ARTICLES https://doi.org/10.1038/s41477-020-00835-4 ‘White gold’ guano fertilizer drove agricultural intensification in the Atacama Desert from AD 1000 Francisca Santana-Sagredo 1,2,3,17 ✉ , Rick J. Schulting 3, Pablo Méndez-Quiros 4, Ale Vidal-Elgueta 5, Mauricio Uribe6, Rodrigo Loyola7,8, Anahí Maturana-Fernández6, Francisca P. Díaz9, Claudio Latorre 10,11,12, Virginia B. McRostie1,10, Calogero M. Santoro13, Valentina Mandakovic14, Chris Harrod 2,15,16 and Julia Lee-Thorp 3 The archaeological record shows that large pre-Inca agricultural systems supported settlements for centuries around the ravines and oases of northern Chile’s hyperarid Atacama Desert. This raises questions about how such productivity was achieved and sustained, and its social implications. Using isotopic data of well-preserved ancient plant remains from Atacama sites, we show a dramatic increase in crop nitrogen isotope values (δ15N) from around AD 1000. Maize was most affected, with δ15N values as high as +30‰, and human bone collagen following a similar trend; moreover, their carbon isotope values (δ13C) indicate a con- siderable increase in the consumption of maize at the same time. We attribute the shift to extremely high δ15N values—the high- est in the world for archaeological plants—to the use of seabird guano to fertilize crops. Guano—‘white gold’ as it came to be called—thus sustained agricultural intensification, supporting a substantial population in an otherwise extreme environment. he pre-Hispanic archaeological record of northern Chile We analysed the stable carbon and nitrogen isotope composition preserves large quantities of desiccated crop remains in both of archaeological plants (n = 246) to investigate manuring practices Tdomestic and funerary contexts due to exceptional organic in northern Chile, specifically the Tarapacá region (19°–21° S), preservation in the hyperarid Atacama Desert. Their abundance South Central Andes (Fig. 1 and Supplementary Information 1). and diversity suggest a level of agricultural success that is difficult Based on archaeological context and direct radiocarbon dates on to explain given the region’s arid environment. The transition to plants, our dataset spans the transition to agriculture from around agriculture began here around 1000 bc and eventually supported 1000 bc to the expansion of the Inca State around ad 1450 and the permanent villages and a sizeable regional population1. How was following Spanish conquest in the Tarapacá region, comprising the this development possible, given the extreme environmental condi- Formative (1000 bc–ad 900), Late Intermediate (ad 900–1450), tions? Although evidence for irrigation canals and terraces has been Late (Inca) (ad 1450–1531) and Colonial Periods (ad 1531–1800). identified in the Atacama2,3, water is not the only prerequisite for We further compile human stable carbon and nitrogen isotope data successful agriculture. In the hyperarid core of the Atacama, most from northern Chile to evaluate changes in diet associated with agri- soils must be conditioned for agriculture by the addition of organic cultural practices. The human data includes the Middle Period (ad matter and nutrients, with (possible) exceptions around oases and 500–1000), an archaeological period that is not present in Tarapacá, river terraces where organic content is higher. Recent studies of but is found in the regions of Arica to the north and San Pedro de several hyperarid soils associated with certain archaeological sites Atacama to the south. where agricultural activity took place contain elevated concentra- tions of total organic C, N and PO4. These sites, located between Results 1,000–3,200 m above sea level, date to 2,000, 1,000 and 400 years ago, Published radiocarbon dates together with new direct radiocarbon respectively, suggesting an anthropic influence in those periods4,5. dates on crops from the archaeological sites considered here are The question remains, however, as to how these fields and soils were presented in Supplementary Table 1. Isotopic results for the main enriched (probably using manure) for agricultural purposes. C4 plants, maize (Zea mays) and amaranth (Amaranthus sp.), and 1Escuela de Antropología, Pontificia Universidad Católica de Chile, Santiago, Chile. 2Universidad de Antofagasta Stable Isotope Facility, Instituto Antofagasta, Universidad de Antofagasta, Angamos, Antofagasta, Chile. 3School of Archaeology, University of Oxford, Oxford, UK. 4Departamento de Prehistoria, Programa de Doctorado en Arqueología Prehistórica, Universidad Autónoma de Barcelona, Barcelona, Spain. 5Programa de Doctorado en Biología, mención Ecología, Pontificia Universidad Católica de Chile, Santiago, Chile. 6Departamento de Antropología, Universidad de Chile, Santiago, Chile. 7Instituto de Arqueología y Antropología (IIA), Universidad Católica del Norte (UCN), San Pedro de Atacama, Chile. 8UMR 7055 Prehistoire et Technologie (PreTéch), Université Paris Ouest Nanterre La, Défense, France. 9Departamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago, Chile. 10Centro del Desierto de Atacama, Pontificia Universidad Católica de Chile, Santiago, Chile. 11Departamento de Ecología, Pontificia Universidad Católica de Chile, Santiago, Chile. 12Institute of Ecology and Biodiversity, Pontificia Universidad Católica de Chile, Santiago, Chile. 13Instituto de Alta Investigación, Universidad de Tarapacá, Arica, Chile. 14Programa de Magíster en Antropología, Departamento de Antropología, Universidad de Tarapacá, Arica, Chile. 15Núcleo Milenio INVASAL, Concepción, Chile. 16Instituto de Ciencias Naturales Alexander von Humboldt, Universidad de Antofagasta, Antofagasta, Chile. 17Present address: Escuela de Antropología, Pontificia Universidad Católica de Chile, Santiago, Chile, Santiago, Chile. ✉e-mail: [email protected] Nature Plants | www.nature.com/natureplants ARTICLES NATURE PLANTS 70° W 68° W PERU 18° S 1 Tana norte 2 Tana sur 2 1 3 3 Tiliviche-1B 4 6 5 4 Mocha-2 8 20° S 7 11 5 Tarapacá-49 9 10 6 Pircas BOLIVIA 12 7 Tarapacá-13 8 Tarapacá-40 9 lluga túmulos 13 10 Caserones 11 Cerro colorado-7 PACIFIC OCEAN 14 12 Pica-8 13 Guatacondo-1 14 Quillagua—La capilla 22° S ATACAMA Elevation (m.a.s.l.) DESERT 0–1,000 1,000–2,000 2,000–3,000 3,000–4,000 4,000–5,000 5,000–6,000 6,000–7,000 24° S ARGENTINA 0 50 100 200 Kilometres 72° W 70° W 68° W Fig. 1 | Map of northern Chile. Archaeological site locations are indicated by numbers. m.a.s.l., metres above sea level. C3 plants, quinoa (Chenopodium quinoa), chilli pepper (Capsicum for the Late Intermediate and Late Periods (Fig. 2b), compared to sp.), gourd (Lagenaria sp.), squash (Cucurbita sp.), common beans the preceding Formative Period (Supplementary Table 3). One wild (Phaseolus vulgaris), lima beans (P. lunatus), cotton (Gossypium sp.) plant (Prosopis sp.) sample with exceptionally high δ15N (31.1‰) in and the wild legumes algarrobo (Prosopis sp.) and chañar (Geoffroea the Formative is a statistical outlier, and again may be intrusive due decorticans) from inland Tarapacá sites are shown in Fig. 2 and to postdepositional disturbance. Supplementary Table 2. Plants using C3 or C4 photosynthetic path- ways are clearly distinguished by their δ13C values. The δ15N values Seabird guano during pre-Hispanic times. The magnitude of the are uniformly high compared to most other parts of the world, but 15N-enrichment in plants observed here cannot be explained by by far the highest values occur in plants from the Late Intermediate invoking standard influences, such as low rainfall, or conventional Period onwards (Fig. 2). soil enrichment methods. Low rainfall (that is, the ‘aridity effect’) Formative Period crop δ15N values show a mean and standard cannot account for these high δ15N values. The highest observed deviation of 6.3 ± 4.0‰ (n = 70). We exclude on statistical grounds plant δ15N values in both modern and ancient natural Atacama eco- three clear outliers with very high values of 18.3‰, 19.5‰ (both systems are well below 12‰ (ranging from −2‰ to 12‰; mean squash) and 23.0‰ (maize). They may have been misattributed 5.9 ± 3.2‰)6,7, while soil δ15N values decrease below the threshold to the period due to postdepositional disturbance (Supplementary at which most biological activity ceases6. Similarly, high δ15N val- Information 1). A dramatic increase is observed with the Late ues cannot be the product of diagenesis as argued by DeNiro and Intermediate Period (20.2 ± 6.5‰, n = 83; P < 0.001, Kruskal–Wallis Hastorf8, who obtained high δ15N values for desiccated plants from test; Supplementary Table 3) (Fig. 2) that is maintained in the Late Peruvian coastal sites in contrast with charred highland specimens and Colonial Periods, which cannot be distinguished statistically yielding low values more consistent with the usual range for plants. (Supplementary Table 3). Wild fruits, algarrobo (Prosopis sp.) and Recent studies, however, dispute the diagenesis explanation9–11. chañar (G. decorticans), also show a marked increase in δ15N values For instance, no systematic differences were found in δ15N values Nature Plants | www.nature.com/natureplants NATURE PLANTS ARTICLES a b Crops 33 33 30 27 Species 24 30 ) 21 Amaranthus sp. ( 18 27 Capsicum sp. 15 AIR C. quinoa N 12 24 15 9 Curcubita sp. δ 6 21 G. decorticans 3 Gossypium sp. 0 –3 ) 18 Lagenaria sp. –6 ( P. lunatus 15 Formative Late Intermediate Late Period Colonial AIR P. vulgaris n = 75 Period n = 31 n = 13 N Prosopis sp. n = 83 15 12 δ Solanum sp. Wild plants 9 Z. mays 33 30 6 Period 27 24 3 Formative period ) 21 ( Late intermediate period 18 0 15 Late period AIR 12 N –3 Colonial period 15 9 δ 6 3 –6 0 –3 –25 –22 –19 –16 –13 –10 –6 13 Formative Late Intermediate Late Period δ CVPDB(‰) n = 13 Period n = 6 n = 7 Fig. 2 | Stable isotope results for carbon and nitrogen (calibrated in relation to the international standards VPDB and AIR) in archaeological crops and wild plants. a, Bivariate plot showing variation in δ13C and δ15N values for archaeological crops and wild fruits. Plant species are indicated by symbol and 13 13 cultural periods are indicated by colour.