, an overall low frequency of violent
1998), and although only some of these sites have been trauma among shellmound dwellers indicates a relatively
studied intensely, they represent a cultural unit that peaceful lifestyle and little competition for food resources
expanded over a huge geographical area and spanned (Lessa and Medeiros, 2001; Okumura and Eggers, 2005).
*6,000 years (Gaspar, 1992, 1994/1995, 1996; De Blasis The shellmounds included in this study are located in
et al., 1998). Brazilian shellmounds vary in size and can four adjacent coastal states of Southeastern Brazil (Rio
reach 30 m in height. They consist of complex sequences of de Janeiro, São Paulo, Paraná, and Santa Catarina),
layers of shells and sand, containing food remains, hearths, dated to between 5,000 and 800 years BP. They repre-
technological implements, and elaborate burials associated sent the main temporal and geographic distribution of
with bone and stone artefacts and ochre. These shell- shellmounds in this country. Units included in this study
mounds are currently considered as monumental construc- are defined as follows: archaeological site, in the case of
tions intentionally built by sedentary people with high pop- coastal shellmounds and Lagoa Santa; archaeological
ulation densities (De Blasis et al., 1998; Gaspar, 1998). region, in the case of Santo Amaro Island; or group, in
The geographic location of many shellmounds, the occu- the case of Botocudo. Each unit consists of at least eight
pation of islands, and the capture of deep-sea fish species individuals. This arbitrary number was chosen because
indicate the use of boats by these coastal people (Gaspar, a larger one would have excluded several important sites
2000; Tenório, 2000). Zooarchaeological and stable isotope from this study, since usually scarce skeletal material is
studies have shown that these groups were fisher-gather- exhumated from most of the shellmounds. The selection
ers with diets based on marine resources (Figuti, 1992, criteria also included the amount of information avail-

American Journal of Physical Anthropology—DOI 10.1002/ajpa


AUDITORY EXOSTOSES AS AQUATIC ACTIVITY MARKER 561
TABLE 1. Frequencies of individuals affected with auditory exostosis in each unit analyzed, organized from north to south of Brazil
Region N individuals N affected
(state of N affected males/N affected
Unit origin) Oldest date individuals with exostosis Frequency females
Inland
Botocudo BA, ES, MG Mid-Late 40 1 0.03 1/0
XIX century
Cerca Grande Lagoa 9130 6 30 8 0 0.00 0/0
Santa (MG)
Lapa Mortuária de Confins Lagoa 8810 6 50 50 1 0.02 –
Santa (MG)
Coast
Beirada RJ 5420 6 190 11 0 0.00 0/0
Corondó RJ 4260 6 75 32 0 0.00 0/0
Zé Espinho RJ 2260 6 160 11 0 0.00 0/0
Piaçaguera SP 4930 6 110 21 5 0.24 3/1
Santo Amaro island (region) SP – 13 0 0.00 0/0
Tenório SP 1875 6 90 13 3 0.23 2/1
Guaraguaçu PR 4220 6 200 30 4 0.13 3/0
Matinhos PR 2750 6 250 19 3 0.16 2/1
Cabeçudas NSC – 16 5 0.31 4/1
Enseada NSC – 22 0 0.00 0/0
Forte Marechal Luz NSC 4290 6 130 14 1 0.07 1/0
Ilha de Espinheiros II NSC 2970 6 60 9 5 0.56 4/1
Itacoara NSC 1570 6 20 22 2 0.09 1/1
Laranjeiras II NSC – 28 4 0.14 4/0
Morro do Ouro NSC 4030 6 40 37 7 0.19 2/4
Rio Comprido NSC – 31 17 0.55 4/5
Armação do Sul ISC 2670 6 90 13 2 0.15 2/0
Base Aérea ISC 800 6 70 36 8 0.22 6/2
Ponta das Almas ISC 4289 6 400 9 1 0.11 1/0
Tapera ISC 1140 6 180 70 20 0.29 11/8
Balsinha SSC 3780 6 90 14 3 0.21 3/0
Cabeçuda SSC 4120 6 220 74 32 0.43 13/12
Içara SSC 1160 6 50 14 7 0.50 7/0
Jabuticabeira II SSC 2880 6 75 19 3 0.16 3/0

For Lagoa Santa dates see Araujo et al., 2005 and Neves et al., 2004; for most of the coastal site dates, see Lima, 1999–2000.
For the location of the regions studied refer to Fig. 2.

able about each unit. The minimum information neces- Paulo (SP), Paraná (PR), Northern Santa Catarina
sary for inclusion of a site were published reports on the (NSC), Island of Santa Catarina (ISC), and Southern
excavation, daily logs, descriptions of material culture, Santa Catarina (SSC). These six coastal regions com-
published dates, and various sources of data concerning prise 23 archaeological sites and one archaeological unit
diet and subsistence. called ‘‘Santo Amaro Island.’’ This unit consists of 12
Unfortunately, there are almost no skeletal remains skeletons exhumated from shellmounds on Santo Amaro
from the Northern coastal regions because of the scarcity Island (São Paul state) in the early 20th century (Imbel-
of archaeological surveys and the paucity of shellmounds loni, 1956/1958). Although no detailed information on
(Amâncio and Dominguez, 2003). Additionally, many provenience exists, this is an important collection,
researchers have proposed that the shellmounds from because most of the shellmounds in this area were
Northern and Northeastern Brazil belong to a different destroyed by later urban development.
cultural complex from the Southern–Southeastern shell- Among inland groups, Paleoindians from Lagoa Santa
mounds analyzed here (Lima, 1999/2000; Prous, 1991:293; (consisting of two archaeological sites) and Botocudo
but see Gaspar and Imazio, 1999 for a different view). were considered separately. In total, we analyzed six
Preliminary statistical analyses concerning differences coastal and two inland regions.
in the frequency of auditory exostoses were carried out
using the ‘‘unit’’ column of Table 1 (data not shown), but Methods
the small sample size prevented their use in other analy-
ses. Therefore, some units were grouped by state of ori- Data were recorded for 676 individuals with at least
gin (Table 1). This is justified because, in this part of one intact auditory canal (307 males, 258 females, and
Brazil, political state distribution follows increasing lati- 111 of undetermined sex). The external auditory canal
tude and consequently decreasing water and atmos- was examined with the naked eye and, when necessary,
pheric temperature, and increasing wind chill. As stated with the aid of a magnifying glass and a small lamp.
before, these are the environmental factors aimed to be Because auditory exostosis is not necessarily bilateral,
tested here as triggering the presence of auditory exosto- and archaeological material is generally fragmentary
ses. The State of Santa Catarina was divided into three and incomplete, frequencies were calculated using the
regions: Northern (NSC), Island (ISC), and Southern presence or absence of this trait per individual.
(SSC) because of differences in site implantation and the Because this bone anomaly is usually absent in juveniles
large number of sites in each of these areas. Six coastal (Bezold, 1885; DiBartolomeo, 1979; but see Sakalinskas
regions were used for analyses: Rio de Janeiro (RJ), São and Jankauskas, 1993), only adult individuals (with a

American Journal of Physical Anthropology—DOI 10.1002/ajpa


562 M.M.M. OKUMURA ET AL.
TABLE 2. Differences in the frequency of auditory exostoses
among the studied regions
Lagoa Santa Botocudo RJ SP PR NSC ISC
Botocudo NS
RJ NS NS
SP * */NS **
PR NS * * NS
NSC *** ** *** NS NS
ISC * ***/** *** NS NS NS
SSC *** *** *** * ** **/* *

NS, non significant; *significant at P  0.05; **significant at P


 0.01; and ***significant at P  0.001. Fisher exact test and v2
tests were used. Two symbols in the same cell indicate different
results using the Fisher exact test and v2 test, respectively.
Fig. 3. Frequency of auditory exostoses in each region.
White bars: inland groups and black bars: coastal groups. The
fused spheno-occipital suture) were used in this study. In numbers above the bars indicate the number of affected individ-
cases where this suture was not available, age determina- uals and the total number of individuals in which it was possi-
ble to detect the presence or absence of exostoses, respectively.
tion was based on dental eruption (Ubelaker, 1989), epiphy-
seal closure of long bones (Brothwell, 1981), and the degree
of cranial suture closure (Meindl and Lovejoy, 1985). Sex
was determined based on the standard criteria of pelvic and
cranial morphology (Buikstra and Ubelaker, 1994).
Some authors have emphasized the need to distinguish
between auditory exostosis and osteomata. In contrast
with auditory exostoses, osteomata are usually single
and unilateral, uncommon and characterized as bony
growths that present a small pedunculated base im-
planted over the tympanomastoid or tympanosquamous
sutures, projecting into the acoustic meatus (Graham,
1979; Kemink and Graham, 1982; Hyams et al., 1988:283;
Gervais, 1989; Fenton et al., 1996). Based on this defini-
tion, no osteomata were observed in the skeletal material
analyzed.

Fig. 4. Summer (white) and winter (black) sea surface tem-


perature of coastal regions studied (Castro and Miranda, 1998;
RESULTS Atlas de Cartas Piloto no. 14.200, 1993).

The frequency of auditory exostosis varies considerably


from unit to unit (Table 1). Frequencies at inland sites
are low and vary little (ranging from 0.00 to 0.03),
whereas frequencies at coastal sites span over a wide the inland groups exists. Finally, significantly higher fre-
range and reach high values (varying from 0.00 to 0.56). quencies of exostosis appear in coastal males than in
To test whether the observed cline in auditory exosto- inland males (P(v2) ¼ 0.02; P(Fisher) ¼ 0.01), while no
ses could be due to sex differences, we compared the difference exists between females.
smallest units of analysis (see column ‘‘unit’’ in Table 1) As expected, the frequencies of auditory exostosis in
using v2 and Fisher exact test. the inland groups are very low (from 0.00 to 0.03), with
The six units where men and women showed a fre- inland Lagoa Santa and Botocudo showing significantly
quency of zero could not be included in this analysis lower frequencies than any coastal group except RJ (Ta-
(Beirada, Corondó, Zé Espinho, Santo Amaro Island, ble 2). Increasing frequency of auditory exostoses among
Enseada, and Cerca Grande). The sample from Lapa regions is positively correlated with increasing latitude
Mortuária de Confins was also excluded, since it con- (from RJ to SSC) (Fig. 3). RJ presents 0.00 frequency of
sisted only of loose meatii that could not be sexed prop- auditory exostoses; significant differences are found
erly. From the remaining 20 units that could be tested, between RJ and all other coastal regions, but not
only the coastal shellmounds Cabeçuda and Ilha de between RJ and the inland groups of Lagoa Santa and
Espinheiros II present significant differences between Botocudo (Table 2). The frequency of auditory exostoses
sexes (Cabeçuda: P(v2) ¼ 0.03; P(Fisher) ¼ 0.04 and Ilha in individuals from sites in SSC is significantly higher
de Espinheiros II: P(v2) ¼ 0.02; P(Fisher) ¼ 0.05). When than in all other groups, both inland and coastal.
coastal units are considered together according to the The increasing frequency of auditory exostoses with
region (see column ‘‘region’’ in Table 1), only SSC shows increasing latitude of coastal site location requires an ex-
significantly higher frequencies in males than in planation. Sea surface temperatures (Fig. 4) decline with
females. When all coastal individuals are aggregated increasing latitude only in winter and vary relatively lit-
and compared with all inland individuals, only males tle from RJ to SSC (Castro and Miranda, 1998; Atlas de
from coastal settlements exhibit significantly more exos- Cartas Piloto no. 14.200, 1993). More importantly, sea
toses than do coastal females (P(v2) ¼ 0.00; P(Fisher) ¼ temperature in the studied area is always above or
0.00), while no significant difference between sexes in nearly above 198C, the threshold below which auditory

American Journal of Physical Anthropology—DOI 10.1002/ajpa


AUDITORY EXOSTOSES AS AQUATIC ACTIVITY MARKER 563

Fig. 5. Summer (white) and winter (black) atmospheric tem- Fig. 6. Summer (white) and winter (black) wind chill of
perature of coastal regions studied (Serra, 1969). coastal regions studied (Serra, 1960).

exostoses are believed to develop (Van Gilse, 1938; However, the coastal groups vary greatly in frequency
Fowler and Osmun, 1942; Kennedy, 1986). Atmospheric of auditory exostosis, although all of them show evidence
temperature was also tested. During summer, there is a of primarily marine resource-based diets. Explanations
small variation in atmospheric temperature (24–268C, of this variation include cultural factors, such as sexual
Fig. 5), but during winter, variation increases, with tem- labor division or distinct genetic composition.
peratures clearly getting lower with increasing latitude The lack of significant differences in frequencies of au-
(20–168C) (Serra, 1969). This difference in winter atmos- ditory exostosis between sexes in most of the Brazilian
pheric temperature is drastically amplified by wind chill coastal groups could be the result of a small sample size
(Fig. 6).1 In winter, wind chill increases greatly from RJ of individuals. In fact, the only sites that present signifi-
to Santa Catarina (150–250 kg cal/m2/h) (Serra, 1960). cant differences between sexes are Cabeçuda, with the
second largest sample size, and Ilha de Espinheiros II, a
small site, where four among 4 males and only one
among 5 females presented exostosis. However, when
DISCUSSION the frequencies of auditory exostoses are compared be-
tween coastal regions, only SSC presents differences
The purpose of this study is to test the usefulness between sexes. This suggests that both sexes were
of auditory exostoses as an aquatic activity marker in equally engaged in aquatic activities in these cases. This
tropical/subtropical regions, using prehistoric coastal and interpretation is supported by ethnographic data from
prehistoric and extant inland osteological materials from other regions. In Gran Canaria almost the same propor-
Brazil. The coastal groups consist of shellmound popula- tion of pre-Hispanic men and women present auditory
tions, whose subsistence depended heavily on aquatic exostoses (0.41 affected males against 0.39 affected
resources, whereas the inland groups included Paleoin- females), while old chronicles report that fishing and
dians and extant Botocudo who relied on terrestrial game shellfishing were performed by both men and women in
and plants. Two main hypotheses were tested: (1) if audi- this region (Velasco-Vazquez et al., 2000). In Tasmania,
tory exostoses are indicators of aquatic activities (such as Pietrusewsky (1984) found a high prevalence of auditory
swimming, diving and rowing), shellmound populations exostoses in native women (7.7%), who were the major
who depended on aquatic resources should show signifi- exploiters of aquatic resources. On the other hand,
cantly higher frequencies than inland groups whose sub- women from Murray River, Australia, who perform other
sistence was terrestrial and (2) if environmental factors functions than aquatic resource procurement, show signif-
influence auditory exostosis frequency in coastal groups, icantly lower frequencies of auditory exostosis (0.04) than
increasing frequency of auditory exostosis should parallel fishermen of their community (0.44) (Roche, 1964). The
decreasing water temperature and, especially, atmos- same picture emerges in a study of modern populations of
pheric temperature and increases in wind chill. We Arica (Chile), where almost 100% of the fishermen and di-
expected water temperature to have only a minimal influ- vers presented auditory exostoses, in contrast to only
ence, because water temperature along the Brazilian 6.6% of the nonfishing women (Corrales, 1999). However,
coast is always above or near the threshold temperature all of these studies were performed with large sample
of 198C, below which auditory exostosis are reported to sizes, and for the small number of individuals studied
develop (Van Gilse, 1938; Fowler and Osmun, 1942). from each Brazilian site analyzed herein, any statement
Indeed, the frequency of auditory exostoses among about the lack of sexual labor division is preliminary.
inland Brazilian groups is very low (0.00–0.03), and also On the other hand, differential genetic predisposition
significantly lower than in most coastal groups (0.00–0.56). to auditory exostosis has not been entirely ruled out,
This finding is in accordance with previous studies in although many evidences point to a homogeneous compo-
which coastal groups show higher frequencies of auditory sition of most of the coastal groups analyzed. Individuals
exostoses than inland groups (Finnegan, 1972; Kennedy, presenting distinct genetic predisposition may or may
1986; Standen et al., 1997; Velasco-Vazquez et al., 2000). not develop auditory exostosis even if exposed to the
same environmental factors. One of the methods possible
1
Wind chill is calculated using the formula: K0 ¼ [(100v)1/2 + to use in such cases are biodistance studies, be they met-
10.45 – v] (33 – Ta), with K0 ¼ total refrigerating effect (kg cal/m2/ ric, nonmetric, cranial, or dental. Some biodistance stud-
h); v ¼ wind velocity (m/s); Ta ¼ atmospheric temperature. ies have been carried out on Brazilian shellmound collec-

American Journal of Physical Anthropology—DOI 10.1002/ajpa


564 M.M.M. OKUMURA ET AL.

tions (Neves, 1988; Bartolomucci, 2005; Hubbe, 2005; ing, develop severe exostoses significantly faster than
Filippini and Eggers, in press; Okumura and Neves, sportsmen in the ‘underwater’ group.’’
2005; 2006; Okumura et al., 2006), and most of them point Therefore, if auditory exostoses are more likely to de-
to a relative similarity between these coastal groups, velop in individuals performing ‘‘above water’’ activities,
especially when compared to Brazilian inland groups, protecting ears from the refrigerating action of atmos-
although small differences between them do exist. pheric temperature and wind chill may be a simple and
Therefore, although differences in sexual labor and efficient means of avoiding the development of auditory
genetic composition could be responsible for some of the exostoses. Although the efficiency of the use of earplugs
differences in frequencies of auditory exostosis reported, or hoods to avoid auditory exostosis development
most of them must be related to distinct environmental remains controversial (Graham, 1979; Fenton et al.,
factors that these coastal groups were exposed to on 1996; Timofeev et al., 2004), ethnographic data confirm
daily activities. While the low frequency of auditory that when the meatus is protected from cold wind and
exostoses in coastal RJ is similar to that of inland Bra- low atmospheric temperature, intense contact with water
zilian sites, the high proportion of auditory exostoses does not trigger auditory exostoses. Coastal Eskimos,
among southern Brazilian coastal groups (such as those who are strongly dependent on marine resources and
of SSC with a mean frequency of 0.37) are within the use boats extensively, rarely present auditory exostoses
range of frequencies reported for many coastal popula- (Finnegan, 1972), probably due to the constant use of
tions worldwide (frequencies ranging from 0.31 to 0.40), hoods.
and comparable to those of modern surfers, divers, and Exostoses develop as a result of the refrigeration
sailors, with frequencies varying from 0.46 to 0.99 action of the meatus. In fact, Van Gilse (1938) conducted
(Fabiani et al., 1984; Umeda et al., 1989; Manzi et al., an experiment in order to test the meatal reflex of hiper-
1991; Standen et al., 1997; Corrales, 1999; Velasco- emia when the meatus was stimulated with cold (158C)
Vazquez et al., 2000; Kroon et al., 2002; Altuna Mariez- or warm water (408C), and he found that the meatal ery-
kurrena et al., 2004). thema following the cold water irrigation of the meatus
The increase in auditory exostosis frequency from RJ was definitively prolonged. The periosteum of the ear
to SSC is coincident with decreasing atmospheric tem- canal is easily traumatized by some irritative stimuli
perature and increasing wind chill. This suggests that such as the thermic shock, resulting from exposure of
these environmental factors trigger auditory exostosis, the auditory canal to cold, stimulating osteogenic activ-
because water temperature varies little and generally ity. Vasodilatation associated with cold exposure seems
remains above the 198C threshold. Ito and Ikeda (1998) to cause increased tension on the periosteum, resulting
reached similar conclusions; ‘‘cold water navy divers’’ in osteoblastic activity. Continuous exposure to cold can
showed significantly more exostoses than ‘‘warm water trigger a local reaction of the ear’s soft tissue, which
navy divers,’’ which was attributed primarily to differen- leads to the stimulation of osteogenic cell activities and
ces in atmospheric temperature and wind chill, not finally, to exostosis (Belgraver, 1938; Fowler and Osmun,
water temperature. 1942; Harrison, 1951, 1962; DiBartolomeo, 1979; Filipo
Among the Brazilian coastal shellmound groups stud- et al., 1982; Fabiani et al., 1984). Accordingly, the refrig-
ied, atmospheric temperature in conjunction with wind erating effect of the meatus to cold water can be
chill appear to be the main causative factor of auditory enhanced by the chill effect caused by low atmospheric
exostoses, whereas water temperature plays only a temperature and wind.
minor role in the development of this trait. Although the Thus, the absence of auditory exostoses does not exclude
correlation of higher frequencies of exostosis in coastal aquatic activities. Auditory exostosis may fail to form de-
regions with lower atmospheric temperatures and higher spite aquatic activities, especially when water temperature
wind chill factors is provocative, it does not prove causal- is above 198C, atmospheric temperature is high, and the
ity, as discussed later. However, these findings represent wind chill effect is low. As demonstrated by the southeast-
the most parsimonious conclusions available to date, ern Brazilian coastal sites studied here, this situation
based on these osteological collections. The populations occurs more frequently in warm regions (but also among
studied provide the advantage of including groups coastal Eskimos with protected meatii). Thus, auditory
clearly adapted to the aquatic environment, living in exostoses as an aquatic activity marker in tropical and sub-
and from it, as well as inland groups that show no de- tropical regions should be used only cautiously.
pendence on aquatic activities. We hope this study will encourage future research
Although numerous mollusk shells suggest that the that includes environmental factors beyond traditionally
shellmound people practiced underwater activities, such proposed water temperature, making important contri-
as diving, hooks and net weights in the archaeological butions to the growing body of bioarchaeological litera-
record indicate that many aquatic activities were per- ture on skeletal markers of human activity patterns.
formed above water. However, the high frequency of audi-
tory exostoses in some of these groups is not surprising,
because even above water, the auditory canal can be sub- ACKNOWLEDGMENTS
jected to water jets that trigger the development of this
trait when in contact with low atmospheric temperatures We thank the staff and curators of the following institu-
and strong wind chill. Fabiani et al. (1984) reported the tions for allowing us to examine skeletons in their care:
presence of auditory exostoses in 37% of sailors, explain- Hilton Pereira da Silva, Sheila Mendonça de Souza, and
ing that ‘‘this sport, although it does not actively involve Claudia Rodrigues-Carvalho of the Museu Nacional
immersion of the head, may expose the subjects to contin- (UFRJ-RJ); Lı́lia Cheuiche Carvalho (in memoriam) of the
uous cold water jets causing rapid perfrigeration in the Instituto de Arqueologia Brasileira (RJ); Murillo Marx
external auditory canal under the action of wind.’’ Fur- and Dorath Uchôa of the Museu de Arqueologia e Etnolo-
thermore, Timofeev et al. (2004) state that ‘‘people partici- gia (USP-SP); Cláudia Parrellada of the Museu Para-
pating in ‘above water’ activities, such as surfing and sail- naense (PR); Igor Chmyz of the Centro de Estudos e Pes-

American Journal of Physical Anthropology—DOI 10.1002/ajpa


AUDITORY EXOSTOSES AS AQUATIC ACTIVITY MARKER 565
quisas Arqueológicas (UFPR-PR); Ana Luiza Fayet Chaplin JM, Stewart IA. 1998. The prevalence of exostoses in
Salla and Patrı́cia Gaulier of the Museu de Arqueologia the external auditory meatus of surfers. Clin Otolaryngol
e Etnologia (UFPR-PR); Gelci José Coelho, Teresa 23:326–330.
Domitila Fossari, Cristina Castellano, and Hermes José Corrales J. 1999. Presencia de exostosis en el meato acus-
tico externo en la población de Arica. Rev Chil Anat 17:103–
Graipel Jr. of the Museu Universitário ‘‘Professor
128.
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Bandeira, Adriana Maria Pereira dos Santos, and references for the discussion of complexity among the Samba-
Maria Cristina Alves of the Museu Arqueológico do qui moundbuilders from the southern shores of Brazil. Rev
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De Masi MAN. 2001. Pescadores coletores da costa sul do Brasil.
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