AMERICAN JOURNAL OF HUMAN BIOLOGY 00:00–00 (2016)

Original Research Article Growth Patterns among Indigenous Qom Children of the Argentine

1 2 MARTA P. ALFONSO-DURRUTY, AND CLAUDIA R. VALEGGIA * 1Department of Anthropology, Sociology & Social-Work, Kansas State University, 008 Waters Hall, Manhattan, Kansas 2Department of Anthropology, Yale University, 10 Sachem St., New Haven, Connecticut

OBJECTIVES: This study describes and compares the growth strategies of rural (Western) and peri-urban (Eastern) Qom indigenous children from . METHODS: Height and weight were cross-sectionally assessed in Western (n 5 263) and Eastern Qom (n 5 512) individuals aged 0-18.9 years. Height-for-age (HAZ), weight-for-age (WAZ), and BMI-for-age (BMIZ) z-scores were cal- culated with an LMS software. Results were organized into four age categories: infancy, childhood, juvenility, and ado- lescence. Between-group comparisons of HAZ, WAZ, and BMIZ were carried out by age and sex categories and compared with Student’s t or Mann Whitney tests. Nutritional status was classified based on BMIZ following WHO rec- ommendations and was compared with x2 tests. RESULTS: In both groups, height and weight followed the typical human growth curve. Mean HAZ scores in both groups were within two standard deviations from the international reference, and increased from infancy to juvenility. WAZ and BMIZ scores were high during infancy and showed a general declining trend with age. Overall, Western Qom had higher HAZ scores. WAZ and BMIZ score comparisons showed only a handful of statistically significant differences, which, along with the analysis of BMI categories, indicated an association between peri-urban environments and a higher prevalence of overweight and obese individuals (P < 0.01). CONCLUSION: Among the Qom, low HAZ and high WAZ scores during the early years of development allow for the attainment of a relatively high adult stature. Their adaptive life-history strategy seems to be to divert energy toward body mass during early development, and catch-up with linear growth at a later stage of development. Am. J. Hum. Biol. 00:000–000, 2016. VC 2016 Wiley Periodicals, Inc.

Human growth variability results from the complex identified in a few indigenous lowland populations in interaction between constitutional (e.g., genetic) and South America. This pattern of linear growth deficits, but extrinsic factors (Bogin, 1999; Eveleth and Tanner, 1991; not necessarily body mass deficits, seems to be widespread Hallgrimsson, 2003; Metcalfe and Monaghan, 2001). Con- among indigenous children in Argentina (Mbya-Guarani- sequently, there is extensive variation in the timing, dura- Orden and Oyhenart, 2006; Zonta et al., 2010), Bolivia tion, and final outcome of growth across individuals and (Tsimane-Foster et al., 2005; Tanner et al., 2014), Brazil populations. Examples of this variability are differences (Campos et al., 2015; Ferreira et al., 2012; Karapoto et al., in age at menarche (Eveleth and Tanner, 1991; Ellis, 2009) and Ecuador (Shuar- Urlacher et al., 2016). This 2004; Gluckman and Hanson, 2006; Wood, 1994), average trade-off between body-mass and body-height has been adult height (Bogin, 1999), and child-juvenile growth explained by poverty, marginalization, market integra- velocity and timing (Walker et al., 2006). tion, and parasitism. Thus, when compared to interna- Plasticity in growth dynamics leads to a variety of phe- tional growth standards, many of these populations have notypes that biomedical and adaptationist approaches high prevalence of low height-for-age (HAZ) measures interpret as the result of short-term responses, which can (Benefice et al., 2007; Blackwell et al., 2009; Foster et al., be adaptive or maladaptive (e.g., small-but-healthy vs. 2005) and, increasingly, overweight and obesity (Duran small-but-unhealthy; Bogin et al., 2007; Seckler, 1982; et al., 2006; de Onis et al., 2012; Urlacher et al., 2016; Schell and Magnus, 2007). Similar to the adaptationist Zonta et al., 2010). This dual nutritional burden has been approach, life-history theory recognizes that humans have associated with later risk of metabolic disease and short evolved to withstand environmental hardship, such as adult stature (Barker et al., 2002; Bateson et al., 2004). In energy crises, by responding in ways that would maintain this study, a life-history approach is used to assess the some evolutionary fitness, even if responses are sub- impact that the interaction between the sociocultural and optimal (Hochberg, 2009). However, unlike the biomedical and adaptationist approaches, life-history theory examines variations in growth as a matter of resource allocation Additional Supporting Information may be found in the online version strategies in a time-integrated fashion. Thus, life-history of this article. theory expands our understanding of growth beyond the Contract grant sponsor: National Geographic Society; Contract grant adaptive/maladaptive dichotomy (Charnov, 1993; Schell number: 8395-08; Contract grant sponsor: LSB Leakey Foundation. and Magnus, 2007; Stearns, 1992) by analyzing changes in *Correspondence to: Marta P. Alfonso-durruty, Department of Anthro- pology, Sociology & Social-Work, Kansas State University, 008 Waters phenotypic trajectories in terms of trade-offs between Hall, Manhattan, Kansas. maintenance and production (Jones, 2005; Hochberg, 2009; E-mail: [email protected] Hochberg et al., 2011; Kuzawa, 2007; Metcalfe and Received 3 November 2015; Revision received 5 May 2016; Accepted 5 Monaghan, 2001; Worthman and Kuzara, 2005). June 2016 DOI: 10.1002/ajhb.22886 Possible trade-offs between linear growth (height) and Published online 00 Month 2016 in Wiley Online Library growth in body mass (weight and BMI) have been (wileyonlinelibrary.com).

VC 2016 Wiley Periodicals, Inc. 2 ALFONSO-DURRUTY AND VALEGGIA biological contexts have on growth trajectories and out- comes in two indigenous groups in northern Argentina: the Eastern and Western Qom1. The goal of this analysis is twofold: first, to provide a descriptive overview of child- ren’s growth and nutritional status in these indigenous groups that can be used for comparative purposes, and, second, to evaluate the possible associations between early life-history traits and the environmental variables that may lead to potential trade-offs that shape infant and child growth. Based on the existing literature, a Westernized lifestyle is associated with indexes of positive energy balance. Thus, we predict differences between rural and peri-urban populations, so that children who are closer to urban centers will be taller and more likely to be overweight or obese than those who live in rural environments and follow a more traditional lifestyle.

STUDY PARTICIPANTS AND METHODS Until the 1930s the Qom of the Gran Chaco were semi- nomadic hunter-gatherers, using horticulture on occasion. During the last century, disruptions to their traditional lifestyle forced their migration to urban centers. However, many semi-isolated communities still use the forest and rivers as a source of food and shelter. This situation results in a spectrum of lifestyles and subsistence patterns that range from the more traditionally living rural groups, to transitional, peri-urban villages, as well as market- economy urban “barrios” (Mendoza and Wright, 1989). In this study, data collection was conducted in two Qom populations (Eastern and Western). The Eastern Qom live in the peri-urban village of Namqom, located 11 km West of the city of Formosa (58˚W and 26˚S; Fig. 1). The village is located in a mosaic of savannah, marshes, and wood- lands. The mean annual precipitation in this region is approximately 1,400 mm (Fernandez-Duque, 2016). Fig. 1. Location of the Eastern Qom and Western Qom commun- Monthly mean rainfall varies significantly during the ities included in this study. year, with two rain peaks in April and November, with the lowest average rainfall occurring during the period of Cacique Sombrero Negro, a 35,000-ha rural community June through August. Monthly mean temperatures are located 550 Km West of the city of Formosa (61-62 W, lowest between May and August (16–188C) and highest and 23-24 S; Fig. 1). The villages are located in a dry between October and March (23–278C). Extreme low woodland environment. Official meteorological sources (below freezing) and high temperatures (above 408C) are (https://www.formosa.gob.ar/upca/precipitaciones) indi- frequent. cate a mean annual precipitation of approximately Namqom has a population of approximately 3,000 peo- 700 mm a month, but mean rainfall varies significantly ple, distributed in a 120 ha area. The first Qom families during the year (200–1400 mm). The rainy season extends established themselves in this settlement in the early between November and April, and the dry season from 1970’s, and the village has since then experienced a rapid June through August. Monthly mean temperatures are population growth both as a result of high fertility and lowest between May and August (16–188C), and highest immigration from rural areas (Sanchez-Ocasio and Valeg- between October and March (23–308C). Extreme low gia, 2005). Extended families tend to live close to one (278C) and high temperatures (above 428C) are frequent. other and participate in microeconomic exchanges (Kap- Sombrero Negro has a population of approximately salakis, 2011). There is incipient social stratification, 1,600 people. Ethnohistorical reports indicate that the mainly associated with participation in provincial politi- Western Qom have occupied this area at least for the last cal dynamics. However, all families live below the poverty couple of centuries (Mendoza, 2002). These villages still line and rely mainly on temporary jobs and government rely in part on hunting, gathering, and fishing for subsist- subsidies. The health center offers prenatal and child ence (Lanza and Valeggia, 2005; Sanchez-Ocasio and health care, and keeps good health records of the families Valeggia, 2005; Valeggia et al., 2005). Most families live in the village. off subsidies from the government and political parties. The Western Qom live in a cluster of 12 villages Socioeconomic stratification is almost non-existent, and collectively known as Comunidades Aborıgenes de their egalitarian concept of leadership persisted until the late 1980’s (Mendoza, 2002). However, association with 1Qom people were previously known as Toba, a pejorative name given by local political parties has introduced dissonance into their Guaranı people. We are choosing to use the current self-adopted name for traditional leadership patterns. Extended families live this Chacoan indigenous group. close to each other and individuals tend to marry

American Journal of Human Biology GROWTH STRATEGIES IN THE ARGENTINE GRAN CHACO 3 exogamously with members of other historical bands are common among children in the summer, while (Mendoza, 2002). respiratory infections, including bronchitis and pneumo- The two study groups share the same genetic and eth- nia, are more prevalent during the winter months (data nohistorical background, as well as most cultural values not published). in terms of social practices. Monogamy is the main mat- ing pattern, with serial monogamy being more common DATA COLLECTION AND ANALYSIS among Eastern than Western Qom. Qom women have had an independent and influential position in their soci- Anthropometric data was obtained from 775 children, ety as a consequence of their central role in the family ages 0-18 years, from Eastern (n 5 512) and Western Qom economy (Braunstein, 1983; Karsten, 1967). Qom moth- (n 5 263; Supporting Information Table S1). Data collec- ers breastfeed their children until the following preg- tion took place at the childrens’ house under parental sur- nancy is visibly obvious, or until the child weans him/ veillance. Age was reported by the child’s principal herself at about 2-3 years of age (Olmedo and Valeggia, caretaker, and confirmed through national identification 2014). The interbirth interval (IBI) is quite similar in and/or health center records. Height was measured with a both populations, with a median IBI of 29.2 months for portable stadiometer, and body weight was assessed with the Eastern Qom (Valeggia and Ellison, 2004), and 31.0 a TanitaVR TBF scale. The measurements were taken months for the Western Qom (Sanchez-Ocasio and Valeg- once, thus the technical error of measurement for gia, 2005). Both populations have access to Western med- anthropometry is not available in this study. Based on height and weight, BMI was calculated as weight (kg)/ icine via provincially run health centers in their 2 community, and the majority of births occur at public hos- height (m ). pitals, even in the more remote areas (Mirassou, 2013). HAZ, weight-for-age (WAZ), and BMI z-scores (BMIZ) Infant mortality rates for the provincial departmental were estimated for each participant with the LMS soft- divisions in which these populations are located are 22& ware program (Cole, 1990). Individual Z-scores calcula- and 16& for the Western and the Eastern Qom respec- tions were based on the chronological age of each tively (Mirassou, 2013). Infant mortality rates for the participant. HAZ and BMIZ were estimated based on the of Formosa are the highest in Argentina (Minis- international reference (WHO, 2006). WAZ scores were terio de Salud, 2014). calculated based on the Argentine reference (Lejarraga Diet has diverged substantially between these two Qom et al., 2009), given that the international reference limits groups. The diet of Western Qom families is much more WAZ calculations to children under the age of 10 years. varied, including foraged items such as fruits and vegeta- Additionally, individual BMIZ scores were categorized as bles from the bush, as well as fish, honey, and game (Are- healthy (within two 2SD for those aged 0–5 years of age, nas, 2003). In general, the Western Qom diet is rich in and between 22 and 1SD for individuals aged 6–18 proteins and vitamins. Hunted game include deer, arma- years), severely thin/severely wasted (< 23sd), thin/ dillo, wild pigs, and tapir (Alvarsson, 1988; Karsten, wasted (<22sd), overweight (>2SD–3SD for those aged 1932). Women gather an array of wild produce including 0–5 years of age, and between > 11sd-2SD for those aged honey, carob pods, cactus figs, wild squash, wild roots, and 6–18 years of age) or obese (>3SD for individuals aged 0– hearts of palm. These economic activities are comple- 5 years of age, and > 12SD for those aged between 6–18 mented by some horticulture of squash and beans (Men- years of age), following international recommendations doza and Wright, 1989). Since they do not have specially (de Onis and Lobstein, 2010; WHO, 2006). prepared weaning foods, infants transition from breast- After the Z-scores were individually calculated based on milk directly into the adult diet. Foraged items are sup- chronological age, participants were grouped into four age- plemented with store-bought items, particularly wheat based categories: infancy, childhood, juvenility, and adoles- flour to make dough, rice, pasta noodles, and polenta. The cence (Bogin, 1999; Hochberg, 2012). These life-history Eastern Qom diet only occasionally includes foraged items stages have been defined based on behavioral and biologi- (fish, armadillos), but it is overall quite monotonous and cal traits: (1) Infancy (birth to 2.9 years-of-age) is a period highly caloric. Typically, the Eastern Qom eat one meal a of rapid, but steeply decelerating growth rate, where fifty day which consists of some kind of stew made with pasta, percent of the metabolic rate is directed to brain growth rice, or polenta, supplemented with onions and potatoes. and function. Individuals are breastfed and, thus, are Meat and dairy products are consumed only during the highly dependent on their mothers; (2) Childhood (3.0 to first week of the month, when they receive their subsidies 6.9 years-of-age) starts after weaning and is characterized (Olmedo and Valeggia, 2014). Weaning foods include for- by a moderate, but steady, growth rate. Around the age of mula milk, which mothers receive at the local health cen- 6 years, the mid-childhood growth spurt takes place; (3) ter, white bread, fried dough, noodle/rice soups and, less Juvenility (7.0 to 10.9 years of age in girls, 7.0 to 12.9 years frequently, fruits like bananas or apples (Olmedo and of age in boys) is a slow-growth period marked by adre- Valeggia, 2014). narche and a cognitive shift. Juveniles are semi- In general, both populations can be classified as hav- independent individuals who can provide most of their own ing a moderate to high pathogenic environment. In the food and protect themselves from most danger; and (4) Western community, water needs to be fetched from Adolescence (11.0 to 19 years of age in girls, 13.0 to 21.0 nearby reservoirs or from a central pump and carried years of age in boys) is marked by gonadarche. As a result, to the individual households. The Eastern Qom have endocrine changes ensue, secondary sexual characteristics access to water provided by the nearby city to a central develop and growth velocity accelerates, leading to the ado- water tank, and about half of the households have a lescent growth spurt (Bogin, 1999; Hochberg, 2012). These pipe that receives this water. The rest of the families life-history stages are assumed to be universal, but there is need to fetch water from smaller tanks distributed ample evidence showing that there is substantial variation around the village. Gastrointestinal and skin infections in growth trajectories that should be incorporated into our

American Journal of Human Biology 4 ALFONSO-DURRUTY AND VALEGGIA models (for example, Walker et al., 2006). For our data, clustering around the Argentine mean in both groups. however, we considered that this classification was broadly Between infancy and juvenility, WAZ scores were highest applicable for the purposes of our analysis. among the Eastern Qom in comparison to the Western Statistical analyses were conducted in SPSS 21.0 (IBM Qom girls. However, in adolescence, Western Qom girls Corp., 2012). Descriptive statistics were used to charac- had the highest mean WAZ scores. For the most part, terize the height, weight, and BMI of Eastern and West- weight scores revealed an urban to rural trend (Fig. 2b; ern Qom by sex and age (in years). Means and standard Supporting Information Table S2). Among girls, mean deviations were calculated for all z-scores (HAZ, WAZ, WAZ score comparisons showed no statistically significant and BMIZ). Eastern and Western Qom boys and girls difference during infancy. During childhood, however, the were compared based on their mean HAZ, WAZ, and analysis revealed significant differences between the BMIZ scores by age category (infancy, childhood, juvenil- groups (Student’s t 5 2.132, df 5 99, P < 0.05) due to West- ity, and adolescence). When the variable examined ern Qom girls weighing less. Comparisons for the juvenile showed a normal distribution (based on Kolmogorov- and adolescent segments do not reveal statistically signifi- Smirnoff Lilliefors tests) in both Qom groups, between- cant differences between the groups, although the results group comparisons were conducted with parametric sta- show that between childhood and juvenility, WAZ scores tistics (Student’s t-test). For cases in which the variables among Western Qom girls rapidly climbed, a trend that deviated from normality, between-group comparisons continued during adolescence. In contrast, WAZ scores in were conducted with Mann-Whitney U tests. HAZ scores Eastern Qom girls showed only a moderate increase deviated from normality among East Qom girls in the between childhood and juvenility, although they did childhood category (P < 0.05). In boys, deviations from increase toward adolescence albeit at a lower rate (Fig. normality were identified in HAZ scores among Eastern 2b; Supporting Information Table S2). Qom infants (P < 0.01) and juveniles (P < 0.05), and West- Mean BMIZ scores among girls were within the normal ern Qom adolescents (P < 0.05). No deviations from nor- rage, except for the Eastern Qom infant girls who showed mality were identified for WAZ scores, and in the case of a mean BMIZ score that corresponded, marginally, to the BMIZ scores, deviations from normality are restricted to overweight category (x52.02; Supporting Information the juvenile Western Qom boys. The frequency of healthy, Table S2). Additionally, mean BMIZ scores for Eastern severely thin, thin, overweight, and obese BMIZ scores Qom girls in the childhood category and infant Western were calculated in each group and compared between Qom girls were normal but above 1SD, which indicates groups as a total (not separated by age categories), in these individuals are at risk for overweight and obesity order to have a general assessment of the nutritional sta- (de Onis and Lobstein, 2010). However, BMIZ scores tus of both groups. Between-group comparisons of BMIZ showed positive but descending values between birth and categories were carried out with chi-square (x2) tests. juvenility in both groups. While BMIZ scores showed a small decline between juvenility and adolescence in East- RESULTS ern Qom girls, Western Qom girls showed an upward Girls trend in their BMIZ scores between these two periods. In general, when all age periods are considered, Eastern Height and weight followed the typical human growth Qom girls’ BMIZ scores were the highest, except for the pattern in both groups (Supporting Information Table adolescent period when Western Qom scores were slightly S1). When grouped by age category (infancy, childhood, higher. Thus, BMIZ scores showed an urban-to-rural gra- juvenility, and adolescence), Eastern and Western Qom dient in which girls who lived closer to urban centers had girls presented mean HAZ scores that were within the higher BMIZ scores than those who lived further away normal range (> 22SD). However, the mean HAZ score (Fig. 2c; Supporting Information Table S2). Between- changed by age category, so that in both groups we group BMIZ score comparisons showed no statistically observe an increase in HAZ scores from infancy through significant difference during infancy. In both childhood juvenility. However, while HAZ scores for Eastern Qom and juvenility, BMIZ scores were significantly different girls plateau between juvenility and adolescence, Western between Eastern and Western Qom girls (Student’s Qom girls maintained an upward trend. (Fig. 2a; Support- t 5 3.77, df5 96, P < 0.01, and; Student’s t 5 2.765, df5 ing Information Table S2). Overall, mean HAZ scores 113, P < 0.01 respectively), with the former having higher were consistently higher among Western Qom girls in BMIZ scores. However, no statistically significant differ- comparison to Eastern Qom girls. Between-group compar- ence was observed between the BMIZ scores of Eastern isons, however, revealed no statistically significant differ- and Western Qom adolescent girls (P > 0.05), showing ence in HAZ scores between infancy and juvenility that the upward trend in BMIZ scores observed among (P > 0.05). During adolescence, a significant difference in Western Qom girls between juvenility and adolescence their HAZ scores (Student’s t5-3.449,df 5 111, P < 0.01) eliminated the differences in BMIZ present in the previ- was found, indicating that Western Qom girls had signifi- ous two periods. In summary, during childhood and juve- cantly higher HAZ scores than their Eastern Qom peers. nility, the more urbanized Eastern Qom girls had the Thus, we do not observe a clear urban-to-rural gradient in highest BMIZ scores. During adolescence, the groups the HAZ scores of girls. become more similar and no statistical difference between Among girls, mean WAZ scores were within the range of them was identified (Fig. 2c; Supporting Information what is considered healthy (between two standard devia- Table S2). tions). WAZ scores among girls were higher, and positive, Further classification of individuals by BMI category, during infancy, rapidly dropping by the time they reached revealed that in both groups over half of the girls had a childhood. Among the Western Qom, this drop resulted in healthy BMI (66.4% of Eastern Qom and 81.2% of West- negative WAZ scores during childhood and juvenility. ern Qom; Fig. 3). However, while 27.5% of Eastern Qom Between childhood and juvenility, WAZ scores increased girls were overweight, only 17.3% of their Western Qom

American Journal of Human Biology GROWTH STRATEGIES IN THE ARGENTINE GRAN CHACO 5

Fig. 2. Mean height-for-age (HAZ; (a), weight-for-age (WAZ; (b) and BMI (BMIZ; (c) Z-scores for girls and boys. (Infancy 5 0–2.9 years of age; Childhood 5 3.0 to 6.9 years of age; Juvenility 5 7.0 5 10.9 years of age in girls and 7.0–12.9 years in boys, and; Adolescence 5 11.0 0 19.0 years of age in girls, and 13.0–21.0 years of age in boys). 1 Statisitically significant differences between the groups are signaled with an asterisk (P < 0.05). peers fell within that category. Moreover, 6.5% of Eastern wasting or severe wasting were identified among the girls Qom girls were categorized as obese and only 1.5% of in these groups. Cross tabulation of these results indicate Western Qom girls belonged in that category. No cases of that there is a statistically significant relation between

American Journal of Human Biology 6 ALFONSO-DURRUTY AND VALEGGIA

Fig. 3. Percent distribution of Eastern and Western Qom girls and boys by BMI category.

BMI category and group (Chi-square x2 5 10.46, n 5 380, statistically significant during childhood, and was P < 0.01, Cramer’s V 5 0.166). Eastern Qom girls show a reversed during the adolescent period when Western Qom prevalence of overweight and obese scores that are 1.6 boys had slightly higher WAZ scores. and 4.3 times (respectively) higher than that of Western Mean BMIZ scores remained at or above the interna- Qom girls (Fig. 3). tional mean in both Eastern and Western Qom boys from infancy to adolescence. During infancy, the mean BMIZ in Boys both groups was above 1SD, which indicates that infant Mean HAZ scores for boys in both Qom groups fell within Eastern and Western Qom boys are generally at risk for the range of normality, (Fig. 2a, Supporting Information overweight and obesity (de Onis and Lobstein, 2010). In Table S2) but were consistently below the international both groups BMI scores showed a small decline between mean throughout their period of growth and development. infancy and childhood. This trend accelerated afterwards, In both Eastern and Western Qom boys, HAZ scores dis- so that by juvenility both Eastern and Western Qom boys played an upward trend from birth to juvenility. However, showed lower BMIZ scores than in previous age catego- between juvenility and adolescence, Eastern and Western ries. Among Eastern Qom boys, scores continued to Qom seemed to reach a plateau characterized by a slight decline, so that during adolescence the average score was decline in their HAZ scores. Overall, HAZ scores between zero. In contrast, Western Qom boys showed a small groups were similar (Fig.2a; Supporting Information Table increase in their average BMIZ scores between juvenility S2). In fact, between-group comparisons among boys and adolescence (Fig. 2c; Supporting Information Table showed no statistically significant differences in HAZ S2). BMIZ scores among Eastern Qom boys, the most scores for any age category (P > 0.05). urbanized, and thus Westernized, group were higher but Mean WAZ scores in boys also remained within the nor- tended to decline as they moved from infancy into adoles- mal range. The scores stayed relatively stable among cence. Thus, it is only during this last period that BMIZ Western Qom between infancy and adolescence. In East- scores were higher among Western than Eastern Qom ern Qom boys, the mean was also stable and slightly (Fig. 2c; Supporting Information Table S2). BMIZ score above the Argentine mean during infancy and childhood comparisons showed no significant differences among (Fig. 2b; Supporting Information Table S2). After that infants. During childhood, however, the analysis revealed period, the average scores rapidly decline to negative val- a statistically significant difference (Student’s t 5 3.196, ues during juvenility and adolescence. Comparisons of df5 97, P < 0.01). The difference in BMIZ scores between WAZ scores revealed no statistically significant differen- the groups remained significant during the juvenile ces between the infants of the two groups. The childhood period (Mann Whitney U 523.365, P < 0.01). In both category, however, did show significant differences (Stu- childhood and juvenility, the difference showed that East- dent’s t 5 2.13, df 5 112, P < 0.05), indicating that Eastern ern Qom boys had higher BMIZ scores than their Western Qom boys had WAZ scores that were significantly higher Qom peers. No statistically significant difference, how- than those of their Western Qom peers. In contrast, no ever, were identified among adolescents. statistically significant difference was identified during In boys, the trends for BMI categories were the same as juvenility or adolescence. Overall, from birth to juvenility, those observed in girls (Fig. 3). Most Eastern and Western boys showed an urban-to-rural gradient in their WAZ Qom boys had a healthy BMI (65.6% of Eastern and scores so that the more urban and Westernized Eastern 83.5% of Western boys), but 29.2% of Eastern boys and Qom had the higher scores. This trend, however, is only 13.4% of Western boys were overweight. The rates of

American Journal of Human Biology GROWTH STRATEGIES IN THE ARGENTINE GRAN CHACO 7 obesity in both groups were similar with a 3.8% of Eastern When overall infancy WAZ and HAZ scores are consid- boys and a 3.1% of Western boy falling within that cate- ered, indigenous children of the Argentine Chaco appear gory. Only 0.5% of Western boys showed wasting and. 09% to be shorter than the median, and relatively heavy. This presented severe wasting. No cases of wasting or severe phenotype has been found in other Latin American popu- wasting were observed among Eastern boys. Cross- lations (Castro et al., 2010; Duran et al., 2006; Guedes tabulation of these results show statistically significant et al., 2010), and can be interpreted as the result of early differences between the groups (chi-square x2 5 13.98, adaptation to conditions of scarcity (Hochberg, 2009; Han- df 5 4, P < 0.01, Cramer’s V 5 0.203). This difference son et al., 2011; Solomons et al., 2015). However, the reflects the fact that the prevalence of overweight boys hypothesis of an adaptive response to a “bad start” among the Eastern Qom is 2.2 times higher than in West- (Kuzawa, 2007; Metcalfe and Monaghan, 2001) does not ern boys (Fig. 3). BMI categories show a clear urban-to- fit this particular case; first, birth weight is relatively rural trend, where boys who lived closer to urban centers high in this population (3.5 kg for boys and 3.3 kg for girls; were more likely to be overweight. Valeggia et al., 2002) and thus there is no evidence of intrauterine growth retardation. Second, although Qom DISCUSSION infants’ weight-for-age is relatively high, and their height-for-age is comparatively low, finalized adult stat- Indigenous children of the Argentine Gran Chaco, ure is among the highest in Native South American unlike neighboring groups (Ferreira et al., 2012; Horta groups (Walker et al., 2006). This seems to indicate that et al., 2013; Solomons et al., 2015; Tanner et al., 2014) the Qom have a different growth strategy, perhaps adapt- have HAZ and WAZ scores that are mostly within the ive, that invests more energy in body mass than in linear range of international growth norms. Among girls, we growth early during development. Later, there is a shift to observed an overall higher investment in body mass than investment in linear growth. in linear growth during infancy. This early investment in While both boy and girls from Eastern and Western mass is followed by an acceleration, or catch-up, of their Qom communities show adolescent HAZ scores that are linear growth during childhood and juvenility. Thus, as close to the international median, they remain consis- Qom girls approached juvenility, mean HAZ scores tently below it. This may indicate the presence of a approached the international median. During juvenility, blunted or attenuated adolescent growth spurt. The ado- WAZ scores were also near the international mean, so lescent growth spurt is considered one of the hallmark that in this period, Qom girls presented a pattern of derived traits of our species (Nelson and Thompson, weight and height scores that paralleled each other. How- 1999). This trait is, however, plastic and subject to the ever, the investment during juvenility seems to be higher influences of environmental factors that lead to variations in linear growth than in mass. By the time of adolescence, in velocity and timing (Gluckman and Hanson, 2006; while Western Qom girl HAZ scores continued to climb, Rogol et al., 2002). It is possible that Qom individuals con- Eastern Qom girls’ scores did not. Interestingly, although tinue to grow into their twenties, as has been observed BMIZ scores were higher among the more westernized among other non-westernized groups (Little et al., 1999). Eastern Qom, which is associated with an increased risk Further longitudinal studies are needed to assess vari- in overweight and obesity, we did not find the same trends ability in growth spurt among the indigenous Qom of the in height. The results suggest that further examination of Argentine Gran Chaco. It is possible, however, that social the sociocultural, historical, and political ecologies is discrimination and the environment experienced by previ- required. In a comparative pilot study of Eastern and ous generations continue to exert their influences in the Western Qom female reproductive patterns (Sanchez-Oca- growth patterns of these Indigenous groups (Moffat and sio and Valeggia, 2005 and unpublished data), for exam- Galloway, 2007). ple, we found earlier ages at first pregnancy and higher HAZ, WAZ, and BMIZ score comparisons showed only a adolescent fertility rates among Eastern Qom girls handful of statistically significant differences. In particu- (15.5 6 1.1 years old and m(x) 5 0.19) than among the lar, WAZ and BMIZ comparisons showed that ecological Western ones (17.8 6 2.4 years old and m(x)5 0.11). If con- differences between peri-urban and rural groups resulted firmed in a study that includes a larger sample size (in in a gradient where the former showed some of the telltale prep.), this difference in reproductive strategies may signs of the transition to a Westernized life style. Changes account for the lower adolescent HAZ scores, as a result of in diet associated with urbanization have been reported in a deviation of resources away from linear growth and into other studies, where geographic location plays an impor- reproduction (Scholl et al., 1994). tant role (Lazarou and Kalavana, 2009). Among non- Boys’ mean HAZ scores climbed from infancy to juvenil- Native Argentine, increased levels of urbanization likely ity, but remained below the international median. accompanied by dietary changes and low activity levels Between the juvenile and the adolescence periods, their lead to significantly higher frequencies of obese and over- scores declined, so that among adolescents we observed weight individuals (Dahinten et al., 2011; Hirschler et al., HAZ scores that were below the international median, but 2008; Kovalskys et al., 2011; Ramirez-Zea et al., 2014). were overall higher than those observed during infancy. Unlike non-Native Argentines, the Qom show a positive No statistically significant difference was identified association between socioeconomic status and BMI (Valeg- between the two groups. However, Western Qom boys gia et al., 2010), which has been observed in other Argen- were, for the most part, consistently taller than their tinean indigenous groups (Orden and Oyhenart, 2006; Eastern Qom counterparts, except during infancy. Given Romaguera et al., 2008) for whom heavy individuals are that boys may continue to grow in height, the absence of a regarded as “healthy” (Valeggia et al., 2010). Moreover, a statistically significant difference in the HAZ scores of previous study has shown that Westernized Qom adults adolescent boys may, in fact, reflect the exclusion of older show a prevalence of obesity that is above 45% (Lagranja boys (ages 18–21 years) in this study. et al., 2015). It is important to note, however, that Qom

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WAZ scores are very close to the Argentine median (Lejar- children living in socioeconomic situations favorable to raga et al., 2009), which, when contrasted with the high growth in selected populations in the US, Brazil, Oman, BMIZ scores of these children, indicate that the Argentine Norway, Ghana, and India. The Argentine growth curves reference for weight is skewed toward the right, further are based on a sample of Argentine children, most of which highlighting the importance of applying international were not breastfed, and incorporate the WHO growth standards (de Onis and Lobstein, 2010). standards for the infancy age category (Lejarraga et al., As predicted by the research hypothesis, westernized 2009). The WHO standards provide a more general picture Eastern Qom show, for the most part, higher WAZ and in which population-specific differences in growth trajecto- BMIZ scores. Surprisingly, however, HAZ scores were ries are smoothed out. The value of using these curves is higher among Western Qom. Further studies that comparability with other studies and having a sense of include reproductive strategies, e.g., age at first preg- where the study population falls in the landscape of human nancy, and the inclusion of boys up to 21 years of age, growth in privileged populations. The justification for using are needed. In particular, an early age at first birth may more locally derived growth curves is that they are be indicative of a trade-off between growth and repro- intended to control for ethnicity variables. The construction duction, which may be part of a reproductive strategy of these growth standards follows a Western biomedical among the Qom. In addition, detailed nutritional studies model of “normality” and the main objective is to provide that assess dietary differences, especially regarding ways of assessing whether the growth of individual chil- micronutrient content, are necessary to explain why dren follow the statistically normal trajectory. Thus, it is Western and not Eastern Qom children are taller by the based on a dichotomous normal-pathological model which time of adolescence. Based on known economic strat- is in clear contrast with a life-history approach and its asso- egies, we propose that the incorporation of hunting, ciated concept of trade-offs during development, for which gathering, and fishing, along with store-bought items, variation in growth is not taken as “noise” but a source of among Western Qom provides higher levels of food secu- scientific inquiry. The use of the term “stunting,” which we rity and a better dietary quality, that are not available have avoided here, is a clear reflection of this contrast. For for the more urban Eastern Qom. the Western public health world, a child that is 2 SD below Although this work makes an important contribution to the median in height-for-age is considered to be abnormal our understanding of variation in human growth strat- (i.e., away from the norm) and not growing to her/his poten- egies, it is necessary to note its limitations. First, the cross- tial. A life-history approach considers the costs and benefits sectional nature of this study introduces possible biases in of different phenotypes and the traits that compose them, our results. For example, cohort effects may have influ- and incorporates the concept of trade-offs that are negoti- enced the z-scores of particular age stages (e.g., adoles- ated at different stages of development. In the case of the cence) so that children born around the same time native Qom of South America, the deviation from “normal” experienced a more (or less) favorable environment, which patterns may inform us about evolutionary strategies that might shape their growth trajectory differently. Moreover, are not necessarily pathological. Among the Qom, we do not the relevance of BMI scores must be cautiously assessed. It observe the co-occurrence of short height and obesity/over- has become increasingly clear that BMI is not an accurate weight found in other South American groups. However, indicator of nutritional status or body composition, and it the negative HAZ scores in infancy are surprising given is, at best, only a proxy for adiposity (Benefice et al., 2007; their positive WAZ scores. Considering their relatively Garn et al., 1986; Hall and Cole, 2006; Maynard et al., heavy birth-weight, the Qom seem to have resolved the 2001; Wilson et al., 2011). Furthermore, given that some of energy allocation trade-off during infancy by diverting the variation in body fat and BMI is influenced by the more energetic resources to body mass (particularly, it child’s age and degree of maturation (Ellis et al., 1999; seems, adipose tissue) than linear growth. However, this Freedman and Sherry, 2009; Hall and Cole, 2006; Maynard strategy changes later during development. Given that et al., 2001), future studies among the Qom must include their HAZ scores increase through their development up variables that account for these developmental parame- until juvenility, this early investment in mass may help ters. In this study, BMI tends to be higher among the East- Qom children by improving their ability to attain a final ern Qom, who are overall shorter than the Western Qom. adult stature. Results obtained in this study are in agree- Thus, the difference in the percentages of overweight and ment with the principle that growth is a robust, but plastic, obese individuals between these two groups is likely the process that evolved to provide individuals with the best result of higher levels of adiposity among the Eastern chances of attainting adulthood under diverse and fluctuat- Qom. However, given the limitations of BMI, future studies ing conditions. must include other measures of nutritional status, such as skinfolds and waist circumference, in order to understand ACKNOWLEDGMENTS the causes behind the shorter stature and higher weight of the Eastern Qom. In addition, our relatively small sample The authors thank the Qom Communities at Namqom size did not allow for a more detailed description of growth and Sombrero Negro for their participation in the study. patterns by age. Although the issue of small sample sizes They are grateful to Norberto Lanza (in memoriam), is endemic to those of us working with small-scale popula- Claudia R. Fernandez, Roxana Bogarın, Marisa Galeano, tions, future studies of growth strategies should aim at Nahomi Gutierrez, and Roxana Campuzano for their incorporating longitudinal designs. work in the field. They are also indebted to Dr. Marita In this context, it is worth commenting on the use and Baia, Director of the Centro de Salud Namqom, for her value of comparing growth trajectories against interna- support. Special thanks to Babette Zemel, for her feed- tional (e.g., WHO) and national (e.g., Argentine) standards. back on the analysis of growth curves and to four anony- The most updated WHO standard growth curves have been mous reviewers for their insightful comments on an constructed based on a cross-population sample of breastfed earlier version of this work.

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