Mapping Carbon and Nitrogen Isotopic Composition of Fingernails To

Received: 22 November 2019 Revised: 8 April 2020 Accepted: 27 April 2020 DOI: 10.1002/ajpa.24078

RESEARCH ARTICLE

Mapping carbon and nitrogen isotopic composition of fingernails to demonstrate a rural–urban nutrition transition in the Center-West, Northeast, and Amazon regions of Brazil

1Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília, Abstract Brasília, Brazil Objective: The main objective of this study is to investigate diet patterns among rural 2 Universidade Federal Rural da Amazônia and urban populations of the Center-West, Northeast, and Amazon regions of Brazil (UFRA), Belém, Brazil 3Departamento de Geografia, Universidade through the carbon and nitrogen isotopic composition of fingernails, recognizing that Federal do Amazonas, Manaus, Brazil the extent of market integration is a key driver of food consumption. 4 ~ ESALQ, Universidade de Sao Paulo, Materials and methods: In the Center-West, Northeast, and Amazon regions of Piracicaba, Brazil Brazil, fingernails were sampled in clusters encompassing a major city, town, and 5Departamento de Gest~ao Ambiental, Universidade do Estado do Rio Grande do rural village. A total of 2,133 fingernails were analyzed. Fingernails were clipped Norte, Mossoró, Brazil by donors using fingernail clippers. In the laboratory, samples were cleaned then 6Faculdade UnB Planaltina, Universidade de Brasília, Brasília, Brazil weighed in small tin capsules before being isotopically analyzed for carbon and 7Laboratório de Arqueologia, Antropologia nitrogen. Ambiental e Evolutiva (LAAAE), Instituto de Results: The overall mean δ13C and δ15N were −19.7 ± 2.8‰ and 10.6 ± 1.1‰, Biociências, Universidade de S~ao Paulo, Sao~ Paulo, Brazil respectively. In the more remote villages, where access to food markets is more 8Laboratório de Ecologia Isotópica, CENA, challenging, lower δ13C prevails, suggesting that Brazilian staple foods (rice, beans, Universidade de Sao~ Paulo, Piracicaba, Brazil and farinha) still dominate. In areas with easier access to food markets, δ13C 9Departamento de Estatística e Informática, Universidade Federal Rural de Pernambuco, values were higher, suggesting a change to a diet based on C4 plants, typical of a Recife, Brazil Brazilian supermarket diet. The variability among inhabitants in the same location 13 15 Correspondence expressed by a significant inverse correlation between δ C and δ N fingernail Gabriela B. Nardoto, Departamento de values suggested that “market integration” does not affect everyone equally in Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília, Brasília, DF, each community. 70910-900, Brazil. Discussion and Conclusion: The nutrition transition has not yet reached some Email: [email protected] remote villages in these regions of Brazil or that the nutrition transition has not yet Funding information reached all residents of these remote villages. On the other hand, in several villages Conselho Nacional de Desenvolvimento Científico e Tecnológico, Grant/Award there is a considerable adherence to the supermarket diet or that some residents of Numbers: 201929/2012-0, 407559/2012-4, these villages are already favoring processed food. 475311/2010-8; Fundaçao~ de Amparo à Pesquisa do Estado de S~ao Paulo, Grant/Award Number: 2011/50345-9

KEYWORDS carbon and nitrogen stable isotopes, dietary patterns, market-oriented urban centers, modern human, remote villages

1 | INTRODUCTION gold-mining activities in the State of Minas Gerais (Baiocchi, 1999). Residents of these villages are known as Kalungas, and only in the The nutrient transition as defined by Popkin (2002) began developing 1980s did these villages become, to some extent, integrated into a in Latin America in the 1970s. Since then, there has been increasing market economy (de Jesus Silva, de Paula Eduardo Garavello, Nardoto, consumption of animal proteins, and sugary foods, coupled with a Mazzi, & Martinelli, 2019; Fernandes, 2014). decline in cereal (wheat, rice, and corn) consumption (Monteiro, Levy, In contrast with these two more remote regions of the country, Claro, de Castro, & Cannon, 2011). These changes were followed by a the Northeast region of Brazil was one of the first regions to be inte- sharp increase in the consumption of highly processed food (Monteiro grated in the colonial mercantilism system implemented by Portugal. et al., 2011), defining the so-called “supermarket era” of food Vast tracts of the Atlantic Forest were converted into sugarcane consumption. fields, and the more arid inland regions were used for cattle ranching In the Brazilian Amazon, this phenomenon probably started in the (Schulz, Koch, Cierjacks, & Kleinschmit, 2017). However, in this region 1980s due to the opening of roads linking this remote region to con- there are still fishing villages where perhaps, the nutrient transition solidated markets of the more industrialized south–southeast regions has not yet consolidated (Nobre, 2005). Such is the case of several (Ahmed et al., 2013). One of the consequences of such “integration” fishing villages of the Sustainable Development Reserve of Ponta do was the increase in deforestation rates mainly due to the conversion Tubar~ao, located on the coast of the State of Rio Grande do Norte. of natural forests into cattle ranches (Hecht, 2015). Parallel to defor- The classical method to investigate food consumption of modern estation there was also a sharp increase in population growth, from populations is the 24 hr-diet recall, which is a good proxy of food con- 7 to 25 million people between 1970 and 2010 (IPEA, 2019). Both sumption compared with the more accurate but labor-intensive Amerindian and non-Amerindian rural riverine dwellers replaced tradi- method of weighing all food consumed over several days in different tional subsistence agriculture with an agriculture model based on cash households. Although very useful, these methods reflect the short- income, allowing for purchasing and consumption of processed food term food consumption trends and depend on information provided products (Blackwell, Pryor, Pozo, Tiwia, & Sugiyama, 2009; Coimbra by the target population (Archer, Pavela, & Lavie, 2015). Jr, 1984; de Jesus Silva, de Paula Eduardo Garavello, Nardoto, Mazzi, & In the early 1980s, DeNiro and Epstein (1978, 1981), established Martinelli, 2017; Giugliano, Giugliano, & Shrimpton, 1981; Godoy the basis for the use of carbon and nitrogen stable isotopic ratios to et al., 2005; Lourenço, Santos, Orellana, & Coimbra CE a., 2008; investigate food consumption by showing small differences between the Murrieta, 1998; Nardoto et al., 2011; Piperata, 2007; Santos & Coim- isotopic ratio of diet and consumer (Ambrose & DeNiro, 1986). In mod- bra Jr, 1991; Urlacher et al., 2016). ern humans, Webb et al. (1980) was the first to use stable isotopes to The Center-West region of Brazil, the Cerrado, a Neotropical address patterns of food consumption. This pioneer work was followed savanna that originally covered almost 2 million km2, had a similar fate by a series of studies using several human tissues such as, hair, finger- probably due its location between the Amazon region and more consol- nails, enamel, and bones (Bol & Pflieger, 2002; Correia, Foley, O'Connell, idated markets of the South–Southeast regions of the country. In the Ramirez-Rozzi, & Lahr, 2019; Katzenberg, 1989; Minagawa, 1992; 1940s and 1950s, this region was integrated with the majority of the Nakamura, Schoeller, Winkler, & Schmidt, 1982; O'Connell & population living on the coastline of Brazil by the “Roncador-Xingu Hedges, 1999; O'Connell, Hedges, Healey, & Simpson, 2001; Schoeller, Expedition,” which crossed the central region in a south–north direction Minagawa, Slater, & Kaplan, 1986; Valenzuela, Chesson, Bowen, Cer- with the main objectives of establishing telegraph posts and opening ling, & Ehleringer, 2012; Yoshinaga et al., 1996). airstrips (Villas Bôas & Villas Bôas, 2012). Such integration was consoli- In Brazil, Nardoto et al. (2006) were the first to use stable isotopic dated later by the construction of Brasília in the 1960s, the new capital natural abundance in fingernails to investigate modern human diets. of the country, and by the so-called “opening” of the Cerrado to agricul- This study, followed by Nardoto et al. (2011), led to detecting inter- ture and livestock. Consequently, almost half of the original vegetation esting food habits between different regions of the country. For of the Cerrado has been replaced by soybean, corn, sugarcane, and cat- example, patterns of food consumption were surprisingly homoge- tle (Pereira, Ferreira, Pinto, & Baumgarten, 2018). nous among large urban areas and rich in plants that followed the C4 In the 1970s, the population of the Center-West region was only photosynthetic metabolism (sugar cane, maize, and pastures). One the 4.5 million people, increasing to 14 million people 40 years later other hand, in the rural areas, there was an unequivocal higher con-

(www.ipeadata.gov.br), but it still has the smallest population density sumption of plants that followed the C3 plants' photosynthetic metab- among the five main regions of the country. In some of its rural areas, olism than in urban areas, especially for Brazilian staple foods, such as like the Biosphere Reserve of Chapada dos Veadeiros, remote villages rice, beans, and cassava. In such areas it seems that the nutrient tran- were established composed of slave-descendants who worked in sition has been delayed by a more complex and slower market TABLE 1 Municipalities and respective neighborhoods with populations, percent of population living in rural areas, gross domestic product per capita (GDP), human development index (HDI), NARDOTO Brazilian macro geographic region, number of fingernail samples (N), and percentage of women sampled in each place

GDP per TAL ET Municipality Neighborhood Group Pop. Rural (%) capita (R$) HDI Micro region Macro region N Female (%) . Alto Paraíso (16) Downtown Village 7,328 24 21,484 0.713 Chapada CW 54 80 Moinho Village – Chapada CW 07 43 Fraternidade Village – Chapada CW 40 55 Alvar~aes (5) Downtown Town 15,860 44 9,406 0.527 Medium-Solimões N 57 74 Porto Nazaré Village Medium-Solimões N 19 58 Benjamin Constant (1) Downtown City 42,020 40 6,602 0.574 Upper Solimões N 85 76 Brasília (17) Downtown Capital 2,974,703 79,100 0.824 Brasília CW 38 50 Cavalcante (14) Downtown Village 9,623 49 25,303 0.584 Chapada CW 38 76 Kalungas Village – Chapada CW 81 58 Colinas do Sul (13) Downtown Village 3,404 28 11,540 0.658 Chapada CW 40 58 Guamaré (20) Downtown Town 15,349 125,315 0.629 Reserva Tubar~ao NE 30 60 Itacoatiara (11) Downtown City 99,995 33 20,860 0.644 Upper Amazon N 04 80 Macau (21) Downtown City 31,584 17,222 0.665 Reserva Tubar~ao NE 33 76 Sert~aozinho Village Reserva Tubar~ao NE 38 71 Barreiras Village Reserva Tubar~ao NE 49 NA Mangue Seco Village Reserva Tubar~ao NE 31 NA Manacapuru (7) City 96,236 29 13,027 0.614 Lower Solimões N –– Costa do Caldeir~ao Village Lower Solimões N 135 92 Manaus (9) Downtown Capital 2,145,455 1 33,554 0.737 Lower Solimões N 62 50 Maraa~ (3) 18,186 50 7,805 0.498 Medium-Solimões N – Boa Esperança Village Medium-Solimões N 83 46 Jarauá Village Medium-Solimões N 58 53 Nova Jerusalém Village Medium-Solimões N 69 59 Santa Maria Village Medium-Solimões N 35 69 Sao~ Francisco Village Medium-Solimões N 33 51 Mossoró (18) Downtown City 237,241 9 19,714 0.720 Mossoró NE 101 75 Rancho da Caça Village Mossoró NE 38 68 Riachinho Village Mossoró NE 40 69 Natal (22) Downtown Capital 803,739 0 24,890 0.763 Natal NE 111 79 Nova Olinda do Norte (10) 35,870 56 5,861 0.558 Lower Solimões N –– Novo Airao~ (8) Downtown Town 18,974 36 6,650 0.570 Lower Solimões N 23 51 Santarém (12) Downtown City 297,580 23 15,531 0.691 Lower Amazon N 42 49 3 (Continues) 4 NARDOTO ET AL.

integration (Bartoli, 2018; Lima, Brondízio, Nardoto, & Nascimento, 2019; Moraes & Schor, 2010; Schor, Azenha, & Bartoli, 2018; Schor, Marinho, Costa, & Oliveira, 2014).

Female (%) In this context, the main objective of this study is to investigate diet patterns among rural and urban populations of the Center-West, Northeast, and Amazon region of Brazil through the carbon and nitro- N gen isotopic composition of fingernails, recognizing that the extent of market integration is a key driver of food consumption. Our main

hypothesis is that in areas of high market integration, a diet rich in C4

plants will prevail, since processed food in Brazil is rich in C4 carbon (Abdalla Filho et al., 2019; Coletta et al., 2012; Galera et al., 2019; Mardegan et al., 2013; Martinelli et al., 2011; Morais, Pellegrinetti, Sturion, Sattolo, & Martinelli, 2019). In order to achieve this objective, we rely on previously publi- shed data (de Jesus Silva et al., 2017; de Jesus Silva et al., 2019; Lima et al., 2019; Nardoto et al., 2006, 2011; Reinaldo, da Silva, Nardoto, & Garavello, 2015; Rodrigues et al., 2016), as well as new data on carbon and nitrogen isotopic ratios encompassing a total of approximately 2,000 fingernail samples collected in the abovementioned regions of Brazil. As differences in food habits between genders were previously found in the Amazon region (Piperata, Schmeer, Hadley, & Ritchie-Ewing, 2013), we also tested if such differences could be detected by stable isotopes as a second- ary objective. GDP per capita (R$) HDI Micro region Macro region 2 | MATERIAL AND METHODS

2.1 | Study area and sampling

In the Amazon region, samples were collected from residents living along the Solimões-Amazon River (Table 1). In the Center-West region, samples were collected among residents living in several counties located in the political micro-region of the State of Góias called Chapada dos Veadeiros. In the Northeast region, fingernail samples came from two major counties of the State of the Rio Grande do Norte, and fishing villages of the Reserve for Sustainable Develop- ment of Ponta do Tubar~ao (Figure 1). In each of these major regions, fingernails were sampled in clusters encompassing a major city, town, and a rural village as described in the Supplemental Material (Appen- ~ a Village Medium-Solimões N 149 100 dix S1). For most of the previous works and the new isotopic data included ao Village Medium-Solimões N 06 60 ~ in this survey, an authorization by the official Brazilian human ethical N.S.P.Socorro VillageReserva Aman Medium-Solimões N 22 73 CapaceteNova S. FranciscoTerezina III Village VillageMiss Villagecommittee was previously Upper Solimões Upper Solimões submitted, N Upper Solimões N approved N and 18 received 10 50 31 60 the regis- 55 tration number of COET 053, Piracicaba, S~ao Paulo, Brazil. Part of the Amazonian data was approved by the human ethical committee of the Universidade Federal do Amazonas—UFAM number 1.582.636. s (15) Village 3,016 29 8,934 0.661 Chapada CW 27 74 á (Continued) 2.2 | Isotopic analysis

The number between brackets after the name of the municipality is the key for the geographic localization of each municipality in Figure 1. Details of the sampling can be found in detail in our previous studies Teresina de Goi Uarini (4) Downtown Town 13,276 43 13,244 0.527 Medium-Solimões N 22 72 Tabatinga (2)Tefé (6) Downtown City Downtown 62,346 30 City 62,622 6,651 18 0.616 Upper Solimões 10,450 N 0.639 Medium-Solimões N 37 70 132 65 Municipality Neighborhood Group Pop. Rural (%) Note: TABLE 1 (de Jesus Silva et al., 2019; Nardoto et al., 2006, 2011; Reinaldo NARDOTO ET AL. 5

ratio of carbon (13C:12C) and nitrogen (15N:14N) in these samples was determined through a Delta Plus mass spectrometer for isotopic ratios (Finnigan MAT), in the Laboratory of Isotope Ecology, CENA (University of S~ao Paulo), Brazil. The results were reported as the deviation (δ) in parts per thousand (‰) relative to standard interna-

tional references; δX=(Rsample/Rstd − 1) × 1,000; where, X is carbon or nitrogen and R is the heavy to light isotope ratio for carbon or

nitrogen of the sample (Rsample) and of the standard (Rstd; VPDB- Vienna Pee Dee Belemnite for carbon and atmospheric air for nitrogen). Internal, certified laboratory standards are routinely interspersed with target samples during analysis runs. Long-term standard deviations of internal standards used at the Ecology Isotope Laboratory (CENA/University of Sao~ Paulo) are of 0.2‰ for carbon and 0.3‰ for nitrogen. The isotope raw data is available at http://dx.doi.org/10.17632/ g7rhtwnn8m.1

2.3 | Statistical analysis

We first tested differences between δ13C and δ15N of fingernails among residents grouped by regions of the country regardless of the FIGURE 1 Map of Brazil with state borders, showing counties size of the urban agglomerate (city, town, or village) using a general- and regions where fingernails were sampled. (a) Amazon region, ized linear model (GLM). Second, we tested for differences among iso- points 1–12; (b) Center-West region, points 13–17, and (c) Northeast region, points 18–22. Names of each county and respective numbers topic fingernail data comparing cities, towns, and villages nested in can be found in Table 1 the same region. GLMs were followed by the pos-hoc Tukey HSD to test for specific differences between regions and sites clustered in a et al., 2015; Rodrigues et al., 2016). Fingernails were clipped by specific region. donors using fingernail clippers. Finally, we tested for differences between gender grouping data This survey included only adults, spanning from 18 to 65 years of by urban agglomerate nested in the same region. First, we tested the age, where most of them aged between 20 and 45 years old. On aver- distribution of the isotopic data using the R package “fitdistrplus.” As age every volunteer donated between three and five clipping samples data was normally distributed, a GLM was applied, using the R pack- of their fingernails. We then storage all the pieces into the same small age “lme4” (Bates, Mächler, Bolker, & Walker, 2014). The raw dataset hermetic plastic bag to compose the clipped samples for the individ- will become available to download through the link that will be gener- ual. In the end, our survey accounted for 2,133 volunteers that ated by a Mendeley account. donated clipping samples from their hands. A nail is composed of keratin protein that is also found in skin and hair. Approximately 2/3 of the carbon and nitrogen atoms in keratin 3 | RESULTS are derived from nonessential amino acids, a mixing or scrambling of the dietary component isotopic signals is possible (see Nardoto The overall mean δ13C and mean δ15Nof−19.7 ± 2.8‰ and et al., 2006 for details). In our following studies (Nardoto et al., 2011; 10.6 ± 1.1‰, respectively. On average, fingernails of the Amazon Reinaldo et al., 2015; Rodrigues et al., 2016; de Jesus Silva region had the lowest mean δ13C value (−21.0 ± 2.3‰), contrasting et al., 2019, Lima et al., 2019) we were able to shed light on protein with the Northeast region, which had the highest mean value route issue using isotope data combined with individual questionnaire (−16.8 ± 0.5‰; Figure 2). The mean δ13C value of fingernails from the data (as well as regional comparisons). Despite all the complications Center-West region of Brazil was intermediate between the two related, we have been able to interpret our fingernail data in a semi- other regions (−17.5 ± 1.6‰), but significantly different from the quantitative manner based on the consensus of several previous stud- other two regions (Table 2). ies that the δ13C and δ15N values from fingernails are directly relative The δ15N of fingernails were also distinct among regions to the diet. (Table 2). In the Amazon region, the mean δ15N was 10.9 ± 1.1‰, In the laboratory, fingernail samples were cleaned with a solution decreasing to 10.4 ± 0.5‰ in the Northeast region, and finally to of distilled water, methanol and chloroform, and then the fingernail 9.8 ± 1.3‰ in the Center-West region (Figure 2). samples were weighed (1–2 mg) in small tin capsules before being Besides differences among regions, differences between large subjected to isotopic analyses for carbon and nitrogen. The isotopic consolidated urban centers and small towns and villages clustered in 6 NARDOTO ET AL. each region were also present, this was true mainly in the Amazon TABLE 3 Tukey HSD statistics for comparisons of δ13C and δ15N and Center-West region (Table 3). In the Amazon region, δ13C values between sites inside each region of fingernails progressively decreased from Manaus, the capital of the AMAZON state of Amazonas, to cities, then to towns and finally to villages Estimate SE z Pr(>|z|) (Figure 3). On the other hand, the δ15N values were similar in δ13C City–capital −2.17 0.25 −8.80 <0.01 Town–capital −3.30 0.28 −11.64 <0.01 Village–capital −4.98 0.23 −21.49 <0.01 Town–city −1.13 0.20 −5.54 <0.01 Village–city −2.81 0.12 −23.00 <0.01 Village–town −1.69 0.18 −9.12 <0.01 δ15N City–capital −0.70 0.11 −6.18 <0.01 Town–capital −0.48 0.13 −3.67 0.01 Village–capital 0.26 0.11 2.46 0.06 Town–city 0.22 0.09 2.39 0.07 Village–city 0.96 0.06 17.15 <0.01 Village–town 0.74 0.08 8.70 <0.01

CENTER-WEST

Estimate SE z Pr(>|z|) δ13C Chapada–capital −1.28 0.26 −5.00 <0.01 Kalungas–capital −2.43 0.27 −9.13 <0.01 Village–capital −0.48 0.30 −1.64 0.47 Town–capital −0.69 0.29 −2.42 0.11 Kalungas–Chapada −1.15 0.20 −5.74 <0.01 Village–Chapada 0.79 0.24 3.35 0.01 Town–Chapada 0.59 0.23 2.59 0.07 Village–kalungas 1.94 0.25 7.83 <0.01 Town–kalungas 1.73 0.24 7.30 <0.01 FIGURE 2 δ13 δ15 Box-plot of C (upper panel) and N (lower panel) Town–village −0.21 0.27 −0.77 0.94 of fingernails in the three sampling regions: Center-West, Northeast, δ15N and Amazon. Black dots represent the isotopic ratio of fingernails; horizontal bars inside the box represent median isotopic ratios, the Chapada–capital 1.18 0.21 5.58 <0.01 lower and upper lines of the box represent the first and the third Kalungas–capital 0.20 0.22 0.91 0.89 quartiles, the bar represents 1.5 times the interquartile range Village–capital −0.66 0.24 −2.73 0.05 Town–capital −0.39 0.24 −1.67 0.45 Kalungas–Chapada −0.98 0.16 −5.94 <0.01 TABLE 2 Tukey HSD statistics for comparisons of δ13C and δ15N – − − among the Center-West (CW), Northeast (NE), and Amazon regions Village Chapada 1.84 0.20 9.42 <0.01 Town–Chapada −1.57 0.19 −8.41 <0.01 δ13C Estimate SE z Pr(>|z|) Village–kalungas −0.86 0.20 −4.23 <0.01 CW–Amazon 3.66 0.12 29.85 <0.01 Town–kalungas −0.59 0.20 −3.03 0.02 NE–Amazon 4.31 0.11 37.69 <0.01 Town–village 0.27 0.22 1.22 0.74 NE–CW 0.64 0.15 4.34 <0.01 NORTHEAST δ15N Estimate Std. err z Pr(>|z|) Estimate SE z Pr CW–Amazon −1.19 0.06 −20.31 <0.01 (>|z|) NE–Amazon −0.62 0.05 −11.35 <0.01 δ13C NE–CW 0.57 0.07 8.09 <0.01 City–capital −0.47 0.10 −4.79 <0.01 Note: Differences are considered significant when Pr(>|z|) is lower Town-coast–capital −0.12 0.11 −1.05 0.83 than 0.05. NARDOTO ET AL. 7

TABLE 3 (Continued) remote villages (Figure 4). On the other hand, no difference between gender was detected in the two other regions (Figure 4). NORTHEAST In order to better constrain the contribution of different foodstuff Estimate SE z Pr to these populations, stable isotope ratios of fingernails and putative (>|z|) food sources were compared through a bi-plotδ13C vs. δ15N Village-coast–capital −0.18 0.14 −1.30 0.68 (Figures 5–7). We included the following putative food sources in this Village-inland–capital −0.18 0.11 −1.63 0.47 comparison: fish, cassava, rice, beans, commercial chicken, beef, and – Town-coast city 0.35 0.12 3.06 0.02 processed foods. In the Northeast region, we included for comparison Village-coast–city 0.30 0.14 2.16 0.19 fingernails collected from residents of a remote ocean island (Apeú- Village-inland–city 0.30 0.11 2.74 0.06 Salvador) located on the coast of the Pará State (Figure 7). Village-coast–town-coast −0.06 0.15 −0.38 1.00 In general, beef consumption seems to be low in all regions; on Village-inland–town-coast −0.05 0.12 −0.45 0.99 the other hand, the consumption of chicken and processed food Village-inland–village-coast 0.00 0.14 0.01 1.00 seems to be widespread (Figures 5–7). In the Amazon region, as the δ15N size of the urban settlement decreases, the consumption of fish, fari- City–capital −0.13 0.09 −1.45 0.59 nha, rice, and beans increase, and the consumption of commercial chicken and processed foods decreases (Figure 5). The δ15N of finger- Town-coast–capital −0.27 0.10 −2.60 0.07 nails of the rural population in the Amazon was higher than in other Village-coast–capital 0.08 0.12 0.66 0.96 regions probably because fish, cassava, and rice have higher δ15N Village-inland–capital −0.19 0.10 −1.98 0.27 values than commercial chicken and processed foods (Figure 5). Town-coast–city −0.14 0.11 −1.32 0.68 The same pattern of food consumption was observed in the Village-coast–city 0.21 0.13 1.70 0.43 Center-West region of the country, with more remote villages of the – − − Village-inland city 0.06 0.10 0.62 0.97 Chapadas dos Veadeiros and Kalunga villages tending to consume Village-coast–town-coast 0.35 0.14 2.60 0.07 mainly Brazilian staple foods, while larger cities tend to consume more Village-inland–town-coast 0.08 0.11 0.69 0.96 commercial chicken and processed food (Figure 6). However, this calls Village-inland–village-coast −0.28 0.13 −2.11 0.21 attention to the fact that in some communities of the Chapadas dos Veadeiros a sharp increase in the δ15N values was observed (Figure 6). Note: Differences are considered significant when Pr(>|z|) is lower than 0.05. Although there were significant small statistical differences, it seems that residents from all types of urban settlements have a similar diet in the Northeast region (Figure 7). The observed lower δ15N fingernail samples in the villages and capital, and lower and similar in values of fishing villages compared to the remote island of Apeú- fingernails from cities and towns (Table 3). Salvador suggest lower consumption of marine fish and seafood in The range of δ13C values was smaller in the Center-West than in these coastal communities than in the ocean island (Figure 7). the Amazon region; however, the same pattern persisted (Figure 3). Based on the bi-plot δ13C versus δ15N of fingernails, we also The capital, Brasília, had the highest δ13C, followed by the town of noticed that in each remote village, there was a high degree of vari- Alto Paraíso, then by remote towns of Chapada dos Veadeiros, ability in food consumption among residents. In 9 out of 15 remote decreasing further in the Kalungas villages (Figure 3). The δ13C was villages of the Amazon region, we found a significant inverse correla- significantly higher in the capital than in the Chapada dos Veadeiros tion between δ13C and δ15N of fingernails (Table 4). and Kalungas villages, but not significantly different than δ13C values When the overall data are grouped between larger market- of Alto Paraíso (town) and villages near by this town (Table 3). oriented urban centers and remote villages, a clear distinction among The δ15N values of fingernails were highest in the towns of these two groups appears (Figure 8). While in the aggregate data on Chapada dos Veadeiros (Table 3), and villages of the Kalungas, which remote villages the inverse correlation between δ13C and δ15N is very were higher than Alto Paraíso and its village, but not higher than the significant, in the larger urban centers, such inverse correlation does Capital (Figure 3). not hold, mainly because the lower δ13C values of urban residents are Finally, on the contrary, differences of δ13C of fingernails were not correlated with higher δ15N values as observed in remote villages. very small between urban settlements in the Northeast region Therefore, it seems that in urban centers there is wide variability in (Figure 3), and on the capital had δ13C values statistically higher than δ13C, but not in δ15N of fingernails (Figure 8). the city (Table 3). On the other hand, there was not a significant difference between δ15N values of fingernails between urban settlements (Table 3). 4 | DISCUSSION We were also interested in differences between genders, and in general, we found small, but significant differences in the Amazon The results of this study confirm earlier findings on the importance of 13 15 region, where women's fingernails had higher δ C and lower δ N C4 plants in the diet of Brazilians over a much broader region than values than men (p < .01), such differences were accentuated in small surveyed in previous studies (de Jesus Silva et al., 2019; Lima 8 NARDOTO ET AL.

FIGURE 3 Box-plot of δ13C and δ15N of fingernails in the three sampling regions: (a) Amazon, (b) Center-West, and (c) Northeast. In the Center-West region, “village-K” denotes samples collected in Kalunga villages, and in the Northeast region, “v-coast” and “v-inland” denote samples collected in coastal and inland villages, respectively. Black dots represent the isotopic ratio of fingernails; horizontal bars inside the box represent median isotopic ratios, the lower and upper lines of the box represent the first and the third quartiles, the bar represents 1.5 times the interquartile range

et al., 2019; Nardoto et al., 2006, 2011; Reinaldo et al., 2015; Rodri- both related to differences in socioeconomic status (Bender gues et al., 2016). In addition, the main hypothesis of this study was et al., 2014) or cultural (Hispanic × Non-Hispanic white) influences in supported because we observed that in more remote villages, where the diet (Valenzuela et al., 2018). access to food markets is more challenging, lower δ13C values prevail, It seems that personal preferences coupled with purchasing suggesting that Brazilian staple foods (rice, beans, and farinha) still power will drive the replacement of local staple C3-like foods by C4- dominate. On the other hand, in areas with easy access to food mar- like foods purchased at the individual level. Therefore, we think it is kets, δ13C values were higher, suggesting a change to a diet based on fair to conclude that the nutrition transition has not yet reached some

C4 plants, typical of a Brazilian supermarket diet (sugary products, fro- remote villages in the country or that the nutrition transition has not zen chicken, preserved meats, dairy products and derivatives). yet reached all residents of these remote villages. On the other hand, Recently, Correia et al. (2019) working on the dietary isotopic signa- we also observed that several villages in different regions of Brazil tures of tropical African communities reported that the hunter– already adhere to the supermarket diet or that some residents of gatherer community have low carbon and high nitrogen isotopic these villages are already favoring processed food. This trend is well ratios, consistent with the tropical forest environment they inhabit. In illustrated in Figure 8, which compares the isotopic composition of contrast, the agriculturalist and pastoralist communities have high car- residents from all remote villages with the isotopic composition of fin- bon and relatively low nitrogen isotopic ratios, indicating they have gernails from residents of medium to large cities. diverged from their traditional way of life, indicating an increase in In large urban centers, the δ13C values of the fingernails reflected sedentism and inclusion in market economies. a clear influence of C4 plants in their diet. On the other hand, in the In most of the remote villages studied, even in the more remote remote villages, the decrease in δ13C of fingernails indicated a pre- ones, we found a high degree of variability in food habits among their dominance of C3 plants in the diet, and it was followed by an increase residents. This variability is expressed by a significant inverse correla- in δ15N of fingernails. This pattern indicates either a higher consumption between δ13C and δ15N fingernail values, suggesting that “market tion of fish, in the case of the Amazon region, or an increase in the integration” does not affect everyone equally in each community. This consumption of cassava and rice, which are C3-like staple foods and local variability in stable isotopes has also been detected elsewhere, have high δ15N values. In this regard, we suspected that the high δ15N NARDOTO ET AL. 9

FIGURE 4 Box-plot of δ13C (upper panel) and δ15N (lower panel) of fingernails of males and females of cities (including the capital— Manaus), towns, and villages of the Amazon region. Black dots represent the isotopic ratio of fingernails; horizontal bars inside the box represent median isotopic ratios, the lower and upper lines of the box represent the first and the third quartiles, the bar represents 1.5 times the interquartile range

values of fingernails found in some remote village of the Center-West region, especially in Colinas do Sul, could be attributed not only to freshwater fish, but also to a significant presence of bushmeat in the diet of these people, since bushmeat in Brazil generally has high δ15N values (Nardoto et al., 2006). We found low δ15N values among residents of coastal fishing villages of the Rio Grande do Norte State compared with δ15Nvaluesof residents of the ocean island Apeú-Salvador. This trend was unex- FIGURE 5 Bi-plot of δ13C versus δ15N of fingernails (black circles) pected since according to a study on food habits of these villages, fish- and putative food sources in the Amazon region: (a) Manaus (capital of the State of Amazon); (b) Cities; (c) Towns; and (d) Villages. Putative ing was the most important economic activity of these villages. On the food sources are represented by rectangles delimited by dashed lines. other hand, Silva (2018) argued that although fishing is indeed an The mean isotopic values are in the center of the rectangles, and the important activity, fishermen tend to save most of their catch to be sold sides are delimited by the standard deviations of the mean isotopic to provide a cash supply. Fish and seafood were replaced by processed values. Trophic fractionations of 3 and 5‰ for carbon and nitrogen food since in these villages food markets are easily accessible; this is were applied to the fingernail data (see Abdalla Filho et al., 2019) 10 NARDOTO ET AL.

particularly true among the young population that eat less fish than elderly people in these villages. A similar trend was found in other fishing villages of the Northeast (Pinto et al., 2016), and Southeast of the country (Hanazaki & Begossi, 2010; MacCord & Begossi, 2006; Pinto, Mour~ao, & Alves, 2017). Only in the Amazon region, the δ15N of fingernails was consis- tently lower in females than in males in all urban settlement types. One possible explanation for such a trend would be the distinct food consumption between gender. Indeed, Piperata, McSweeney, and Murrieta (2016), observed in mothers of riverine villages, a decrease

in the consumption of home-produced farinha, fish, and açai (C3-like food), followed by an increase in processed food, which includes sev-

eral C4-like foods such as frozen chicken, crackers, and salted meat. As processed food items in the Amazon region generally have lower δ15N than farinha and fish, such differences in food consumption would explain the lower δ15N of women's fingernails. However, this would imply lower δ13C values in women's fingernails, which was indeed observed especially in remote villages, where the average δ13C of women's fingernails was −22.5 ± 1.7‰ compared to −22.1 ± 1.8‰ (p < .01) observed in men. A second possible explanation for the difference noted between gender would be to consider that men are positioned in a higher trophic level than women by eating more fish or meat. This would imply a difference in social status in the community that would render a gender bias in diet or different access to food resources. This trend has been seen in Amerindians of the Amazon region like the Xavantes in Brazil (Welch et al., 2009) or among the Tsimane in Bolivia (Rosinger, Tanner, & Leonard, 2013). But it has yet to be confirmed among the riverine dwellers of the Amazon River. Such changes in food consumption by some residents of remote villages relying more on purchased food has several implications. First, it is important to remember that the main conclusion of pioneering studies on food consumption in the Amazon and in some parts of the Northeast has primarily been about food scarcity and malnutrition (de Castro, 1946; Hanson, 1933). Therefore, it is a positive aspect of our findings that residents of such villages now have the purchasing power to change their diets, which was suggested to be highly homogenous in the past, incorporating different products that they have not previously accessed or had no cash to buy. There are several studies showing that this food transition was possible due to the implementation of a major cash-transfer program (called as Programa Bolsa Família) for poor families together with other cash-transfer programs established by the Brazilian government at the beginning of the 2000s (Cotta & Machado, 2013; de Jesus Silva et al., 2017, 2019; Dufour, Piperata, Murrieta, Wilson, & Williams, 2016; Lima et al., 2019; Piperata, 2007, 2016; Schor & Azenha, 2017; Schor, Tavares-Pinto, Avelino, & Ribeiro, 2015). FIGURE 6 Bi-plot of δ13C versus δ15Noffingernails(blackcircles) The capacity to purchase food is also important in order to buffer and putative food sources in the Center-West region: (a) Brasília (capital of the country); (b) Towns; (c) Kalunga villages; and (d) Other villages. seasonal scarcity of locally produced food. For instance, such scarcity The mean isotopic values are in the center of the rectangles, and the is frequent among riverine dwellers of the Solimões-Amazon River sides are delimited by the standard deviations of the mean isotopic due to the annual flooding when fish spread over the extensive flood- values. A trophic fractionation of 3 and 5‰ for carbon and nitrogen plains making it challenging to catch them (Castello, Isaac, & were applied to the fingernail data (see Abdalla Filho et al., 2019) Thapa, 2015; Fabré, Castello, Isaac, & Batista, 2017). Additionally, also NARDOTO ET AL. 11

TABLE 4 Statistical parameters for the regression analysis between δ13C versus δ15N in villages of the Amazon region

2 Village r adj df df Fp Porto Nazaré −.03 1 17 0.52 .48 Costa do Caldeir~ao .41 1 86 61.48 .00 Boa Esperança .29 1 81 34.11 .00 Jarauá .00 1 56 0.92 .34 Nova Jerusalém .21 1 67 19.19 .00 Santa Maria .39 1 33 22.97 .00 S~ao Francisco −.01 1 29 0.63 .43 Paquequer .44 1 67 54.66 .00 S~ao Jorge .01 1 11 1.08 .32 Maguari .18 1 4 2.08 .22 Capacete .68 1 8 20.18 .00 Novo Sao~ Francisco −.05 1 16 0.16 .70 Terezina III .23 1 28 9.71 .00 N.S. Perpétudo Socorro .53 1 20 24.68 .00 Aman~a .15 1 147 26.70 .00

2 Abbreviations: df, degrees of freedom; F, statistics F, p, probability; r adj, adjusted regression coefficient.

FIGURE 7 Bi-plot of δ13C versus δ15N of fingernails (black circles) and putative food sources in the Northeast region: (a) Natal (capital of the State of the Rio Grande do Norte); (b) city of Mossoró; (c) inland FIGURE 8 Bi-plot of δ13C versus δ15N of fingernails grouping the villages; and (d) coastal villages. The mean isotopic values are in the data by villages (a) and cities (b). The black line represents the center of the rectangles, and the sides are delimited by the standard regression line between δ13C and δ15N deviations of the mean isotopic values. The small white circles represent fingernails sampled in the ocean island of Apeú-Salvador, located on the coast of the State of Pará, in the northern region of the due to seasonal flooding, dry land is not available for cultivation, Brazil. A trophic fractionation of 3 and 5‰ for carbon and nitrogen decreasing cash and staple crop production (Schor et al., 2018). The were applied to the fingernail data (see Abdalla Filho et al., 2019) same in true for the kalungas; however, the main problem in their 12 NARDOTO ET AL. region is not flooding, but seasonal droughts that may lead to food women: Investigating socioeconomic differences. American Journal of – scarcity (Fernandes, 2014; Ungarelli, 2009). Human Biology, 27(2), 207 218. Blackwell, A. D., Pryor, G., Pozo, J., Tiwia, W., & Sugiyama, L. S. (2009). On the negative side of the nutrient transition, there is the bur- Growth and market integration in Amazonia: A comparison of growth “ ” den of diseases associated with the so-called western diet : obesity, indicators between Shaur, Shiwiar, and Nonindigenous school children. high blood pressure, and diabetes, which are now much more com- American Journal of Human Biology, 21, 161–171. 13 15 34 mon among residents of remote villages than before (Arrifano Bol, R., & Pflieger, C. (2002). Stable isotope ( C, N and S) analysis of the hair of modern humans and their domestic animals. Rapid Commu- et al., 2018; Brito, Libardi, & Ghiberto, 2009; Cunha, Marques, & nications in Mass Spectrometry, 16, 2195–2200. Dórea, 2018; dos Santos, 2016; França, Lima, & Vieira, 2016; Piperata, Brito, A. D. S., Libardi, P. L., & Ghiberto, P. J. (2009). Componentes do bal- Spence, Da-Gloria, & Hubbe, 2011). In this sense, it is crucial that anço de água no solo com cana-de-açúcar, com e sem adubaç~ao cash-transfer programs be followed by efforts to increase awareness nitrogenada. Rev Bras Ciência Do Solo, 33, 295–303. Castello, L., Isaac, V. J., & Thapa, R. (2015). Flood pulse effects on multi- of health problems caused by diet changes among residents of these species fishery yields in the Lower Amazon. Royal Society Open Sci- remote villages, empowering them to make their own food choices by ence, 2, 150299. balancing the beneficial and the deleterious health effects of the food de Castro, J. (1946). Geografia da Fome, o dilema brasileiro: pao~ ou aço. Rio transition. de Janeiro: Civilizaç~ao Brasileira. Coimbra, C. E., Jr. (1984). Estudos de Ecologia Humana entre os Suruí do parque indígena Aripuan~a, Rondônia. 1. O uso de larvas de coleôpteros ACKNOWLEDGMENTS (Bruchidae e Curculionidae) na alimentaç~ao. Rev Bras Zool, 2,35–47. We are grateful to all volunteers that donated a piece of their finger- Coletta, L. D., Pereira, A. L., Coelho, A. D., Savino, V. J. M., nails to make this work possible. This study was supported by the Foun- Menten, J. F. M., Correr, E., … Martinelli, L. A. (2012). Barn vs. free- dation Research Support of the State of S~ao Paulo (FAPESP) and the range chickens: Differences in their diets determined by stable isotopes. Food Chemistry, 131, 155–160. National Council for Brazilian Research (CNPq). We thank Jim Hesson Correia, M. A., Foley, R., O'Connell, T. C., Ramirez-Rozzi, F., & Lahr, M. M. from Academic English Solutions for the revision of the English. (2019). Carbon and nitrogen isotopic signatures of hair, nail and breath from tropical African human populations. Rapid Communications in – DATA AVAILABILITY STATEMENT Mass Spectrometry, 33, 1761 1773. Cotta, R. M. M., & Machado, J. C. (2013). Programa Bolsa Família e The raw dataset will become available to download through the link segurança alimentar e nutricional no Brasil: revis~ao crítica da literatura. that will be generated by a Mendeley account. Rev Panam Salud Pública, 33,54–60. Cunha, M. P. L., Marques, R. C., & Dórea, J. G. (2018). Child nutritional sta- ORCID tus in the changing socioeconomic region of the northern Amazon, Brazil. International Journal of Environmental Research and Public Health, Gabriela B. Nardoto https://orcid.org/0000-0001-8062-7417 15,1–12. 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