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The Domestication of Annatto (Bixa orellana) from Bixa urucurana in Amazonia Priscila Ambrósio Moreira, Juliana Lins, Gabriel Dequigiovanni, Elizabeth Ann Veasey & Charles R. Clement Economic Botany ISSN 0013-0001 Econ Bot DOI 10.1007/s12231-015-9304-0

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The Domestication of Annatto (Bixa orellana) from Bixa urucurana in Amazonia1 PRISCILA AMBRÓSIO MOREIRA*,2, JULIANA LINS2,3, GABRIEL DEQUIGIOVANNI4, ELIZABETH ANN VEASEY4, AND CHARLES R. CLEMENT3 2

Post–Graduate Program in Botany, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas (AM), Brazil 3 Coordenação de Tecnologia e Inovação, INPA, Manaus, AM, Brazil 4 Post–Graduate Program in Genetics and Plant Breeding, Escola Superior de Agricultura BLuiz de Queiroz^ (ESALQ/USP), Piracicaba, São Paulo, Brazil *Corresponding author; e-mail: [email protected], [email protected] The Domestication of Annatto (Bixa orellana) from Bixa urucurana in Amazonia. Annatto (Bixa orellana) is an important colorant domesticated in the Neotropics, although it is not clear where or from which wild populations. We reviewed the available biological, archaeological, and ethnographic information about annatto, and integrated this with our recent ethnobotanical observations of cultivated and non–cultivated populations in order to evaluate the hypothesis that what is classified as Bixa urucurana is the wild ancestor of cultivated annatto, Bixa orellana. Most B. urucurana populations we found in Amazonia occurred in open forests or anthropogenic landscapes, although never cultivated, and always associated with riparian environments. While cultivated annatto always produces abundant pigment, B. urucurana populations that we observed contained variable amounts of pigment, from very little to nearly the amount of cultivated annatto, suggesting gene flow from cultivated to non–cultivated. Bixa urucurana has indehiscent fruits, which indicate changes in dehiscence during annatto domestication, a notable feature rarely found in other tree species. Local residents identified the non–cultivated populations as wild annatto (urucum bravo), and they emphasized their smaller fruits with less pigment, their spontaneous regeneration, their non–use, and that they hybridize with cultivated annatto. Ethnography identified the symbolic importance of annatto, but an explicit mention of origin only comes from southern Amazonia. Although the oldest annatto archaeological record came from the Caribbean, domestication occurred in northern South America, since B. urucurana does not occur in the Caribbean. Traditional ecological knowledge and morphology identified the close relationship between B. urucurana (never cultivated) and B. orellana (always cultivated). Evidence reported here strongly supports Kuntze’s (1925) suggestion that Bixa urucurana Willd. is a variety of B. orellana L., thus identifying the wild ancestor of cultivated annatto. A domesticação do urucum (Bixa orellana) a partir de Bixa urucurana na Amazônia. Urucum (Bixa orellana) é um importante corante domesticado na região Neotropical, mas não é claro onde ou a partir de quais populações silvestres. Nós revisamos as informações biológicas, arqueológicas e etnográficas disponíveis sobre urucum, e integramos com nossas recentes observações etnobotânicas de populações cultivadas e não cultivadas com o objetivo de avaliar a hipótese de que o que é classificado como Bixa urucurana seja o ancestral silvestre do urucum cultivado, Bixa orellana. A maioria das populações de Bixa urucurana que encontramos na Amazônia foi 1 Received 12 December 2013; accepted 23 February 2015; published online ___________

Economic Botany, XX(X), 2015, pp. 1–9 © 2015, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.

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encontrada em florestas abertas, ambientes antropogênicos, embora nunca cultivadas, e sempre associadas com ambientes ripários. Enquanto o urucum cultivado sempre produz pigmento em abundância, as populações de B. urucurana que observamos continham quantidades variáveis de pigmento, desde muito pouco até quantidade próxima à produzida pelo urucum cultivado, sugerindo fluxo gênico de populações cultivadas para não cultivadas. Bixa urucurana possui frutos indeiscentes, o que indica mudanças na deiscência ao longo do processo de domesticação do urucum, uma característica notável e raramente encontrada em outras espécies arbóreas. Populações locais identificaram as populações não cultivadas como Burucum bravo^, e enfatizaram seus frutos menores e com menos pigmentação, sua regeneração espontânea, seu não uso e a possibilidade de hibridizar com o urucum cultivado. Registros etnográficos identificaram a importância simbólica do urucum, mas uma menção explícita de origem vem somente do sul da Amazônia. Embora o registro arqueológico mais antigo do urucum esteja no Caribe, a domesticação ocorreu no Norte da América do Sul, uma vez que B. urucurana não ocorre no Caribe. Conhecimento ecológico tradicional e as informações biológicas disponíveis apoiam a proximidade entre B. urucurana (nunca cultivado) e B. orellana (sempre cultivado). As evidências aqui relatadas apoiam fortemente a sugestão de Kuntze (1925), de que Bixa urucurana Willd. seja uma variedade de B. orellana L., identificando, portanto, o ancestral silvestre do urucum cultivado. Key Words:

Ethnobotany, taxonomy, archaeology, domestication syndrome..

Introduction Annatto (Bixa orellana L., Bixaceae) is an important colorant that had domesticated populations grown throughout the Neotropics at the time of European contact (Clement 1999; Patiño 1967). It was used in many different cultural contexts for the red–orange pigment in the arils around its seeds (León 2000). When Europeans conquered the Americas, the native peoples in the lowlands were often described as having their skin painted with annatto (Patiño 1967). At that time there was already long distance trade among lowland groups, such as the Guaycuru, Arawak, and Guarani (Métraux 1948). This trade was based on an annatto paste, called Bpanecillos,^ Bpelotas,^ or Bbolos^ by the chroniclers (Donkin 1974). The paste was prepared by rinsing the aril of the seeds in water, then drying the solution in the bottom of a bowl, and finally the powder was mixed with animal fat or vegetable gum (Lévi–Strauss 1987; Patiño 1967). In South America, this paste was commonly used as daily body paint, for protection against insects and healing wounds, as well as body paint in ceremonies and warfare (León 2000; Sauer 1987). In Mesoamerica, annatto powder was used to color chocolate drinks, with a possible ritual significance (Norton 2008; Sauer 1987). Throughout the 16th to 19th centuries, annatto pigment continued as an important item of trade and exchange, and was exported to Europe (Patiño 1967).

The current culinary use of annatto as a food coloring (colorau) by traditional Amazonian populations was inspired by the Spanish, who considered annatto similar to saffron (Crocus sativus L.) (Ocampo 1983). Annatto is now commercially valued by the food industry because it replaces synthetic dyes developed in the last century (Leal and Clavijo 2010). World production is about 17,500 tons/year, of which 68% originates from Northeast Brazil, mostly from family farmers (Franco et al. 2008). However, the once–widespread use of homemade colorau has been replaced by the commercial product. Families in traditional communities think that it is easier to buy the product than prepare it, even though the knowledge to make it is still reported. Ethnotaxonomic studies show that some indigenous peoples recognize different types of annatto. The Kayapó, a Ge–speaking people inhabiting the Xingu River basin in Brazil’s southern state Pará, cultivate four varieties (p’y kumrenx, p’y poi ti, p’y krã re, p’y jabiê) (Posey 1985). The Ka’apor, a Tupi– speaking people inhabiting the region of the Gurupi River in Maranhão, eastern Amazonia, recognize two types: one cultivated (uruku) and the other wild (urukuran’ ), which also occurs in secondary forests (Balée 1994). This wild type has not been identified botanically, but Balée (pers. comm.) thinks it may be B. arborea. According to the only systematic study of the genus (Baer 1976), five species of Bixa are

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recognized (B. orellana, B. arborea, B. excelsa, B. platycarpa, and B. urucurana). The main distinction between these species is growth habit, which can be either a tree or a shrub. In the first case, trees can reach 30 m in height, as observed in B. arborea, described by Huber (1910) in Bragança, Pará; B. excelsa, described by Gleason and Krukoff (1934) along the Envira River, a tributary of the Juruá River, southwestern Amazonia; and B. platycarpa, described by Ruiz and Pavón (Don 1831) in Peru. The other species are shrubs: B. orellana, which was described by Linnaeus (1753), and B. urucurana, described by Willdenow (1809) in Brazil (without an identified locality). The latter’s specific epithet is derived from the Tupi urukuran’i-), in which ran’i- or rana means false, and is often attributed to wild populations of a species with domesticated populations. Domestication is an evolutionary process mediated by humans that modifies morphological and auto–ecological adaptations in plant populations, and these often cause behavioral changes in human populations (Rindos 1984, p.138). The most highly selected cultivated plants are incapable of survival in the wild (Harlan 1992; Rindos 1984). Although domesticated annatto remains relatively common in Amazonian and other Neotropical home gardens, its history of domestication is unknown (Schultes 1984). The identification of wild forms is important to identify centers of domestication and decipher the history of domestication, as well as to guide future prospection for crop development (Harlan 1992). Adolpho Ducke (1946) hypothesized that B. excelsa might have been the wild ancestor of B. orellana, which was accepted by Schultes (1984) and cited by Meyer et al. (2012). However, we think tree species of Bixa should be excluded as candidates for the wild form of annatto, since a few thousand years of domestication is unlikely to be enough time to turn a large tree into a shrub exclusively by mass selection. No other domesticated shrubs are reported to have originated from large trees (Meyer et al. 2012). This same argument excludes B. arborea as the wild ancestor of annatto, although it may be managed in secondary forests in eastern Amazonia (Balée 1994). In his systematic study of Bixa, Baer (1976)made no direct statements about the domestication of annatto, but he offered some clues when he emphasized the similarity between B. orellana and B. urucurana, and that the former is

planted and the latter is collected from the wild. As both are the only shrubs in the genus, the most parsimonious hypothesis is that cultivated annatto originated from Bixa urucurana. This agrees with the taxonomic proposal of Pilger, published by Kuntze (1925), who transferred Bixa urucurana to a variety of B. orellana. Our goal is to review the available biological, archaeological, and ethnographic information about annatto (Bixa orellana L.), and integrate them with our recent ethnobotanical observations of cultivated and non–cultivated annatto populations in order to evaluate the hypothesis that what is now classified as Bixa urucurana is the wild ancestor of cultivated annatto, Bixa orellana.

Methods From 2009 to 2013, we visited 30 villages along the Branco River, 7 along the Negro River, 28 along the Solimões River, 36 along the Amazon River, 18 along the Madeira River, and 30 along the Guaporé River, in most of which we found cultivated and more rarely non–cultivated annatto (Table 1). Non–cultivated annatto was identified by local residents as wild (urucum bravo) and as regenerating spontaneously, often in anthropogenic landscapes, more Table 1. NUMBER OF INDIVIDUALS OF CULTIVATED AND NON–CULTIVATED ANNATTO OBSERVED ALONG SIX MAJOR RIVERS OF THE AMAZON BASIN.*

River

Cultivated

Branco

39

Negro Solimões Amazonas

21 46 64

Madeira

163

Guaporé

62

Total

395

*

Non–Cultivated

2 1 1 0 5 70 1 31 33 20 25 48 9

(Mucajaí, RR) (Rorainópolis, RR) (Novo Airão, AM) (Monte Alegre, PA) (Almeirim, PA) (Nova Mamoré, RO) (Corumbiara, RO) (Cerejeiras, RO) (Ariquemes, RO) (Ji–Paraná, RO) (Cabixi, RO) (São Francisco do Guaporé, RO)

246

The municipalities where non–cultivated annatto was found are indicated in parentheses; AM = Amazonas, PA = Pará, RO = Rondônia, and RR = Roraima.

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rarely in apparently undisturbed landscapes, and having smaller fruits with less pigment. Fruit morphology, color and quantity of pigment, growth habit, local names, propagation methods, and uses were noted for all cultivated plants and up to 30 randomly chosen plants in non–cultivated populations. These features were compared with the descriptions in Baer (1976), with botanical collections available in the INPA herbarium, Manaus, and agronomic studies (Akshatha et al. 2011). The geographical distribution of Bixa species available at CRIA (Centro de Referência em Informação Ambiental), GBIF (Global Biodiversity Information Facility), and our cultivated and non–cultivated samples were plotted in a map using ArcGIS 9.3 software (ESRI) (Fig. 1). We also reviewed the bibliography to identify present and early annatto uses by traditional peoples reported in ethnographies and archaeological sources.

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Results and Discussion BIOLOGICAL EVIDENCE We observed a total of 395 cultivated annatto plants distributed along six of the major rivers of the Amazon Basin, as well as 246 non–cultivated annatto plants distributed along five of them, sometimes in large populations (Fig. 1, Table 1). This wide geographical distribution of non–cultivated annatto agrees with Baer’s (1976) distribution of B. urucurana, as well as with online distribution databases (Fig. 1). According to Ducke, B. urucurana commonly grows on bluffs adjacent to floodplain forests (Ducke 1939, as cited in Baer 1976). Similarly, the largest population of non–cultivated annatto we observed (approximately 70 plants in a ¼–hectare patch) was found on a bluff along the Paru River

Fig. 1. Geographical distribution of shrub and tree species of Bixa in northern South America, and localities where we found cultivated and non–cultivated populations of annatto in Brazilian Amazonia: Roraima (RR), Amazonas (AM), Pará (PA), Rondônia (RO), Acre (AC), Amapá (AP), Maranhão (MA), and Mato Grosso (MT).

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(left bank of the lower Amazon River), near Almeirim in northern Pará (Table 1, Fig. 2). Smaller populations of non–cultivated annatto were found in other parts of Amazonia, both in terra firme (non–flooded) and igapó (flooded by black or clear waters) landscapes, although rarer along igapós. Most populations were found in open forests, such as woody savannas, and anthropogenic environments, such as roadsides, pastures, burned fallows, and plantations of other crops, and always associated with riparian environments. The variability of morphological characteristics in cultivated and non–cultivated populations, especially pigment production from the aril of the seeds, the main part of the plant used by humans, is the key to understanding domestication and subsequent dispersal (Table 2). While cultivated annatto produces abundant pigment, B. urucurana has little pigment in its scanty arils (Baer 1976). The non–cultivated annatto we observed contains variable amounts of pigment, from very little to nearly the amount of cultivated annatto. In southwestern Amazonia, non–cultivated annatto sometimes has arils that fully covered the seeds, whereas in the rest of the observed distribution the arils were scanty. High pigment production in non–cultivated annatto was found where there are adjacent areas of intense cultivation of annatto, strongly suggesting gene flow

from cultivated to non–cultivated by cross pollination and introgression. In all home gardens visited, all cultivated annatto originated from seed propagation. If annatto is fully domesticated, it would be expected that seed dispersal of cultivated annatto would be completely dependent on humans, but because there are the possibilities of escapes, the dispersal biology of seeds requires further study. Dehiscence is a distinctive difference between B. urucurana and cultivated annatto (Table 2). B. urucurana and the non–cultivated annatto we observed have indehiscent fruits, which remain closed after maturation. Cultivated annatto is dehiscent, exposing its red–pigmented seeds to potential dispersers while still attached to the shrub. If our hypothesis is correct, dehiscence in cultivated annatto is a consequence of selection pressure for more seeds and pigment. This type of fruit, considered superior by agronomists, is associated with larger ovate fruits (Akshatha et al. 2011). Selection of these features should indirectly have favored the spontaneous opening of an indehiscent wild ancestor. Dispersal strategies in cultivated and non–cultivated annatto are quite different. The whole non– cultivated fruit may fall into the river and be transported to another region downstream (Baer 1976). The flexible spines of the fruit may increase

Fig. 2. Above. A population of non–cultivated annatto found along the Paru River (left bank of the lower Amazon River), Pará, Brazil. Below. Fruits and seeds of this non–cultivated annatto.

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Table 2. COMPARISON OF DOMESTICATION SYNDROME TRAITS IN BIXA ORELLANA AND B. URUCURANA, BOTH BASED ON DATA IN BAER’S (1976) DESCRIPTIONS, WITH ADDITIONAL DESCRIPTIONS FROM AGRONOMIC STUDIES OF CULTIVATED ANNATTO (AKSHATHA ET AL. 2011), AND OUR ETHNOBOTANICAL OBSERVATIONS OF CULTIVATED AND NON– CULTIVATED ANNATTO IN AMAZONIAN HOME GARDENS AND ADJACENT AREAS.

Bixa orellana

Trait Fruit shape Fruit size (cm) Seed number Aril with pigment Pigment color Dehiscence

Cultivated Oval, spherical, conical 2.5–4.5 30–60 Entire seed Reddish–orange Dehiscent

the chances for it to Bcatch^ a plant along a riverbank and its seeds germinate before they lose their viability. This dispersal pattern would explain the wide distribution of B. urucurana and its preference for riparian habitats, while cultivated annatto needs people to disperse seeds, mostly in upland locations. Based on these observations and Baer’s (1976) descriptions, the non–cultivated annatto we observed is B. urucurana. The contrasts between B. urucurana and B. orellana represent the domestication syndrome (Table 2) and strongly support the hypothesis that B. urucurana is the wild ancestor of B. orellana.

ARCHAEOLOGICAL EVIDENCE Archaeological records can provide proof of the presence of annatto in ancient human settlements. The only archaeological record of annatto in Amazonia comes from the Llanos de Mojos, in lowland Bolivia, dated to 2400 years before present (BP) (Erickson 1995). However, annatto was found in other places in the Neotropics, such as Plum Piece, a pre–Arawak site dated to 3700–3600 BP on the Caribbean island of Saba (Pagán–Jiménez 2013), and Caral, an urban settlement that flourished in the Late Archaic period (3000–1800 BP) in central western Peru (Solis 2006). In Mesoamerica, where numerous other South American crops were introduced also, a Proto–Mayan name for annatto was reconstructed linguistically and dated to 2400 BP (Brown 2010). In Calima, southwestern Colombia, carbonized seeds were dated to 1310–700 BP (Morcote–Ríos 2006). In the Peruaçu Valley, Minas Gerais, Brazil, annatto seeds were found in archaeological sites dated to 1010–570 BP (Freitas 2004). Although the oldest archaeological record is from the Caribbean, the geographical distribution

Bixa urucurana

Non–Cultivated Spherical, heart–shaped 1–2 1–10 Entire to sparse Orange–yellow Indehiscent

Spherical, tipped spherical 1–2 2–10 Partial to sparse Not described Indehiscent

of Bixa urucurana does not include the Caribbean (Fig. 1), so domestication must have occurred in northern South America.

ETHNOGRAPHICAL EVIDENCE Different indigenous groups of the Amazon Basin have oral histories that mention annatto. Among the Tikuna from western Brazil, annatto Bfigures in the legends of culture heroes^ (Nimuendajú 1952). Similarly, the Guarani, the most expansive Tupi language group, believe that yrukú grows along the road to heaven and it is mentioned as an eternal shrub (Cadogan 1966). In southeastern Amazonia between Maranhão and Pará, where Posey (1987) and Balée (1994) identified wild populations, the Tenetehara (Tupi) believe that Maíra, the creator, hid fire in an annatto stick (Wagley and Galvão 1948). The Bororo, in the periphery of southern Amazonia in Central Brazil, have a tale about the origin of the urucú bush (Lévi–Strauss 1969). Although small in number, all of these narratives suggest symbolic importance, but explicit mentions of origin only come from southern Amazonia. Ethnographies report different intensities of selection practices in a wide variety of environments and cultural contexts. Donkin (1974) argues that selection was minimal and mostly wild seedlings (or escapes) were transplanted to more convenient locations. Similarly, the Nambicuara in southwestern Brazilian Amazonia cultivated annatto in home gardens along the bluffs after burning and opening gallery forests (Lévi–Strauss 1948, 1969), but among other peoples, young individuals of annatto were only transplanted near to home (Lévi–Strauss 1957). This author thought that annatto is a Bwild plant that belongs to the list of those that have not changed when cultivated^ (Lévi–Strauss 1957), but

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recognized it principally in cultivation. The Kayapó, in southeastern Amazonia, cultivate annatto associated with papaya and genipap in forest patches (apêtê) mediated by plant selection practices (Posey 1985). In the 17th–century Guianas, explorers reported that annatto grew in the forest, where the natives collected the substance they needed to prepare the ink (Wilson 1606, cited in Baer 1976). However, Patiño (1967) reports that the Bororo of Central Brazil select individuals of annatto with larger leaves and fruits, and seeds with intense red pigment for propagation. It is clear that the authors cited did not reach a consensus about what is cultivated or wild annatto, and probably also had difficulty in recognizing local selection practices. This is certainly because the authors cited were not specifically studying annatto, but only as one species among a set of useful plants. Thus, the fact that most cultivated plants cited have abundant pigment suggests the existence of selection practices, as suggested by Patiño’s observations, but also that these may be largely unconscious, as suggested by Rindos (1984) for selection in general. Variation in pigment production and fruit size and shape is also recognized by riverine families, as we observed in our field work. Plants that produce little pigment and/or have smaller and spherical fruits are called Bbravos^ (wild). These plants are considered useless and are not cultivated. Local knowledge indicates the occurrence of hybridization between Bmanso^ (Btamed,^ cultivated) and Bbravo^ annatto. According to a dweller of a traditional community along the Paru River in eastern Amazonia, BIf you have tamed annatto near the wild one they cross and the wild prevails. We had a few who crossed and after a while everything was wild.^ This traditional ecological knowledge and available biological information in morphology identified the close relationship between B. urucurana (never cultivated) and B. orellana (always cultivated). The fact that they cross easily confirms that they are the same species.

Conclusions The available biological information confirms that the non–cultivated annatto we observed in Amazonia is Bixa urucurana. It follows that the Pilger’s proposal, published by Kuntze (1925), should be accepted: Bixa orellana var. urucurana (Willd.) Kuntze ex Pilg. Hence, Bixa urucurana is not a distinct species, as affirmed by Baer (1976).

Accepting this means that Ducke’s (1946) hypothesis is wrong: cultivated B. orellana is not derived from B. excelsa, and by extension B. arborea, both large trees, while annatto, is a shrub. While few ethnographic reports contain information about domestication, some from the southern periphery of Amazonia highlight the importance of annatto and one (Bororo) mentions its origin (Lévi–Strauss 1969), including selection practices (Patiño 1967) that are in agreement with the domestication syndrome presented here. Changes in dehiscence are a notable feature of annatto, rarely found in other tree species (Meyer et al. 2012). All other domestication syndrome traits described are expected if B. urucurana is the wild ancestor of cultivated annatto. Phylogeographic studies in progress will be important to confirm that Bixa urucurana is the ancestor of cultivated annatto, as well as to identify the origin of domestication of annatto in Amazonia or showing that it must be sought elsewhere. Acknowledgements We thank numerous families along the main rivers of Amazonia for information and field support; CT–Amazonia, proc. no. 575588/ 2008–0, and FAPESP, proc. no. 2012/08307–5, for primary financial support; the Instituto de Desenvolvimento Agropecuário e Florestal Sustentável do Amazonas (IDAM) in Amazonas and the Empresa de Assistência Técnica e Rural (EMATER) in Pará and Rondônia for field support; PAM thanks CNPq for a doctoral scholarship, JL thanks CNPq for a masters scholarship, GD thanks FAPESP for a doctoral scholarship, and EAV and CRC thank CNPq for research fellowships. We thank William Balée for sharing information about Ka’apor use of annatto, Freddy Leal, three anonymous reviewers, and our associate editor for valuable criticism and suggestions on earlier versions of the manuscript.

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