Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

‘White gold’ guano fertilizer drove agricultural intensification in the Atacama Desert from ad 1000

Nature Plants volume 7, pages 152–158 (2021)Cite this article

Subjects

Abstract

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 considerable increase in the consumption of maize at the same time. We attribute the shift to extremely high δ15N values—the highest 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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
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.
Fig. 3: Modern, historical and archaeological images associated with seabird guano and crops.
Fig. 4: Boxplots showing variation in the isotope composition of carbon and nitrogen (calibrated in relation to the international standards VPDB and AIR) in different tissues from archaeological human samples from coastal, inland and Precordillera sites dating to the Formative, Middle, Late Intermediate and Late Periods.

Data availability

The authors declare that all data generated or analysed during this study are included in this published article (and its Supplementary Information files).

References

  1. Ugalde, P. C. et al. 13,000 years of sociocultural plant use in the Atacama Desert of northern Chile. Veget. Hist. Archaeobot. https://doi.org/10.1007/s00334-020-00783-1 (2020).

  2. Santoro, C. et al. Proyectos de irrigación y la fertilización del desierto. Estud. Atacameños. 16, 321–336 (1998).

    Google Scholar 

  3. Parcero-Oubiña, C. et al. Sistemas agrohidráulicos en el Loa Superior: el caso de Topaín. Boletín de. la Soc. Chil. de. Arqueología 46, 23–42 (2016).

    Google Scholar 

  4. Sandor, J. A. & Homburg, J. A. Anthropogenic soil change in ancient and traditional agricultural fields in arid to semiarid regions of the Americas. J. Ethnobiol. 37, 196–217 (2017).

    Article  Google Scholar 

  5. Segura, C., Vidal-Elgueta, A., Maldonado, A., Uribe, M. Soil use in pre-Hispanic and historical crop fields in the Guatacondo Ravine, northern Chile (2400 y bp): a geoarchaeological and paleobotanic approach. Preprint at Geoarchaeology https://doi.org/10.1002/gea.21833 (2020).

  6. Díaz, F. P., Frugone, M., Gutiérrez, R. A. & Latorre, C. Nitrogen cycling in an extreme hyperarid environment inferred from δ15N analyses of plants, soils and herbivore diet. Sci. Rep. 6, 22226 (2016).

    Article  Google Scholar 

  7. Evans, R. D. & Ehleringer, J. R. Plant δ15N values along a fog gradient in the Atacama desert, Chile. J. Arid Environ. 28, 189–193 (1994).

    Article  Google Scholar 

  8. DeNiro, M. J. & Hastorf, C. A. Alteration of 15N/14N and 13C/12C ratios of plant matter during the initial stages of diagenesis: studies utilizing archaeological specimens from Peru. Geochim. Cosmochim. Acta 49, 97–115 (1985).

    Article  CAS  Google Scholar 

  9. Metcalfe, J. Z. & Mead, J. I. Do uncharred plants preserve original carbon and nitrogen isotope compositions? J. Archaeol. Method Theory 26, 844–872 (2019).

    Article  Google Scholar 

  10. Szpak, P. & Chiou, K. L. A comparison of nitrogen isotope compositions of charred and desiccated botanical remains from northern Peru. Veg. Hist. Archaeobot 29, 527–538 (2019).

    Article  Google Scholar 

  11. Killian-Galván, V., Oliszewski, N., Olivera, D. E. and Panarello, H. O. in Physical, Chemical and Biological Markers in Argentine Archaeology: Theory, Methods, and Applications (eds Kligmann, D. & Morales, M.) 39–51 (BAR International Series, Archaeopress, 2014).

  12. Bogaard, A., Heaton, T. H. E., Poulton, P. & Merbach, I. The impact of manuring on nitrogen isotope ratios in cereals: archaeological implications for reconstruction of diet and crop management practices. J. Archaeol. Sci. 34, 335–343 (2007).

    Article  Google Scholar 

  13. Bogaard, A. et al. Crop manuring and intensive land management by Europe’s first farmers. Proc. Natl Acad. Sci. USA 110, 12589–12594 (2013).

    Article  CAS  Google Scholar 

  14. Szpak, P., Longstaffe, F. J., Millaire, J. F. & White, C. D. Stable isotope biogeochemistry of seabird guano fertilization: results from growth chamber studies with maize (Zea mays). PLoS ONE 7, e33741 (2012).

    Article  CAS  Google Scholar 

  15. Szpak, P., Millaire, J.-F., White, C. D. & Longstaffe, F. J. Influence of seabird guano and camelid dung fertilization on the nitrogen isotopic composition of field-grown maize (Zea mays). J. Archaeol. Sci. 39, 3721–3740 (2012).

    Article  CAS  Google Scholar 

  16. Frezier, A. A Voyage to the South-Sea and Along the Coasts of Chili and Peru, In the Years 1712, 1713, and 1714 (Jonah Bowyer, 1717).

  17. Cieza de León, P. de. La Crónica del Perú (Lima, Pontificia Univ. Católica del Perú, 1984 [1553]).

  18. De la Vega, G. Los Comentarios Reales de los Incas Vol. 1 (Sanmartí, 1919 [1609]).

  19. de San Miguel, G. D. Visita hecha a la Provincia de Chucuito por Garci Diez de San Miguel en el año 1567 (ed. Soriano, W. E. Lima) (Casa de la Cultura del Perú, 1964 [1567]).

  20. de Bibar, G. Crónica y Relación Copiosa y Verdadera de los Reinos de Chile. Colección de Escritores Coloniales (Editorial Universitaria, 1979 [1558]).

  21. Sánchez, T. & Méndez-Quirós, P. El Ciclo del Guano en el Litoral del Tarapacá (Consejo Nacional de la Cultura y las Artes, 2011).

  22. Mizutani, H. & Wada, E. Nitrogen and carbon isotope ratios in seabird rookeries and their ecological implications. Ecology 69, 340–349 (1988).

    Article  Google Scholar 

  23. Cocks, M. P., Balfour, D. A. & Stock, W. D. On the uptake of ornithogenic products by plants on the inland mountains of Dronning Maud Land, Antarctica, using stable isotopes. Polar Biol. 20, 107–111 (1998).

    Article  Google Scholar 

  24. Lucassen, F. et al. The stable isotope composition of nitrogen and carbon and elemental contents in modern and fossil seabird guano from Northern Chile—Marine sources and diagenetic effects. PLoS ONE 12, e0179440 (2017).

    Article  Google Scholar 

  25. McRostie, V. B., Gayo, E. M., Santoro, C. M., De Pol-Holz, R. & Latorre, C. The pre-Columbian introduction and dispersal of Algarrobo (Prosopis, section Algarobia) in the Atacama desert of northern Chile. PLoS ONE 12, e0181759 (2017).

    Article  Google Scholar 

  26. Szpak, P., Longstaffe, F. J., Millaire, J.-F. & White, C. D. Large variation in nitrogen isotopic composition of a fertilized legume. J. Archaeol. Sci. 45, 72–79 (2014).

    Article  CAS  Google Scholar 

  27. Latcham, R. E. La Agricultura Precolombiana en Chile y los Países Vecinos (Univ. Chile, 1936).

  28. Michalski, G., Kolanowski, M. & Riha, K. M. Oxygen and nitrogen isotopic composition of nitrate in commercial fertilizers, nitric acid, and reagent salts. Isotopes Environ. Health Stud. 51, 382–391 (2015).

    Article  CAS  Google Scholar 

  29. Böhlke, J. K., Ericksen, G. E. & Revesz, K. Stable isotope evidence for an atmospheric origin of desert nitrate deposits in northern Chile and Southern California, USA. Chem. Geol. 136, 135–152 (1997).

    Article  Google Scholar 

  30. Julien, C. in Andean Ecology and Civilization: An Interdisciplinary Perspective on Andean Ecological Complementarity (eds Masuda, S., Shimada, I. & Morris, C.) 185–231 (Univ. Tokyo Press, 1985).

  31. Rodrigues, P. & Micael, J. The importance of guano birds to the Inca Empire and first conservation measures implemented by humans. IBIS https://doi.org/10.1111/ibi.12867 (2020).

  32. Murra, J. V. La Organización Económica del Estado Inca (Siglo XXI, 1978).

  33. Rostworowski, M. Recursos Naturales Renovables y Pesca, Siglos XVI-XVII: Curacas y Sucesiones, Costa Norte (Instituto de Estudios Peruanos, 2005).

  34. Lee-Thorp, J. A., Sealy, J. C. & van der Merwe, N. J. Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. J. Archaeol. Sci. 16, 585–599 (1989).

    Article  Google Scholar 

  35. Santana-Sagredo, F., Lee-Thorp, J. A., Schulting, R. & Uribe, M. Isotopic evidence for divergent diets and mobility patterns in the Atacama Desert, Northern Chile, during the late intermediate period (AD 900–1450). Am. J. Phys. Anthropol. 156, 374–387 (2015).

    Article  Google Scholar 

  36. Núñez, L. Tráfico de Complementariedad de Recursos entre las Tierras Altas y el Pacífico en el área Centro sur Andina. Doctoral thesis, Univ. Tokyo (1984).

  37. García, M. & Uribe, M. Contextos de uso de las plantas vinculadas al Complejo Pica Tarapacá, Andes Centro-Sur: Arqueobotánica y agricultura en el período Intermedio Tardío (ca. 1250-1450 DC). Estudios Atacameños. 44, 107–122 (2012).

    Article  Google Scholar 

  38. Mandakovic, V. Historias de Plantas: Curso bajo de la Quebrada de Tarapacá entre los periodos Formativo e Intermedio Tardío. Los poblados Pircas y Caserones (400 AC-1000 DC). Undergraduate thesis, Univ. Chile (2017).

  39. De Souza Herreros, P., Méndez-Quiros Aranda, P., Catalán Contreras, D. G., Carrasco González, C. A. & Baeza de la Fuente, V. E. Aleros ceremoniales del período Formativo en las tierras altas del desierto de Atacama (región de Tarapacá, norte de Chile). Ñawpa Pacha 37, 63–86 (2017).

    Article  Google Scholar 

  40. Santana-Sagredo, F. et al. Paired radiocarbon dating on human samples and camelid fibres and textiles from northern Chile: the case of Pica 8 (Tarapacá). Radiocarbon 59, 1195–1213 (2017).

    Article  CAS  Google Scholar 

  41. Pestle, W. J., Torres-Rouff, C., Gallardo, F., Ballester, B. & Clarot, A. Mobility and exchange among marine hunter-gatherer and agropastoralist communities in the formative period atacama desert. Curr. Anthropol. 56, 121–133 (2015).

    Article  Google Scholar 

  42. Alfonso-Durruty, M. P. et al. Dietary diversity in the Atacama desert during the Late intermediate period of northern Chile. Quat. Sci. Rev. 214, 54–67 (2019).

    Article  Google Scholar 

  43. Hastorf, C. A. Agriculture and the Onset of Political Inequality Before the Inka (CUP Archive, 1993).

  44. Dietler, M. & Hayden, B. Feasts: Archaeological and Ethnographic Perspectives on Food. Politics, and Power (Smithsonian Institution, 2001).

  45. Zori, C. & Brant, E. Managing the risk of climatic variability in late prehistoric northern Chile. J. Anthropol. Archaeol. 31, 403–421 (2012).

    Article  Google Scholar 

  46. Pinder, D. M., Gallardo, F., Cabello, G., Torres-Rouff, C. & Pestle, W. J. An isotopic study of dietary diversity in formative period Ancachi/Quillagua, Atacama Desert, northern Chile. Am. J. Phys. Anthropol. 170, 613–621 (2019).

    Article  Google Scholar 

  47. Poulson, S.P. et al. Paleodiet in northern Chile through the Holocene: extremely heavy δ15N values in dental calculus suggest a guano-derived signature? J. Archaeol. Sci. 40, 4756–4585 (2013).

    Article  Google Scholar 

  48. Schnug, E., Jacobs, F. and Stöven, K. in Seabirds (ed. Mikkola, H.) 79–100 (InTech, 2018).

  49. Vaiglova, P. et al. An integrated stable isotope study of plants and animals from Kouphovouno, southern Greece: a new look at Neolithic farming. J. Archaeol. Sci. 42, 201–215 (2014).

    Article  CAS  Google Scholar 

  50. Coplen, T. B. et al. New guidelines for δ13C measurements. Anal. Chem. 78, 2439–2441 (2006).

    Article  CAS  Google Scholar 

  51. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020); https://www.R-project.org/

  52. Leys, C., Ley, C., Klein, O., Bernard, P. & Licata, L. Detecting outliers: do not use standard deviation around the mean, use absolute deviation around the median. J. Exp. Soc. Psychol. 49, 764–766 (2013).

    Article  Google Scholar 

  53. Brock, F., Higham, T., Ditchfield, P. & Ramsey, C. B. Current pretreatment methods for ams radiocarbon dating at the Oxford radiocarbon accelerator Unit (Orau). Radiocarbon 52, 103–112 (2010).

    Article  CAS  Google Scholar 

  54. Hogg, A. G. et al. SHCal13 southern hemisphere calibration, 0–50,000 years cal BP. Radiocarbon 55, 1889–1903 (2013).

    Article  CAS  Google Scholar 

  55. Ramsey, C. B. & Lee, S. Recent and planned developments of the program OxCal. Radiocarbon 55, 720–730 (2013).

    Article  CAS  Google Scholar 

  56. Santana-Sagredo, F. From the Andes to the Coast: Human Mobility and Diet in the Atacama Desert during the Late Intermediate Period (AD 900–1450). Doctoral thesis, Univ. Oxford (2016).

  57. Fernández-Crespo, T., Czermak, A., Lee-Thorp, J. A. & Schulting, R. J. Infant and childhood diet at the passage tomb of Alto de la huesera (north-central Iberia) from bone collagen and sequential dentine isotope composition. Int. J. Osteoarchaeol. 28, 542–551 (2018).

    Article  Google Scholar 

  58. Ambrose, S. H. & Norr, L. in Prehistoric Human Bone: Archaeology at the Molecular Level (eds Lambert, J. B. & Grupe, G.) 1–37 (Springer, 1993).

Download references

Acknowledgements

We thank the National Geographic Society for Early Career grant nos. EC-53250R-18, FONDECYT 3180317, 1181829 and 1191452 and the Becas Chile-PhD Scholarship for funding support. C.H. is supported by Nucleo Milenio INVASAL funded by Chile’s government programme, Iniciativa Científica Milenio from the Ministerio de Ministerio de Ciencia, Tecnología, Conocimiento e Innovación. C.L. acknowledges support from grant no. ANID PIA CCTE AFB170008 and Nucleo Milenio UPWELL. We are grateful to P. Ditchfield, T. Higham, D. Chival, J. Cameron and F. Docmac for their help in the laboratory. We thank S. Santana-Sagredo for helping and improving the figures of this article. We are also grateful to the institutions that allowed us sampling their archaeological collections. All samples were analysed at the University of Oxford under Chilean government permit (no. 42.649, CVE 1757327, Diario Oficial de la República de Chile).

Author information

Author notes

  1. Francisca Santana-Sagredo

    Present address: Escuela de Antropología, Pontificia Universidad Católica de Chile, Santiago, Chile, Santiago, Chile

Authors and Affiliations

  1. Escuela de Antropología, Pontificia Universidad Católica de Chile, Santiago, Chile

    Francisca Santana-Sagredo & Virginia B. McRostie

  2. Universidad de Antofagasta Stable Isotope Facility, Instituto Antofagasta, Universidad de Antofagasta, Angamos, Antofagasta, Chile

    Francisca Santana-Sagredo & Chris Harrod

  3. School of Archaeology, University of Oxford, Oxford, UK

    Francisca Santana-Sagredo, Rick J. Schulting & Julia Lee-Thorp

  4. Departamento de Prehistoria, Programa de Doctorado en Arqueología Prehistórica, Universidad Autónoma de Barcelona, Barcelona, Spain

    Pablo Méndez-Quiros

  5. Programa de Doctorado en Biología, mención Ecología, Pontificia Universidad Católica de Chile, Santiago, Chile

    Ale Vidal-Elgueta

  6. Departamento de Antropología, Universidad de Chile, Santiago, Chile

    Mauricio Uribe & Anahí Maturana-Fernández

  7. Instituto de Arqueología y Antropología (IIA), Universidad Católica del Norte (UCN), San Pedro de Atacama, Chile

    Rodrigo Loyola

  8. UMR 7055 Prehistoire et Technologie (PreTéch), Université Paris Ouest Nanterre La, Défense, France

    Rodrigo Loyola

  9. Departamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago, Chile

    Francisca P. Díaz

  10. Centro del Desierto de Atacama, Pontificia Universidad Católica de Chile, Santiago, Chile

    Claudio Latorre & Virginia B. McRostie

  11. Departamento de Ecología, Pontificia Universidad Católica de Chile, Santiago, Chile

    Claudio Latorre

  12. Institute of Ecology and Biodiversity, Pontificia Universidad Católica de Chile, Santiago, Chile

    Claudio Latorre

  13. Instituto de Alta Investigación, Universidad de Tarapacá, Arica, Chile

    Calogero M. Santoro

  14. Programa de Magíster en Antropología, Departamento de Antropología, Universidad de Tarapacá, Arica, Chile

    Valentina Mandakovic

  15. Núcleo Milenio INVASAL, Concepción, Chile

    Chris Harrod

  16. Instituto de Ciencias Naturales Alexander von Humboldt, Universidad de Antofagasta, Antofagasta, Chile

    Chris Harrod

Authors
  1. Francisca Santana-Sagredo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rick J. Schulting
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pablo Méndez-Quiros
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ale Vidal-Elgueta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mauricio Uribe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rodrigo Loyola
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anahí Maturana-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Francisca P. Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudio Latorre
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Virginia B. McRostie
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Calogero M. Santoro
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Valentina Mandakovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Chris Harrod
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Julia Lee-Thorp
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.S.-S., R.J.S. and J.L.-T. came up with the original idea and research design. F.S.-S., P.M.-Q., A.V.-E., M.U., R.L. and A.M.-F. conducted and participated in the fieldwork. F.S.-S., A.V.-E. and A.M.-F. carried out sampling in universities and museum collections. A.V.-E., V.B.M., V.M. and F.P.D. undertook taxonomic analysis of crops and wild fruits. F.S.-S. and A.M.-F. conducted sample processing and laboratory work. F.S.-S and P.M.-Q collected information and worked on the human isotope and radiocarbon dates databases. F.S.-S., R.J.S. and C.H. undertook the statistical analysis. R.L. designed the map. F.S.-S., J.L.-T., R.J.S. and C.H. interpreted the results. C.L. and C.M.S. contributed to interpreting the data based on the local ecology and archaeology. F.S.-S. wrote the paper with the help of R.J.S. and J.L.-T. All the authors commented on the paper.

Corresponding author

Correspondence to Francisca Santana-Sagredo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Jonathan Sandor and the other, anonymous, reviewers for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Information 1–4.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–5.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santana-Sagredo, F., Schulting, R.J., Méndez-Quiros, P. et al. ‘White gold’ guano fertilizer drove agricultural intensification in the Atacama Desert from ad 1000. Nat. Plants 7, 152–158 (2021). https://doi.org/10.1038/s41477-020-00835-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-020-00835-4

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing