Auditory exostoses as an aquatic activity marker - Wiley Online Library

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 Ce´lia H.C. Boyadjian,2 and Sabine Eggers2* 1

Laborato´rio de Estudos Evolutivos Humanos, Depto. de Gene´tica e Biologia Evolutiva, Instituto de Biocieˆncias, Universidade de Saõ Paulo, 05422-970 Saõ Paulo, SP, Brazil 2 Laborato´rio Antropologia Biolo´gica, Depto. de Gene´tica e Biologia Evolutiva, Instituto de Biocieˆncias, Universidade de Saõ Paulo, 05422-970 Saõ Paulo, SP, Brazil KEY WORDS

shellmound; Paleoindian; Botocudo; Brazilian archaeology; bioarchaeology

ABSTRACT Auditory exostoses are bone masses located in the external auditory canal. Currently, most researchers agree that the environment (especially water temperature, but also atmospheric temperature and wind action) plays a pivotal role in the development of this trait. This article discusses whether the presence of auditory exostoses can be used as an aquatic activity marker in bioarchaeological studies, especially in groups that inhabited tropical and subtropical regions. We analyzed 676 skeletons (5,000 years BP to historical times) from 27 coastal and inland native Brazilian groups. Very low frequencies of auditory exostoses were found in the inland groups (0.00–0.03), but the expected high frequency of auditory exostoses in the coastal groups was not always observed (0.00–0.56). These differences might be explained by the combination of water and atmospheric

temperatures in conjunction with wind effects. In areas with mild atmospheric temperatures and wind chill factors, the coastal populations analyzed do not show high frequencies of auditory exostoses. However, high frequencies of auditory exostoses develop where cold atmospheric temperatures are further lowered by strong wind chill. Therefore, the association between aquatic activities, low atmospheric temperature, and wind chill is strongly correlated with the presence of auditory exostoses, but where these environmental factors are mild, the frequencies of auditory exostoses are not necessarily high. Concluding, auditory exostoses should be cautiously used as a marker of aquatic activity in bioarchaeological studies in tropical and subtropical regions, since these activities do not always result in the presence of this trait. Am J Phys Anthropol 132:558–567, 2007. V 2007 Wiley-Liss, Inc.

Auditory exostoses are bone anomalies mainly located on the floor of the external auditory canal, medial to the sutures of the tympanic plate (for a complete review of this trait, see Hauser and De Stefano, 1989). Auditory exostoses have an extensive base and can be bilateral and multiple (Sheehy, 1982; Hyams et al., 1988) (Fig. 1). Auditory exostoses have been recorded in ancient skeletal remains worldwide: Mesolithic Yugoslavians, pre-Hispanic individuals from the Canary Islands (1,700– 540 years BP), Chileans (7000 B.C. to 1450 A.D.), preColumbian South American mummies, Lithuanians (from the Neolithic to the 17th–18th century A.D.), and individuals from Imperial Rome (1st–3rd century A.D.) (Frayer, 1988; Manzi et al., 1991; Sakalinskas and Jankauskas, 1993; Standen et al., 1997; Gerszten et al., 1998; VelascoVazquez et al., 2000). Auditory exostoses have also been observed in Neanderthals and some European Middle Pleistocene individuals excavated at Sima de los Huesos (Boule, 1911–1913; Trinkaus, 1983:70, 411; Pe´rez et al., 1997). Today, this trait is common in individuals who practice aquatic sports (Van Gilse, 1938; Adams, 1951; Dettman and Reuter, 1964; DiBartolomeo, 1979; Scrivener, 1981; Filipo et al., 1982; Kemink and Graham, 1982; Fabiani et al., 1984; Kennedy, 1986; Umeda et al., 1989; Deleyiannis et al., 1996; Kroon et al., 2002), and prevalence of auditory exostoses and degree of canal obstruction are positively correlated with intensity and number of years involved in aquatic sports (Fowler and Osmun, 1942; Umeda et al., 1989; Deleyiannis et al., 1996; Kroon et al., 2002; Altuna Mariezkurrena et al., 2004).

From the 19th century until recently, the cause of auditory exostoses was thought to be genetic (Blake, 1880; Hartmann, 1893; Berry, 1975). However, an exclusively genetic origin of this trait has recently been rejected, because ancestry has not been shown to be significantly related to the prevalence of auditory exostoses (Kroon et al., 2002). Furthermore, several researchers who supported the genetic hypothesis have also cited chemical or mechanical stimuli that lead to irritation of the auditory canal as possible underlying causes of the development of auditory exostoses (Hrdlicka, 1935; Berry and Berry,

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Grant sponsor: FAPESP: Grant numbers: 02/13441-0, 04/11038-0; Grant sponsor: CNPq; Grant sponsor: FAPESP-CEPID; Grant number: 98/14354-2; Grant sponsor: PIBIC-CNPq. *Correspondence to: Sabine Eggers, Laborato´rio de Antropologia Biolo´gica, Depto. de Gene´tica e Biologia Evolutiva, Instituto de Biocieˆncias, Universidade de Saõ Paulo, CP 11461, 05422-970 Saõ Paulo, SP, Brazil. E-mail: [email protected] Present address of Maria Mercedes M. Okumura: Leverhulme Centre for Human Evolutionary Studies, The Henry Wellcome Building, University of Cambridge, Fitzwilliam Street, Cambridge CB2 1QH, UK. Received 31 January 2006; accepted 7 November 2006 DOI 10.1002/ajpa.20544 Published online 22 January 2007 in Wiley InterScience (www.interscience.wiley.com).

AUDITORY EXOSTOSES AS AQUATIC ACTIVITY MARKER

Fig. 1. Auditory exostosis as observed in skeletal material.

1967; Berry, 1975; Hutchinson et al., 1997). Currently, most researchers agree that auditory exostoses are probably caused by environmental factors, and genetic predisposition has only a minor role in the development of this trait (Field, 1878; Van Gilse, 1938; Fowler and Osmun, 1942; Harrison, 1962; Fabiani et al., 1984; Kennedy, 1986; Peixoto, 1989; Standen et al., 1997; Chaplin and Stewart, 1998; Velasco-Vazquez et al., 2000; Kroon et al., 2002). While water salinity (Peixoto, 1989) and wind effect (Fabiani et al., 1984) are among the environmental factors reported to cause auditory exostoses, low water temperature is the most frequently cited factor. Although the exact temperature necessary to trigger the development of auditory exostoses has not been established, considerable physiological changes occur in the human ear canal when exposed to water temperatures below 198C (Van Gilse, 1938; Fowler and Osmun, 1942). Significantly higher prevalence of auditory exostoses has been reported in individuals in contact with cold water (Van Gilse, 1938; Fowler and Osmun, 1942; Harrison, 1962; Kennedy, 1986; Standen et al., 1997; Chaplin and Stewart, 1998; Ito and Ikeda, 1998; Velasco-Vazquez et al., 2000). Additionally, cold-water athletes are more likely to develop auditory exostoses than are warm-water athletes (Ito and Ikeda, 1998; Kroon et al., 2002). Inland populations, which lack intense contact with water, present very low frequencies of auditory exostoses. This is the case among the inland Salish, with a frequency of 0.03 (Finnegan, 1972), the central highlanders from Gran Canaria with a frequency of 0.01 (Velasco-Vazquez et al., 2000), and inhabitants of Chilean valleys and highlands with 0.02 and 0.00, respectively (Standen et al., 1997). Similarly, participants of nonaquatic sports were found to have no auditory exostoses (Fabiani et al., 1984). However, the association of low frequencies of exostoses in inland groups and high frequencies in coastal populations is not always straightforward. Development of auditory exostosis also appears to depend on the use of ear protection in the form of earplugs and/or hoods, which mitigate wind chill or low atmospheric temperatures or both, therefore, preventing the auditory canal to cool off (Deleyiannis et al., 1996; Timofeev et al., 2004; Zoltan et al., 2005).

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The purpose of this study is to investigate whether auditory exostoses are an accurate aquatic activity marker in tropical and subtropical regions. We seek to answer two related questions: (1) are auditory exostoses indicators of activities associated with the aquatic environment? and (2) do environmental factors such as atmospheric 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 systematic multisite study of auditory exostosis in tropical and subtropical regions we are aware of. The inland groups (Paleoindians and Botocudo) based their subsistence on terrestrial game and plants, whereas the coastal groups (shellmound builders) subsisted on fish and marine mollusks. Regarding the first question, inland groups are expected to present little or no auditory exostosis, whereas groups adapted to aquatic environments should show higher frequencies of auditory exostosis. To answer the second question, we considered the variation not only of sea water temperature, but also of atmospheric temperature and wind chill. Coastal groups are divided according to geographic location, which coincides with increasing latitude and consequently decreasing water and atmospheric temperature, and increasing wind chill. If these environmental factors influence the frequency of auditory exostosis, low water temperature, low atmospheric temperature, and high wind chill will coincide with higher frequency of this trait in the coastal groups of the highest latitudes.

MATERIALS AND METHODS Materials The geographic distribution of the groups studied is shown in Figure 2. Inland sites. Brazilian inland skeletal remains are usually scarce because of acidic tropical soil, which prevents the preservation of organic remains. With the exception of two fairly large collections, Lagoa Santa and Botocudo, no other inland collections are available. The skeletal series of Paleoindians from Lagoa Santa (Minas Gerais State) comprises a large number of prehistoric inland individuals in a reasonable state of preservation. Most of these hunter-gatherer groups inhabited Lagoa Santa from 11,000 to 8,000 BP. Several studies have been performed on the skeletal remains from this region since the work of Peter Lund in the 19th century, and these remains are the most significant evidence that the New World was first colonized by a non-Mongoloid population (Powell and Neves, 1999; Neves et al., 2004). Although megafauna was contemporaneous with Paleoindian groups in Lagoa Santa (Neves and Pilo´, 2003), their diet was based on small animals (Araujo et al., 2002). A high frequency of dental caries (9%) at two Paleoindian sites from Lagoa Santa (not included in our study) suggests a plant-based diet rich in carbohydrates (Neves and Cornero, 1997; Neves and Kipnis, 2004). The other inland group used in this analysis is a recent (postcontact) group of Brazilian natives called Botocudo (also known as Krena´k). They were huntergatherers with a clear sexual division of labor: men hunted and women were responsible for gathering. The original territory of the Botocudo was the Atlantic Rain

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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, Saõ Paulo; PR, Parana´; NSC, Northern Santa Catarina; ISC, Island of Santa Catarina; SSC, Southern Santa Catarina.

Forest. They were expelled from the coast by another native group, the Tupi, and occupied a parallel stretch of forest between the Atlantic Rain Forest and the edge of the Brazilian Plateau. In the 19th century, the Botocudo groups moved south. This vast and scattered inland distribution was a response to the European conquest as well as wars between the Botocudo and their native enemies (Paraı´so, 1991, 1992). In 1939, the tribe numbered fewer than 100 individuals (IBGE, 2002). The osteological series analyzed derives from the last half of the 19th century and encompasses individuals from three neighboring states: Bahia, Espı´rito Santo, and Minas Gerais. Coastal sites. Shellmounds, common archaeological sites scattered along most of the 8,000 km of the Brazilian coast, represent an excellent opportunity for the study of auditory exostoses. More than 1,000 sites are mapped (Gaspar, 1998), and although only some of these sites have been studied intensely, they represent a cultural unit that expanded over a huge geographical area and spanned *6,000 years (Gaspar, 1992, 1994/1995, 1996; De Blasis et al., 1998). Brazilian shellmounds vary in size and can reach 30 m in height. They consist of complex sequences of layers of shells and sand, containing food remains, hearths, technological implements, and elaborate burials associated with bone and stone artefacts and ochre. These shellmounds are currently considered as monumental constructions intentionally built by sedentary people with high population densities (De Blasis et al., 1998; Gaspar, 1998). The geographic location of many shellmounds, the occupation of islands, and the capture of deep-sea fish species indicate the use of boats by these coastal people (Gaspar, 2000; Teno´rio, 2000). Zooarchaeological and stable isotope studies have shown that these groups were fisher-gatherers with diets based on marine resources (Figuti, 1992,

1999; De Masi, 1999, 2001). Consumption of plants, however, was more common than was believed until recently (Scheel-Ybert, 1998, 2001; Wesolowski, 2000, Scheel-Ybert et al., 2003). Intense dental wear in these skeletal remains is attributed to the admixture of sand, shellfish fragments, and phytoliths present in the food (Reinhard et al., 2001). Although the coastal Brazilian shellmound builders were of relatively low stature, they were within the range of variation of prehistoric and extant Native Americans (Storto et al., 1999). Frequent nonspecific infections in many shellmound dwellers are attributed to the intense contact with animal remains and pathogens typical of tropical coastal areas (Mendonça de Souza, 1995). There is also evidence of communicable infectious diseases in some of the sites, suggesting high demographic density, and although many neighboring sites are contemporaneous, an overall low frequency of violent trauma among shellmound dwellers indicates a relatively peaceful lifestyle and little competition for food resources (Lessa and Medeiros, 2001; Okumura and Eggers, 2005). The shellmounds included in this study are located in four adjacent coastal states of Southeastern Brazil (Rio de Janeiro, Saõ Paulo, Parana´, and Santa Catarina), dated to between 5,000 and 800 years BP. They represent the main temporal and geographic distribution of shellmounds in this country. Units included in this study are defined as follows: archaeological site, in the case of coastal shellmounds and Lagoa Santa; archaeological region, in the case of Santo Amaro Island; or group, in the case of Botocudo. Each unit consists of at least eight individuals. This arbitrary number was chosen because a larger one would have excluded several important sites from this study, since usually scarce skeletal material is exhumated from most of the shellmounds. The selection criteria also included the amount of information avail-


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TABLE 1. Frequencies of individuals affected with auditory exostosis in each unit analyzed, organized from north to south of Brazil

Unit Inland Botocudo Cerca Grande Lapa Mortua´ria de Confins Coast Beirada Corondo´ Ze´ Espinho Piaçaguera Santo Amaro island (region) Teno´rio Guaraguaçu Matinhos Cabeçudas Enseada Forte Marechal Luz Ilha de Espinheiros II Itacoara Laranjeiras II Morro do Ouro Rio Comprido Armaçaõ do Sul Base Ae´rea Ponta das Almas Tapera Balsinha Cabeçuda Içara Jabuticabeira II

Region (state of origin) BA, ES, MG Lagoa Santa (MG) Lagoa Santa (MG) RJ RJ RJ SP SP SP PR PR NSC NSC NSC NSC NSC NSC NSC NSC ISC ISC ISC ISC SSC SSC SSC SSC

N individuals

N individuals affected with exostosis

Frequency

N affected males/N affected females

Mid-Late XIX century 9130 6 30

40

1

0.03

1/0

8

0

0.00

0/0

8810 6 50

50

1

0.02

–

6 6 6 6 – 1875 6 4220 6 2750 6 – – 4290 6 2970 6 1570 6 – 4030 6 – 2670 6 800 6 4289 6 1140 6 3780 6 4120 6 1160 6 2880 6

11 32 11 21 13 13 30 19 16 22 14 9 22 28 37 31 13 36 9 70 14 74 14 19

0 0 0 5 0 3 4 3 5 0 1 5 2 4 7 17 2 8 1 20 3 32 7 3

0.00 0.00 0.00 0.24 0.00 0.23 0.13 0.16 0.31 0.00 0.07 0.56 0.09 0.14 0.19 0.55 0.15 0.22 0.11 0.29 0.21 0.43 0.50 0.16

0/0 0/0 0/0 3/1 0/0 2/1 3/0 2/1 4/1 0/0 1/0 4/1 1/1 4/0 2/4 4/5 2/0 6/2 1/0 11/8 3/0 13/12 7/0 3/0

Oldest date

5420 4260 2260 4930

190 75 160 110 90 200 250 130 60 20 40 90 70 400 180 90 220 50 75

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 necessary for inclusion of a site were published reports on the excavation, daily logs, descriptions of material culture, published dates, and various sources of data concerning diet and subsistence. Unfortunately, there are almost no skeletal remains from the Northern coastal regions because of the scarcity of archaeological surveys and the paucity of shellmounds (Amaˆncio and Dominguez, 2003). Additionally, many researchers have proposed that the shellmounds from Northern and Northeastern Brazil belong to a different cultural complex from the Southern–Southeastern shellmounds analyzed here (Lima, 1999/2000; Prous, 1991:293; but see Gaspar and Imazio, 1999 for a different view). Preliminary statistical analyses concerning differences in the frequency of auditory exostoses were carried out using the ‘‘unit’’ column of Table 1 (data not shown), but the small sample size prevented their use in other analyses. Therefore, some units were grouped by state of origin (Table 1). This is justified because, in this part of Brazil, political state distribution follows increasing latitude and consequently decreasing water and atmospheric temperature, and increasing wind chill. As stated before, these are the environmental factors aimed to be tested here as triggering the presence of auditory exostoses. The State of Santa Catarina was divided into three regions: Northern (NSC), Island (ISC), and Southern (SSC) because of differences in site implantation and the large number of sites in each of these areas. Six coastal regions were used for analyses: Rio de Janeiro (RJ), Saõ

Paulo (SP), Parana´ (PR), Northern Santa Catarina (NSC), Island of Santa Catarina (ISC), and Southern Santa Catarina (SSC). These six coastal regions comprise 23 archaeological sites and one archaeological unit called ‘‘Santo Amaro Island.’’ This unit consists of 12 skeletons exhumated from shellmounds on Santo Amaro Island (Saõ Paul state) in the early 20th century (Imbelloni, 1956/1958). Although no detailed information on provenience exists, this is an important collection, because most of the shellmounds in this area were destroyed by later urban development. Among inland groups, Paleoindians from Lagoa Santa (consisting of two archaeological sites) and Botocudo were considered separately. In total, we analyzed six coastal and two inland regions.

Methods Data were recorded for 676 individuals with at least one intact auditory canal (307 males, 258 females, and 111 of undetermined sex). The external auditory canal was examined with the naked eye and, when necessary, with the aid of a magnifying glass and a small lamp. Because auditory exostosis is not necessarily bilateral, and archaeological material is generally fragmentary and incomplete, frequencies were calculated using the presence or absence of this trait per individual. Because this bone anomaly is usually absent in juveniles (Bezold, 1885; DiBartolomeo, 1979; but see Sakalinskas and Jankauskas, 1993), only adult individuals (with a


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TABLE 2. Differences in the frequency of auditory exostoses among the studied regions

Botocudo RJ SP PR NSC ISC SSC

Lagoa Santa

Botocudo

RJ

SP

PR

NSC

ISC

NS NS * NS *** * ***

NS */NS * ** ***/** ***

** * *** *** ***

NS NS NS *

NS NS **

NS **/*

*

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.

fused spheno-occipital suture) were used in this study. In cases where this suture was not available, age determination was based on dental eruption (Ubelaker, 1989), epiphyseal 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 implanted 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 definition, no osteomata were observed in the skeletal material analyzed.

Fig. 3. Frequency of auditory exostoses in each region. White bars: inland groups and black bars: coastal groups. The numbers above the bars indicate the number of affected individuals and the total number of individuals in which it was possible to detect the presence or absence of exostoses, respectively.

RESULTS

Fig. 4. Summer (white) and winter (black) sea surface temperature of coastal regions studied (Castro and Miranda, 1998; 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 range and reach high values (varying from 0.00 to 0.56). To test whether the observed cline in auditory exostoses could be due to sex differences, we compared the smallest units of analysis (see column ‘‘unit’’ in Table 1) using v2 and Fisher exact test. The six units where men and women showed a frequency of zero could not be included in this analysis (Beirada, Corondo´, Ze´ Espinho, Santo Amaro Island, Enseada, and Cerca Grande). The sample from Lapa Mortua´ria de Confins was also excluded, since it consisted only of loose meatii that could not be sexed properly. From the remaining 20 units that could be tested, only the coastal shellmounds Cabeçuda and Ilha de Espinheiros II present significant differences between sexes (Cabeçuda: P(v2) ¼ 0.03; P(Fisher) ¼ 0.04 and Ilha de Espinheiros II: P(v2) ¼ 0.02; P(Fisher) ¼ 0.05). When coastal units are considered together according to the region (see column ‘‘region’’ in Table 1), only SSC shows significantly higher frequencies in males than in females. When all coastal individuals are aggregated and compared with all inland individuals, only males from coastal settlements exhibit significantly more exostoses than do coastal females (P(v2) ¼ 0.00; P(Fisher) ¼ 0.00), while no significant difference between sexes in

the inland groups exists. Finally, significantly higher frequencies of exostosis appear in coastal males than in inland males (P(v2) ¼ 0.02; P(Fisher) ¼ 0.01), while no difference exists between females. As expected, the frequencies of auditory exostosis in the inland groups are very low (from 0.00 to 0.03), with inland Lagoa Santa and Botocudo showing significantly lower frequencies than any coastal group except RJ (Table 2). Increasing frequency of auditory exostoses among regions is positively correlated with increasing latitude (from RJ to SSC) (Fig. 3). RJ presents 0.00 frequency of auditory exostoses; significant differences are found between RJ and all other coastal regions, but not between RJ and the inland groups of Lagoa Santa and Botocudo (Table 2). The frequency of auditory exostoses in individuals from sites in SSC is significantly higher than in all other groups, both inland and coastal. The increasing frequency of auditory exostoses with increasing latitude of coastal site location requires an explanation. Sea surface temperatures (Fig. 4) decline with increasing latitude only in winter and vary relatively little from RJ to SSC (Castro and Miranda, 1998; Atlas de Cartas Piloto no. 14.200, 1993). More importantly, sea temperature in the studied area is always above or nearly above 198C, the threshold below which auditory



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Fig. 5. Summer (white) and winter (black) atmospheric temperature of coastal regions studied (Serra, 1969).

Fig. 6. Summer (white) and winter (black) wind chill of coastal regions studied (Serra, 1960).

exostoses are believed to develop (Van Gilse, 1938; Fowler and Osmun, 1942; Kennedy, 1986). Atmospheric temperature was also tested. During summer, there is a small variation in atmospheric temperature (24–268C, Fig. 5), but during winter, variation increases, with temperatures clearly getting lower with increasing latitude (20–168C) (Serra, 1969). This difference in winter atmospheric temperature is drastically amplified by wind chill (Fig. 6).1 In winter, wind chill increases greatly from RJ to Santa Catarina (150–250 kg cal/m2/h) (Serra, 1960).

However, the coastal groups vary greatly in frequency of auditory exostosis, although all of them show evidence of primarily marine resource-based diets. Explanations of this variation include cultural factors, such as sexual labor division or distinct genetic composition. The lack of significant differences in frequencies of auditory exostosis between sexes in most of the Brazilian coastal groups could be the result of a small sample size of individuals. In fact, the only sites that present significant 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 the frequencies of auditory exostoses are compared between coastal regions, only SSC presents differences between sexes. This suggests that both sexes were equally engaged in aquatic activities in these cases. This interpretation is supported by ethnographic data from other regions. In Gran Canaria almost the same proportion of pre-Hispanic men and women present auditory exostoses (0.41 affected males against 0.39 affected females), while old chronicles report that fishing and shellfishing were performed by both men and women in this region (Velasco-Vazquez et al., 2000). In Tasmania, Pietrusewsky (1984) found a high prevalence of auditory exostoses in native women (7.7%), who were the major exploiters of aquatic resources. On the other hand, women from Murray River, Australia, who perform other functions than aquatic resource procurement, show significantly lower frequencies of auditory exostosis (0.04) than fishermen of their community (0.44) (Roche, 1964). The same picture emerges in a study of modern populations of Arica (Chile), where almost 100% of the fishermen and divers presented auditory exostoses, in contrast to only 6.6% of the nonfishing women (Corrales, 1999). However, all of these studies were performed with large sample sizes, and for the small number of individuals studied from each Brazilian site analyzed herein, any statement about the lack of sexual labor division is preliminary. On the other hand, differential genetic predisposition to auditory exostosis has not been entirely ruled out, although many evidences point to a homogeneous composition of most of the coastal groups analyzed. Individuals presenting distinct genetic predisposition may or may not develop auditory exostosis even if exposed to the same environmental factors. One of the methods possible to use in such cases are biodistance studies, be they metric, nonmetric, cranial, or dental. Some biodistance studies have been carried out on Brazilian shellmound collec-

DISCUSSION The purpose of this study is to test the usefulness of auditory exostoses as an aquatic activity marker in tropical/subtropical regions, using prehistoric coastal and prehistoric and extant inland osteological materials from Brazil. The coastal groups consist of shellmound populations, whose subsistence depended heavily on aquatic resources, whereas the inland groups included Paleoindians and extant Botocudo who relied on terrestrial game and plants. Two main hypotheses were tested: (1) if auditory exostoses are indicators of aquatic activities (such as swimming, diving and rowing), shellmound populations who depended on aquatic resources should show significantly higher frequencies than inland groups whose subsistence was terrestrial and (2) if environmental factors influence auditory exostosis frequency in coastal groups, increasing frequency of auditory exostosis should parallel decreasing water temperature and, especially, atmospheric temperature and increases in wind chill. We expected water temperature to have only a minimal influence, because water temperature along the Brazilian coast is always above or near the threshold temperature of 198C, below which auditory exostosis are reported to develop (Van Gilse, 1938; Fowler and Osmun, 1942). Indeed, the frequency of auditory exostoses among inland Brazilian groups is very low (0.00–0.03), and also significantly lower than in most coastal groups (0.00–0.56). This finding is in accordance with previous studies in which coastal groups show higher frequencies of auditory exostoses than inland groups (Finnegan, 1972; Kennedy, 1986; Standen et al., 1997; Velasco-Vazquez et al., 2000). 1 Wind chill is calculated using the formula: K0 ¼ [(100v)1/2 + 10.45 – v] (33 – Ta), with K0 ¼ total refrigerating effect (kg cal/m2/ h); v ¼ wind velocity (m/s); Ta ¼ atmospheric temperature.


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tions (Neves, 1988; Bartolomucci, 2005; Hubbe, 2005; Filippini and Eggers, in press; Okumura and Neves, 2005; 2006; Okumura et al., 2006), and most of them point to a relative similarity between these coastal groups, especially when compared to Brazilian inland groups, although small differences between them do exist. Therefore, although differences in sexual labor and genetic composition could be responsible for some of the differences in frequencies of auditory exostosis reported, most of them must be related to distinct environmental factors that these coastal groups were exposed to on daily activities. While the low frequency of auditory exostoses in coastal RJ is similar to that of inland Brazilian sites, the high proportion of auditory exostoses among southern Brazilian coastal groups (such as those of SSC with a mean frequency of 0.37) are within the range of frequencies reported for many coastal populations worldwide (frequencies ranging from 0.31 to 0.40), and comparable to those of modern surfers, divers, and sailors, with frequencies varying from 0.46 to 0.99 (Fabiani et al., 1984; Umeda et al., 1989; Manzi et al., 1991; Standen et al., 1997; Corrales, 1999; VelascoVazquez et al., 2000; Kroon et al., 2002; Altuna Mariezkurrena et al., 2004). The increase in auditory exostosis frequency from RJ to SSC is coincident with decreasing atmospheric temperature and increasing wind chill. This suggests that these environmental factors trigger auditory exostosis, because water temperature varies little and generally remains above the 198C threshold. Ito and Ikeda (1998) reached similar conclusions; ‘‘cold water navy divers’’ showed significantly more exostoses than ‘‘warm water navy divers,’’ which was attributed primarily to differences in atmospheric temperature and wind chill, not water temperature. Among the Brazilian coastal shellmound groups studied, atmospheric temperature in conjunction with wind chill appear to be the main causative factor of auditory exostoses, whereas water temperature plays only a minor role in the development of this trait. Although the correlation of higher frequencies of exostosis in coastal regions with lower atmospheric temperatures and higher wind chill factors is provocative, it does not prove causality, as discussed later. However, these findings represent the most parsimonious conclusions available to date, based on these osteological collections. The populations studied provide the advantage of including groups clearly adapted to the aquatic environment, living in and from it, as well as inland groups that show no dependence on aquatic activities. Although numerous mollusk shells suggest that the shellmound people practiced underwater activities, such as diving, hooks and net weights in the archaeological record indicate that many aquatic activities were performed above water. However, the high frequency of auditory exostoses in some of these groups is not surprising, because even above water, the auditory canal can be subjected to water jets that trigger the development of this trait when in contact with low atmospheric temperatures and strong wind chill. Fabiani et al. (1984) reported the presence of auditory exostoses in 37% of sailors, explaining that ‘‘this sport, although it does not actively involve immersion of the head, may expose the subjects to continuous cold water jets causing rapid perfrigeration in the external auditory canal under the action of wind.’’ Furthermore, Timofeev et al. (2004) state that ‘‘people participating in ‘above water’ activities, such as surfing and sail-

ing, develop severe exostoses significantly faster than sportsmen in the ‘underwater’ group.’’ Therefore, if auditory exostoses are more likely to develop in individuals performing ‘‘above water’’ activities, protecting ears from the refrigerating action of atmospheric temperature and wind chill may be a simple and efficient means of avoiding the development of auditory exostoses. Although the efficiency of the use of earplugs or hoods to avoid auditory exostosis development remains controversial (Graham, 1979; Fenton et al., 1996; Timofeev et al., 2004), ethnographic data confirm that when the meatus is protected from cold wind and low atmospheric temperature, intense contact with water does not trigger auditory exostoses. Coastal Eskimos, who are strongly dependent on marine resources and use boats extensively, rarely present auditory exostoses (Finnegan, 1972), probably due to the constant use of hoods. Exostoses develop as a result of the refrigeration action of the meatus. In fact, Van Gilse (1938) conducted an experiment in order to test the meatal reflex of hiperemia when the meatus was stimulated with cold (158C) or warm water (408C), and he found that the meatal erythema following the cold water irrigation of the meatus was definitively prolonged. The periosteum of the ear canal is easily traumatized by some irritative stimuli such as the thermic shock, resulting from exposure of the auditory canal to cold, stimulating osteogenic activity. Vasodilatation associated with cold exposure seems to cause increased tension on the periosteum, resulting in osteoblastic activity. Continuous exposure to cold can trigger a local reaction of the ear’s soft tissue, which leads to the stimulation of osteogenic cell activities and finally, to exostosis (Belgraver, 1938; Fowler and Osmun, 1942; Harrison, 1951, 1962; DiBartolomeo, 1979; Filipo et al., 1982; Fabiani et al., 1984). Accordingly, the refrigerating effect of the meatus to cold water can be enhanced by the chill effect caused by low atmospheric temperature and wind. Thus, the absence of auditory exostoses does not exclude aquatic activities. Auditory exostosis may fail to form despite aquatic activities, especially when water temperature is above 198C, atmospheric temperature is high, and the wind chill effect is low. As demonstrated by the southeastern Brazilian coastal sites studied here, this situation occurs more frequently in warm regions (but also among coastal Eskimos with protected meatii). Thus, auditory exostoses as an aquatic activity marker in tropical and subtropical regions should be used only cautiously. We hope this study will encourage future research that includes environmental factors beyond traditionally proposed water temperature, making important contributions to the growing body of bioarchaeological literature on skeletal markers of human activity patterns.

ACKNOWLEDGMENTS We thank the staff and curators of the following institutions for allowing us to examine skeletons in their care: Hilton Pereira da Silva, Sheila Mendonça de Souza, and Claudia Rodrigues-Carvalho of the Museu Nacional (UFRJ-RJ); Lı´lia Cheuiche Carvalho (in memoriam) of the Instituto de Arqueologia Brasileira (RJ); Murillo Marx and Dorath Uchoâ of the Museu de Arqueologia e Etnologia (USP-SP); Claúdia Parrellada of the Museu Paranaense (PR); Igor Chmyz of the Centro de Estudos e Pes-


AUDITORY EXOSTOSES AS AQUATIC ACTIVITY MARKER quisas Arqueolo´gicas (UFPR-PR); Ana Luiza Fayet Salla and Patrıćia Gaulier of the Museu de Arqueologia e Etnologia (UFPR-PR); Gelci Jose´ Coelho, Teresa Domitila Fossari, Cristina Castellano, and Hermes Jose´ Graipel Jr. of the Museu Universita´rio ‘‘Professor Oswaldo Rodrigues Cabral’’ (UFSC-SC); Dione da Rocha Bandeira, Adriana Maria Pereira dos Santos, and Maria Cristina Alves of the Museu Arqueolo´gico do Sambaqui de Joinville (SC); Humberto Luiz Sobierajski of the Museu do Homem do Sambaqui ‘‘Padre Joaõ Alfredo Rohr’’ (SC); and Pedro Ignaćio Schmitz and Luciane Zanenga Scherer of the Instituto Anchietano de Pesquisas (UNISINOS-RS). We are deeply appreciative of the assistance of Rafael Silva and Eliane Cristina Trucculo of the AOCEANO for data on ocean surface temperature. Suggestions and commentaries from two anonymous reviewers and Clark Spencer Larsen greatly improved the former version of this article, which are deeply appreciated.

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