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The legacy of 4,500 years of polyculture agroforestry in the eastern Amazon
- S. Yoshi Maezumi ORCID:orcid.org/0000-0002-4333-19721,
- Daiana Alves1,
- Mark Robinson1,
- Jonas Gregorio de Souza ORCID:orcid.org/0000-0001-6032-44431,
- Carolina Levis2,3,
- Robert L. Barnett4,
- Edemar Almeida de Oliveira5,
- Dunia Urrego ORCID:orcid.org/0000-0001-7938-55294,
- Denise Schaan6 &
- …
- José Iriarte ORCID:orcid.org/0000-0002-8155-53601
Nature Plantsvolume 4, pages540–547 (2018)Cite this article
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Abstract
The legacy of pre-Columbian land use in the Amazonian rainforest is one of the most controversial topics in the social1,2,3,4,5,6,7,8,9,10 and natural sciences11,12. Until now, the debate has been limited to discipline-specific studies, based purely on archaeological data8, modern vegetation13, modern ethnographic data3 or a limited integration of archaeological and palaeoecological data12. The lack of integrated studies to connect past land use with modern vegetation has left questions about the legacy of pre-Columbian land use on the modern vegetation composition in the Amazon, unanswered11. Here, we show that persistent anthropogenic landscapes for the past 4,500 years have had an enduring legacy on the hyperdominance of edible plants in modern forests in the eastern Amazon. We found an abrupt enrichment of edible plant species in fossil lake and terrestrial records associated with pre-Columbian occupation. Our results demonstrate that, through closed-canopy forest enrichment, limited clearing for crop cultivation and low-severity fire management, long-term food security was attained despite climate and social changes. Our results suggest that, in the eastern Amazon, the subsistence basis for the development of complex societies began ~4,500 years ago with the adoption of polyculture agroforestry, combining the cultivation of multiple annual crops with the progressive enrichment of edible forest species and the exploitation of aquatic resources. This subsistence strategy intensified with the later development of Amazonian dark earths, enabling the expansion of maize cultivation to the Belterra Plateau, providing a food production system that sustained growing human populations in the eastern Amazon. Furthermore, these millennial-scale polyculture agroforestry systems have an enduring legacy on the hyperdominance of edible plants in modern forests in the eastern Amazon. Together, our data provide a long-term example of past anthropogenic land use that can inform management and conservation efforts in modern Amazonian ecosystems.
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References
Clement, C. R.et al. The domestication of Amazonia before European conquest.Proc. Biol. Sci.282, 20150813 (2015).
Schaan, D. P.Sacred Geographies of Ancient Amazonia: Historical Ecology of Social Complexity (Left Coast Press, Walnut Creek, CA, 2012).
Balee, W.Cultural Forests of the Amazon. A Historical Ecology of People and Their Landscapes (Univ. Alabama Press, Tuscaloosa, AL, 2013).
Roberts, P., Hunt, C., Arroyo-Kalin, M., Evans, D. & Boivin, N. The deep human prehistory of global tropical forests and its relevance for modern conservation.Nat. Plants3, 17093 (2017).
de Souza, J. G. et al. Pre-Columbian earth-builders settled along the entire southern rim of the Amazon.Nat. Commun.9, 1125 (2018).
Iriarte, J. et al. Fire-free land use in pre-1492 Amazonian savannas.Proc. Natl Acad. Sci. USA109, 6473–6478 (2012).
Watling, J. et al. Impact of pre-Columbian ‘geoglyph’ builders on Amazonian forests.Proc. Natl Acad. Sci. USA114, 1868–1873 (2017).
Heckenberger, M. J. et al. Pre-Columbian urbanism, anthropogenic landscapes, and the future of the Amazon.Science321, 1214–1217 (2008).
Roosevelt, A. C. The Amazon and the Anthropocene: 13,000 years of human influence in a tropical rainforest.Anthropocene4, 69–87 (2013).
Erickson, C. L. inThe Handbook of South American Archaeology (eds Silverman, H. & Isbell, W. H.) 157–183 (Springer, New York, NY, 2008).
Barlow, J., Gardner, T. A., Lees, A. C., Parry, L. & Peres, C. A. How pristine are tropical forests? An ecological perspective on the pre-Columbian human footprint in Amazonia and implications for contemporary conservation.Biol. Conserv.151, 45–49 (2012).
McMichael, C. H. et al. Sparse pre-Columbian human habitation in western Amazonia.Science336, 1429–1431 (2012).
Levis, C. et al. Persistent effects of pre-Columbian plant domestication on Amazonian forest composition.Science355, 925–931 (2017).
McMichael, C. H., Feeley, K. J., Dick, C. W., Piperno, D. R. & Bush, M. B. Comment on “Persistent effects of pre-Columbian plant domestication on Amazonian forest composition”.Science358, eaan8347 (2017).
Junqueira, A. B. et al. Response to comment on “Persistent effects of pre-Columbian plant domestication on Amazonian forest composition”.Science358, eaan8837 (2017).
Mayle, F. E. & Iriarte, J. Integrated palaeoecology and archaeology—a powerful approach for understanding pre-Columbian Amazonia.J. Archaeol. Sci51, 54–64 (2014).
Carson, J. F. et al. Environmental impact of geometric earthwork construction in pre-Columbian Amazonia.Proc. Natl Acad. Sci. USA111, 10497–10502 (2014).
Whitney, B. S., Dickau, R., Mayle, F. E., Soto, J. D. & Iriarte, J. Pre-Columbian landscape impact and agriculture in the Monumental Mound region of the Llanos de Moxos, lowland Bolivia.Quat. Res.80, 207–217 (2013).
Maezumi, S. Y., Whitney, B. S., Mayle, F. E., Gregorio de Souza, J. & Iriarte, J. Reassessing climate and pre-Columbian drivers of paleofire activity in the Bolivian Amazon.Quat. Int.https://doi.org/10.1016/j.quaint.2017.11.053 (2017).
Willis, K. J., Gillson, L. & Brncic, T. M. How ‘virgin’ is virgin rainforest?Science304, 402–403 (2004).
Iriarte, J. inTropical Forest Conservation. Long-Term Processes of Human Evolution, Cultural Adaptations and Consumption Patterns (ed. Sanz, N.) 140–161 (UNESCO, Mexico City, 2017).
ter Steege, H. et al. Hyperdominance in the Amazonian tree flora.Science342, 1243092 (2013).
Heckenberger, M. & Neves, E. G. Amazonian archaeology.Annu. Rev. Anthropol.38, 251–266 (2009).
Woods, W. I. et al. (eds)Amazonian Dark Earths: Wim Sombroek’s Vision (Springer, Dordrecht, 2009).
Junqueira, A. B., Shepard, G. H. & Clement, C. R. Secondary forests on anthropogenic soils of the middle Madeira River: valuation, local knowledge, and landscape domestication in Brazilian Amazonia.Econ. Bot.65, 85–99 (2011).
Lins, J. et al. Pre-Columbian floristic legacies in modern homegardens of central Amazonia.PLoS ONE10, e0127067 (2015).
de Souza, N. B., Junqueira, A. B., Struik, P. C., Stomph, T. & Clement, C. R. The role of fertile anthropogenic soils in the conservation of native and exotic agrobiodiversity in Amazonian homegardens.Agroforest. Syst.https://doi.org/10.1007/s10457-017-0137-y (2017).
Wang, X. et al. Hydroclimate changes across the Amazon lowlands over the past 45,000 years.Nature541, 204–207 (2017).
Clement, C. R. 1492 and the loss of Amazonian crop genetic resources. II. Crop biogeography at contact.Econ. Bot.53, 203–216 (1999).
Hanelt, P., Büttner, R. & Mansfeld, R. (eds)Mansfeld’s Encyclopedia of Agricultural and Horticultural Crops (Except Ornamentals) (Springer, Berlin, 2001).
Denevan, W.Cultivated Landscapes of Native Amazonia and the Andes (Oxford Univ. Press, Oxford, 2001).
Chen, Y. et al. Forecasting fire season severity in South America using sea surface temperature anomalies.Science334, 787–791 (2011).
Heriarte, M. d.Descripção do Estado do Maranhão, Pará, Corupá e Rio das Amazonas (Impresa do Filho de Carlos Gerold, Vienna, 1874).
Bozarth, S., Price, K., Woods, W., Neves, E. & Rebellato, R. inAmazonian Dark Earths: Wim Sombroek’s Vision (eds Woods, W. I. et al.) 85–98 (Springer, Dordrecht, 2009).
Herrera, L. F., Cavelier, I., Rodriguez, C. & Mora, S. The technical transformation of an agricultural system in the Colombian Amazon.World Archaeol.24, 98–113 (1992).
Schmidt, M. J. & Heckenberger, M. J. inAmazonian Dark Earths: Wim Sombroek’s Vision (eds Woods, W. I. et al.) 163–190 (Springer, Dordrecht, 2009).
Hecht, S. B. inAmazonian Dark Earths: Origin, Properties, Management (eds Lehmann, J. et al.) 355–372 (Springer, Dordrecht, 2003).
Ford, A. & Nigh, R. Origins of the Maya Forest Garden: Maya resource management.J. Ethnobiol.29, 213–236 (2009).
Levis, C. et al. How people domesticated Amazonian forests.Front. Ecol. Evol.5, 171 (2018).
Willey, G. R. & Phillips, P.Method and Theory in American Archaeology (Univ. Chicago Press, Chicago, IL, 1958).
Arroyo-Kalin, M. The Amazonian Formative: crop domestication and anthropogenic soils.Diversity2, 473–504 (2010).
Heckenberger, M. J. inComparative Arawakan Histories: Rethinking Language Family and Culture Areain Amazonia (eds Hill, J. D. & Santos-Granero, F.) 99–122 (Univ. Illinois Press, Champaign, IL, 2002).
Neves, E. G. El Formativo que nunca terminó: la larga historia de estabilidad en las ocupaciones humanas de la Amazonía central.Boletîn Arqueol. PUCP11, 117–142 (2007).
Hermenegildo, T., O’Connell, T. C., Guapindaia, V. L. C. & Neves, E. G. New evidence for subsistence strategies of late pre-colonial societies of the mouth of the Amazon based on carbon and nitrogen isotopic data.Quat. Int.448, 139–149 (2017).
Roosevelt, A. C., Housley, R. A., Da Silveira, M. I., Maranca, S. & Johnson, R. Eighth millennium pottery from a prehistoric shell midden in the Brazilian Amazon.Science254, 1621–1624 (1991).
Roosevelt, A. C. San Jacinto I: an historical ecological approach to an archaic site in Colombia.HispanicAm. Hist. Rev.87, 738–740 (2007).
Roosevelt, A. C. inComplex Polities in the Ancient Tropical World (eds Bacus, E. A. & Lucero, L. J.) 13–33 (American Anthropological Association, Washington DC, 1999).
Nimuendajú, C. Os Tapajó.Bol. Museu Emílio Goeldi10, 93–106 (1948)
Gomes, D. M. C. Politics and ritual in large villages in Santarém, lower Amazon, Brazil.Camb. Archaeol. J.27, 275–293 (2017).
Schaan, D. P. inBeyond Waters: Archaeology and Environmental History of the Amazonian Inland (ed. Stenborg, P.) 23–36 (GOTARC, Gothenburg, 2016).
Mendes, A. C., Truckenbrod, W. & Nogueira, A. Faciological analysis of Alter do Chão formation (Cretaceous, Amazon basin), near the town of Óbidos, Pará, Brazil.Rev. Bras. Biocienc.52, 39–57 (2012).
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas.Int. J. Climatol.25, 1965–1978 (2005).
Veloso, H. P., Rangel-Filho, A. L. R. & Lima, J. C. A.Classificação da Vegetação Brasileira, Adaptada a um Sistema Universal (IBGE, 1991).
Sugita, S. Pollen representation of vegetation in quaternary sediments: theory and method in patchy vegetation.J. Ecol.82, 881–897 (1994).
Piperno, D. R.Phytoliths: A Comprehensive Guide for Archaeologists and Paleoecologists (Altamira Press, Lanham, MD, 2005).
Wright, H. E. A square-rod piston sampler for lake sediments.J. Sediment. Res.37, 975–976 (1967).
Blaauw, M., Christen, J. A., Mauquoy, D., van der Plicht, J. & Bennett, K. D. Testing the timing of radiocarbon-dated events between proxy archives.Holocene17, 283–288 (2007).
R Development Core Team.R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2014).
Appleby, P. G. inTracking Environmental Change using Lake Sediments: Basin Analysis, Coring and Chronological Techniques Vol. 1 (eds Last, W. M. & Smol, J. P.) 171–203 (Springer, Dordrech, 2001).
Flynn, W. W. The determination of low levels of polonium-210 in environmental materials.Anal. Chim. Acta43, 221–227 (1968).
Stuiver, M. & Polach, H. A. Discussion reporting of14C data.Radiocarbon19, 355–363 (1977).
Reimer, P. J. et al. IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years calbp.Radiocarbon55, 1869–1887 (2013).
Andrés, C. J. & Pérez, S. E. A new robust statistical model for radiocarbon data.Radiocarbon51, 1047–1059 (2009).
Blaauw, M. & Christen, J. A. Flexible paleoclimate age-depth models using an autoregressive gamma process.Bayesian Anal.6, 457–474 (2011).
Croudace, I. W., Rindby, A. & Rothwell, R. G. ITRAX: description and evaluation of a new multi-function X-ray core scanner.Geol. Soc. Spec. Publ.267, 51–63 (2006).
Nowaczyk, N. R. inTracking Environmental Change using Lake Sediments: Basin Analysis, Coring and Chronological Techniques Vol. 1 (eds Last, W. M. & Smol, J. P.) 155–170 (Springer, Dordrecht, 2001).
Reynolds, R., Belnap, J., Reheis, M., Lamothe, P. & Luiszer, F. Aeolian dust in Colorado Plateau soils: nutrient inputs and recent change in source.Proc. Natl. Acad. Sci. USA98, 7123–7127 (2001).
Dean, W. E. Jr Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: comparison with other methods.J. Sediment. Res.44, 242–248 (1974).
Whitlock, C. & Larsen, C. inTracking Environmental Change using Lake Sediments: Terrestrial, Algal, and Siliceous Indicators Vol. 3 (eds Smol, J. P. et al.) 75–97 (Springer, Dordrecht, 2001).
Rodionov, S. N. A sequential algorithm for testing climate regime shifts.Geophys. Res. Lett.31, L09204 (2004).
Rodionov, S. N. A sequential method for detecting regime shifts in the mean and variance. InLarge-Scale Disturbances (Regime Shifts) and Recovery in Aquatic Ecosystems: Challenges for Management Toward Sustainability, Proc. 2005 UNESCO-ROSTE/BAS Workshop on Regime Shifts (eds Velikova, V. & Chipev, N.) 68–72 (UNESCO, 2005).
Faegri, K. & Iversen, J.Textbook of Pollen Analysis (John Wiley and Sons, Chichester, 1989).
Whitney, B. S., Rushton, E. A., Carson, J. F., Iriarte, J. & Mayle, F. E. An improved methodology for the recovery ofZea mays and other large crop pollen, with implications for environmental archaeology in the Neotropics.Holocene22, 1087–1096 (2012).
Stockmarr, J. Tablets with spores used in absolute pollen analysis.Pollen Spores13, 615–621 (1971).
Holst, I., Moreno, J. E. & Piperno, D. R. Identification of teosinte, maize, andTripsacum in Mesoamerica by using pollen, starch grains, and phytoliths.Proc. Natl Acad. Sci. USA104, 17608–17613 (2007).
Burn, M. J. & Mayle, F. E. Palynological differentiation between genera of the Moraceae family and implications for Amazonian palaeoecology.Rev. Palaeobot. Palynol.149, 187–201 (2008).
Dickau, R. et al. Differentiation of neotropical ecosystems by modern soil phytolith assemblages and its implications for palaeoenvironmental and archaeological reconstructions.Rev. Palaeobot. Palynol.193, 15–37 (2013).
Watling, J. & Iriarte, J. Phytoliths from the coastal savannas of French Guiana.Quat. Int.287, 162–180 (2013).
Iriarte, J. et al. Late Holocene neotropical agricultural landscapes: phytolith and stable carbon isotope analysis of raised fields from French Guianan coastal savannahs.J. Archaeol. Sci.37, 2984–2994 (2010).
Piperno, D. R. Identifying crop plants with phytoliths (and starch grains) in Central and South America: a review and an update of the evidence.Quat. Int.193, 146–159 (2009).
Iriarte, J. Assessing the feasibility of identifying maize through the analysis of cross-shaped size and three-dimensional morphology of phytoliths in the grasslands of southeastern South America.J. Archaeol. Sci.30, 1085–1094 (2003).
Pearsall, D. M., Chandler-Ezell, K. & Chandler-Ezell, A. Identifying maize in neotropical sediments and soils using cob phytoliths.J. Archaeol. Sci.30, 611–627 (2003).
Piperno, D. R., Andres, T. C. & Stothert, K. E. Phytoliths inCucurbita and other neotropical Cucurbitaceae and their occurrence in early archaeological sites from the lowland American tropics.J. Archaeol. Sci.27, 193–208 (2000).
Travassos, D.Dark Earth Plant Management in the Lower Tapajós. PhD thesis, Univ. Exeter (2018).
Downey, S. S., Haas, W. R. & Shennan, S. J. European Neolithic societies showed early warning signals of population collapse.Proc. Natl Acad. Sci. USA113, 9751–9756 (2016).
Goldberg, A., Mychajliw, A. M. & Hadly, E. A. Post-invasion demography of prehistoric humans in South America.Nature532, 232–235 (2016).
Shenna, S. et al. Regional population collapse followed initial agriculture booms in mid-Holocene Europe.Nat. Commun.4, 2486 (2013).
Timpson, A. et al. Reconstructing regional population fluctuations in the European Neolithic using radiocarbon dates: a new case-study using an improved method.J. Archaeol. Sci.52, 549–557 (2014).
Zahid, H. J., Robinson, E. & Kelly, R. L. Agriculture, population growth, and statistical analysis of the radiocarbon record.Proc. Natl Acad. Sci. USA113, 931–935 (2016).
Ramsey, C. B. & Lee, S. Recent and planned developments of the program OxCal.Radiocarbon55, 720–730 (2013).
Alves, D. T.Ocupação Indígena na Foz do Rio Tapajós (1610 a.C.–1020 d.C.): Estudo do sítio Porto de Santarém (Novas Edições Acadêmicas, Saarbrücken, 2014).
Quinn, E. R.Excavating “Tapajó” Ceramics at Santarém: their Age and Archaeological Context. PhD thesis, Univ. Illinois at Chicago (2004).
Roosevelt, A. C. The development of prehistoric complex societies: Amazonia, a tropical forest.Archeol. Pap. Am. Anthropol. Assoc.9, 13–33 (1999).
National Register of Archaeological Sites (IPHAN, 2018).
WinklerPrins, A. M. G. A. & Aldrich, S. P. Locating Amazonian dark earths: creating an interactive GIS of known locations.J. Lat. Am. Geogr.9, 33–50 (2010).
Acknowledgements
Funding for this research was supported by the PAST (Pre-Columbian Amazon-Scale Transformations) European Research Council Consolidator Grant to J.I. (ERC_Cog 616179). Research was conducted under permit 01506.004836/2014-69 from the Instituto do Patrimônio Histórico e Artístico Nacional (IPHAN) and ICMBio permit 106/14-FNT. We thank all residents of the Maguarí and Jamaraquá community for their hospitality and help.
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Authors and Affiliations
Department of Archaeology, College of Humanities, University of Exeter, Exeter, UK
S. Yoshi Maezumi, Daiana Alves, Mark Robinson, Jonas Gregorio de Souza & José Iriarte
Programa de Pós-Graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil
Carolina Levis
Forest Ecology and Management Group, Wageningen University & Research, Wageningen, The Netherlands
Carolina Levis
Department of Geography, College of Life and Environmental Sciences, University of Exeter, Exeter, UK
Robert L. Barnett & Dunia Urrego
Universidade do Estado de Mato Grosso, Campus of Nova Xavantina, Mato Grosso State, Brazil
Edemar Almeida de Oliveira
Department of Anthropology, Federal University of Pará, Belém, Brazil
Denise Schaan
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- Carolina Levis
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- Edemar Almeida de Oliveira
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- Denise Schaan
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Contributions
J.I., S.Y.M. and D.S. designed the research. S.Y.M., J.I., D.A. and M.R. carried out the palaeoecological and archaeological fieldwork. E.A.d.O. carried out the botanical inventories. S.Y.M. carried out the pollen, charcoal, geochemistry and magnetic susceptibility analyses. D.A. carried out the analysis of the archaeological data. R.L.B. built the age-model chronology. J.G.d.S. compiled and analysed the archaeological radiocarbon dates. C.L. carried out the analysis of the modern vegetation and compiled the list of edible plants. S.Y.M. and J.I. led the writing of the paper with inputs from all other authors.
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Maezumi, S.Y., Alves, D., Robinson, M.et al. The legacy of 4,500 years of polyculture agroforestry in the eastern Amazon.Nature Plants4, 540–547 (2018). https://doi.org/10.1038/s41477-018-0205-y
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