Source: https://pinpdf.com/persistent-effects-of-pre-columbian-plant-domestication-on-amazonian-.html
Timestamp: 2019-04-25 22:02:36+00:00

Document:
COPYRIGHT AND REUSE Open Research Exeter makes this work available in accordance with publisher policies.
Citation: Levis, C., F. R. Costa, F. Bongers, M. Pena-Claros, C. R. Clement, A. B. Junqueira, E. G. Neves, E. K. Tamanaha, F. O. Figueiredo, R. P. Salomao, C. V. Castilho, W. E. Magnusson, O. L. Phillips, J. E. Guevara, D. Sabatier, J. F. Molino, D. C. Lopez, A. M. Mendoza, N. C. Pitman, A. Duque, P. N. Vargas, C. E. Zartman, R. Vasquez, A. Andrade, J. L. Camargo, T. R. Feldpausch, S. G. Laurance, W. F. Laurance, T. J. Killeen, H. E. Nascimento, J. C. Montero, B. Mostacedo, I. L. Amaral, I. C. Guimaraes Vieira, R. Brienen, H. Castellanos, J. Terborgh, M. J. Carim, J. R. Guimaraes, L. S. Coelho, F. D. Matos, F. Wittmann, H. F. Mogollon, G. Damasco, N. Davila, R. Garcia-Villacorta, E. N. Coronado, T. Emilio, D. A. Filho, J. Schietti, P. Souza, N. Targhetta, J. A. Comiskey, B. S. Marimon, B. H. Marimon, Jr., D. Neill, A. Alonso, L. Arroyo, F. A. Carvalho, F. C. de Souza, F. Dallmeier, M. P. Pansonato, J. F. Duivenvoorden, P. V. Fine, P. R. Stevenson, A. Araujo-Murakami, C. G. Aymard, C. Baraloto, D. D. do Amaral, J. Engel, T. W. Henkel, P. Maas, P. Petronelli, J. D. Revilla, J. Stropp, D. Daly, R. Gribel, M. R. Paredes, M. Silveira, R. Thomas-Caesar, T. R. Baker, N. F. da Silva, L. V. Ferreira, C. A. Peres, M. R. Silman, C. Ceron, F. C. Valverde, A. Di Fiore, E. M. Jimenez, M. C. Mora, M. Toledo, E. M. Barbosa, L. C. Bonates, N. C. Arboleda, E. S. Farias, A. Fuentes, J. L. Guillaumet, P. M. Jorgensen, Y. Malhi, I. P. de Andrade Miranda, J. F. Phillips, A. Prieto, A. Rudas, A. R. Ruschel, N. Silva, P. von Hildebrand, V. A. Vos, E. L. Zent, S. Zent, B. B. Cintra, M. T. Nascimento, A. A. Oliveira, H. Ramirez-Angulo, J. F. Ramos, G. Rivas, J. Schongart, R. Sierra, M. Tirado, G. van der Heijden, E. V. Torre, O. Wang, K. R. Young, C. Baider, A. Cano, W. Farfan-Rios, C. Ferreira, B. Hoffman, C. Mendoza, I. Mesones, A. Torres-Lezama, M. N. Medina, T. R. van Andel, D. Villarroel, R. Zagt, M. N. Alexiades, H. Balslev, K. Garcia-Cabrera, T. Gonzales, L. Hernandez, I. Huamantupa-Chuquimaco, A. G. Manzatto, W. Milliken, W. P. Cuenca, S. Pansini, D. Pauletto, F. R. Arevalo, N. F. Reis, A. F. Sampaio, L. E. Giraldo, E. H. Sandoval, L. V. Gamarra, C. I. Vela and H. Ter Steege (2017). "Persistent effects of pre-Columbian plant domestication on Amazonian forest composition." Science 355(6328): 925-931.
Abstract: The extent to which pre-Columbian societies altered Amazonian landscapes is hotly debated. We performed a basin-wide analysis of pre-Columbian impacts on Amazonian forests by overlaying known archaeological sites in Amazonia with the distributions and abundances of 85 woody species domesticated by pre-Columbian peoples. Domesticated species are five times more likely to be hyperdominant than non-domesticated species. Across the basin the relative abundance and richness of domesticated species increases in forests on and around archaeological sites. In southwestern and eastern Amazonia distance to archaeological sites strongly influences the relative abundance and richness of domesticated species. Our analyses indicate that modern tree communities in Amazonia are structured to an important extent by a long history of plant domestication by Amazonian peoples.
eventually accumulated greater intra-specific diversity (13). Our results suggest that plant species that responded well to selection and propagation were widely cultivated and dispersed within and outside their natural range (6, 7) by different societies and at different moments in time. The influence of modern indigenous and non-indigenous societies in the last 300 years on the distribution of some domesticated species may be stronger than the effect of earlier societies. For instance, in the late 17th century, Portugal and Spain stimulated plantations of cocoa trees in Amazonia (40), which - associated with pre-Columbian cultivation - may have increased the abundance of cocoa trees in south-western Amazonian forests even more. Our results suggest that past human interventions had an important and lasting role in the distribution of domesticated species found in modern forests, despite the fact that the location of many archaeological sites is unknown. Almost one fourth of all domesticated species are hyperdominant, and besides their socio-economic importance they can also help unravel the human history of Amazonian forests, largely overlooked by ecological studies. Detecting the widespread effect of ancient societies in modern forests not only strengthens efforts to conserve domesticated and useful wild-plant populations, of critical importance for modern food security (41), but also strongly refutes ideas of Amazonian forests being untouched by man. Domestication shapes Amazonian forests. References and Notes: 1. C. R. Clement et al., The domestication of Amazonia before European conquest. Proc. R. Soc. Lond., B, Biol., Sci. 282, 20150813 (2015). 2. M. B. Bush et al., Anthropogenic influence on Amazonian forests in pre-history: An ecological perspective. J. Biogeogr. 42, 2277-2288 (2015). 3. C. H. McMichael et al., Sparse pre-Columbian human habitation in western Amazonia. Science 336, 1429–1431 (2012).
4. P. W. Stahl, Interpreting interfluvial landscape transformations in the pre-Columbian Amazon. Holocene 20, 1598-1603 (2015). 5. D. R. Piperno, C. H. McMichael, M. B. Bush, Amazonia and the Anthropocene: What was the spatial extent and intensity of human landscape modification in the Amazon Basin at the end of prehistory? Holocene 25, 1588-1597 (2015). 6. C. R. Clement, 1492 and the loss of Amazonian crop genetic resources. I. The relation between domestication and human population decline. Econ. Bot. 53, 188-202 (1999). 7. N. L. Boivin et al., Ecological consequences of human niche construction: Examining longterm anthropogenic shaping of global species distributions. Proc. Natl Acad. Sci. USA 113, 6388- 6396 (2016). 8. D. Rindos, The Origins of Agriculture: An Evolutionary Perspective, (Academic Press, 1984), pp. 154-158. 9. J. Kennedy, Agricultural systems in the tropical forest: a critique framed by tree crops of Papua New Guinea. Quat. Int. 249, 140-150 (2012). 10. C. Darwin, On the origin of species, (John Murray, London, 1859), p. 37. 11. D. Zohary, Unconscious selection and the evolution of domesticated plants. Econ. Bot. 58, 510 (2004). 12. M. D. Purugganan, D. Q. Fuller, The nature of selection during plant domestication. Nature 457, 843-848 (2009). 13. C .R. Clement, M. de Cristo-Araújo, G. Coppens D’Eeckenbrugge, A. Alves Pereira, D. Picanço-Rodrigues, Origin and domestication of native Amazonian crops. Diversity 2, 72-106 (2010). 14. B. D. O'Fallon, L. Fehren-Schmitz, Native Americans experienced a strong population bottleneck coincident with European contact. Proc. Natl Acad. Sci. USA 108, 20444-20448 (2011).
15. A. B. Junqueira, G. H. Shepard Jr, C. R. Clement, Secondary forests on anthropogenic soils in Brazilian Amazon conserve agrobiodiversity. Biodivers. Conserv. 19, 1933-1961 (2010). 16. C. L. Erickson, W. Balée, in Time and Complexity in Historical Ecology, W. Balee, C. L. Erickson, Eds. (Columbia Univ. Press, New York, 2006), pp. 187–233. 17. H. ter Steege et al., Hyperdominance in the Amazonian tree flora. Science 342, 1243092 (2013). 18. C. Hoorn et al., Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927-931 (2010). 19. H. ter Steege et al., Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443, 444-447 (2006). 20. C. A. Peres, T. Emilio, J. Schietti, S. J. Desmoulière, T. Levi, Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proc. Natl Acad. Sci. USA 113, 892-897 (2016). 21. A. Esquivel-Muelbert et al., Seasonal drought limits tree species across the Neotropics. Ecography 39, 001-012 (2016). 22. M. B. Bush, C. H. McMichael, Holocene variability of an Amazonian hyperdominant. J. Ecol. 104, 1370-1378 (2016). 23. J. Schietti et al., Vertical distance from drainage drives floristic composition changes in an Amazonian rainforest. Plant Ecol. Divers. 7, 241-253 (2014). 24. Materials and methods as well as supplementary text are available as supplementary materials, see Science Online. 25. U. Lombardo, E. Canal-Beeby, H. Veit, Eco-archaeological regions in the Bolivian Amazon. Geog. Helv. 66, 173-182 (2011) 26. C. H. McMichael et al., Predicting pre-Columbian anthropogenic soils in Amazonia. Proc. R. Soc. Lond., B, Biol. Sci. 281, 20132475 (2014).
27. C. Levis et al., “What do we know about the distribution of Amazonian Dark Earth along tributary rivers in Central Amazonia?” in Antes de Orellana - Actas del 3er Encuentro Internacional de Arqueología Amazónica (IFEA, Perú, ed. 1, 2014), pp. 305-312. 28. D. R. Piperno, The origins of plant cultivation and domestication in the New World Tropics: patterns, process, and new developments. Curr. Anthropol. S4, 453-470 (2011). 29. A. C. Roosevelt, The Amazon and the Anthropocene: 13,000 years of human influence in a tropical rainforest. Anthropocene 4, 69-87 (2013). 30. Arroyo-Kalin, M. Slash-burn-and-churn: Landscape history and crop cultivation in preColumbian Amazonia. Quat. Int. 249, 4-18 (2012). 31. E. G. Neves, J. B. Petersen, R. N. Bartone, C. A. da Silva, in Amazonian Dark Earths, J. Lehmann, D.C. Kern, B. Glaser, W.I. Woods, Eds. (Springer, 2003), pp. 29-50. 32. R. S. Walker, L. A. Ribeiro, Bayesian phylogeography of the Arawak expansion in lowland South America. Proc. R. Soc. Lond., B, Biol. Sci. 278, 2562-2567 (2015). 33. E. J. M. dos Santos, A. L. S. da Silva, P. D. Ewerton, L. Y. Takeshita, M. H. T. Maia, Origins and demographic dynamics of Tupí expansion: a genetic tale. Bol. Mus. Para. Goeldi. Ciências Humanas 10, 217-228 (2015). 34. F. E. Mayle, M. J. Power, Impact of a drier Early–Mid-Holocene climate upon Amazonian forests. Proc. R. Soc. Lond., B, Biol. Sci. 363, 1829-1838 (2008). 35. M. Crevels, H. der Voort, in From Linguistic Areas to Areal Linguistics, P. Muysken, Ed. (John Benjamins Press, 2008), pp. 151–179. 36. C. A. Quesada et al., Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9, 2203–2246 (2012). 37. T. Emilio et al., Soil physical conditions limit palm and tree basal area in Amazonian forests. Plant Ecol. Divers. 7, 215-229 (2014). 38. C. H. McMichael et al., Phytolith assemblages along a gradient of ancient human disturbance in Western Amazonia. Front. Ecol. Evol. 3, 141 (2015).
39. E. Thomas et al., Present spatial diversity patterns of Theobroma cacao L. in the neotropics reflect genetic differentiation in Pleistocene refugia followed by human-influenced dispersal. PLoS One 7, e47676 (2012), doi:10.1371/journal.pone.0047676. 40. D. Alden, The significance of cacao production in the Amazon region during the late colonial period: An essay in comparative economic history. Proc. Am. Philos. Soc. 120, 103-135 (1976). 41. J. Esquinas-Alcázar, Protecting crop genetic diversity for food security: political, ethical and technical challenges. Nat. Rev. Genet. 6, 946-953 (2005). 42. E. Thomas, C. Alcázar-Caicedo, C. H. McMichael, R. Corvera, J. Loo, Uncovering spatial patterns in the natural and human history of Brazil nut (Bertholletia excelsa) across the Amazon Basin. J. Biogeogr. 42, 1367-1382 (2015). 43. B. Lehner, K. Verdin, A. Jarvis, New global hydrography derived from spaceborne elevation data. Eos, Trans. Amer. Geophys. 89, 93-94 (2008). 44. BRASIL, “Manual de Construção da Base Hidrográfica Ortocodificada” (Brasília, ANA, SGI, 2007); available online at www.ana.gov.br. 45. E. J. Fittkau, Esboço de uma divisão ecológica da região amazônica. Proc. Symp. Biol. Trop. Amaz., 363–372 (1971). 46. T. Hengl et al., SoilGrids1km-Global Soil Information based on automated mapping. PLoS One 9, e105992 (2013). doi: info:doi/10.1371/journal.pone.0114788. 47. C. Kummerow, W. Barnes, T. Kozu, J. Shiue, J. Simpson, The Tropical Rainfall Measuring Mission (TRMM) sensor package. J. Atmos. Ocean Tech. 15, 809–817 (1998). 48. A. Nobre et al., Height above the nearest drainage - a hydrologically relevant new terrain model. J. Hydrol. 404, 13-29 (2011). 49. P. Perrut de Lima, “Caracterização da variabilidade genética, sistema de cruzamento e parâmetros de germinação e emergência de Euterpe precatoria Martius em populações do baixo rio Solimões” thesis, Instituto National de Pesquisas da Amazônia, Manaus, AM, Brazil (2014).
50. M. Smith, C. Fausto, Socialidade e diversidade de pequis (Caryocar brasiliense, Caryocaraceae) entre os Kuikuro do alto rio Xingu (Brasil). Bol. Mus. Para. Emílio Goeldi. Cienc. Hum. 11, 87-113 (2016). 51. P. A. Moreira, J. Lins, G. Dequigiovanni, E. A. Veasey, C. R. Clement, The domestication of Annatto (Bixa orellana) from Bixa urucurana in Amazonia. Econ. Bot. 69, 127-135 (2015). 52. J. Sosnowska, A. Walanus, H. Balslev, Asháninka palm management and domestication in the Peruvian Amazon. Hum. Ecol. 43, 1-16 (2015). 53. N. García et al., Management of the palm Astrocaryum chambira Burret (Arecaceae) in northwest Amazon. Acta Bot. Bras. 29, 45-57 (2015). 54. P. Hanelt, R. Büttner, R. Mansfeld, Mansfeld's Encyclopedia of Agricultural and Horticultural Crops: Except Ornamentals, (Berlin, Springer, 2001); available online at http://mansfeld.ipk-gatersleben.de/. 55. H. Dempewolf, L. H. Rieseberg, Q. C. Cronk, Crop domestication in the Compositae: a family-wide trait assessment. Genet. Resour. Crop Ev. 55, 1141-1157 (2008). 56. K. Hammer, K. Khoshbakht, A domestication assessment of the big five plant families. Genet. Resour. Crop Ev. 62, 665–689 (2015). 57. B. Boyle et al., The taxonomic name resolution service: an online tool for automated standardization of plant names. BMC Bioinformatics 16, (2013). doi:10.1186/1471-2105-14-16. 58. R Development Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2012); available online at www.Rproject.org. 59. C. Levis et al., Historical human footprint on modern tree species composition in the PurusMadeira interfluve, central Amazonia. PLoS One 7, e48559 (2012). doi:10.1371/journal.pone.0048559.
60. J. Pinheiro, D. Bates, S. DebRoy, D. Sarkar, R Core Team, nlme: Linear and Nonlinear Mixed Effects Models. (Comprehensive R Archive Network, 2016); available online at http://cran.r-project.org/package=nlme. 61. D. Lüdecke, sjPlot: Data Visualization for Statistics in Social Science. (The Comprehensive R Archive Network, 2016); available online at https://cran.r-project.org/package=sjPlot 62. P. Breheny, W. Burchett, Visualization of Regression Models Using visreg. (Comprehensive R Archive Network, 2013); available online at https://cran.rproject.org/web/packages/visreg/index.html 63. P. Legendre, Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. J. Plant Ecol. 1, 3-8 (2008). 64. J. Oksanen et al., ‘vegan’: Community ecology package. (The Comprehensive R Archive Network, 2016); available online at https://github.com/vegandevs/vegan. 65. G. H. Shepard, H. Ramirez, “Made in Brazil”: Human dispersal of the Brazil Nut (Bertholletia excelsa, Lecythidaceae) in Ancient Amazonia. Econ. Bot. 65, 44-65 (2011). 66. C. A. Peres, C. Baider, Seed dispersal, spatial distribution and population structure of Brazil nut trees (Bertholletia excelsa) in southeastern Amazonia. J. Trop. Ecol. 13, 595616 (1997). 67. P. M. Paiva, M. C. Guedes, C. Funi, Brazil nut conservation through shifting cultivation. For. Ecol. Manage. 261, 508-514 (2011). 68. P. S. Sujii, K. Martins, L. H. de Oliveira Wadt, V. n. C. R Azevedo, V. N. Solferini, Genetic structure of Bertholletia excelsa populations from the Amazon at different spatial scales. Conserv. Genet. 16, 955-964 (2015). 69. C. R. Clement, A center of crop genetic diversity in western Amazonia. BioScience 39, 624-631 (1989). 70. I. K. Dawson et al., Origins and genetic conservation of tropical trees in agroforestry systems: a case study from the Peruvian Amazon. Conserv. Genet. 9, 361-372 (2008).
71. J. de Paiva, L. d. M. Barros, J. Cavalcanti, in Breeding Plantation Tree Crops: Tropical Species, S. M. Jain, P. M. Priyadarshan, Eds. (Springer, 2009), pp. 287–324. 72. W. Balée, Indigenous transformation of Amazonian forests: an example from Maranhão, Brazil. L'Homme 33, 231-254 (1993). 73. R. M. Alves, A. M. Sebbenn, A. S. Artero, C. R. Clement, A. Figueira, High levels of genetic divergence and inbreeding in populations of cupuassu (Theobroma grandiflorum). Tree Genet. Genomes 3, 289-298 (2007). 74. V. A. Vos, O. Vaca, A. Cruz, “Sistemas Agroforestales en la Amazonía Boliviana” (Centro de Investigación y Promoción del Campesinado (CIPCA), 2015). 75. N. Smith, Ed., Palms and People in the Amazon (Springer Series in Geobotany Studies, 2015). 76. G. Morcote-Ríos, R. Bernal, Remains of palms (Palmae) at archaeological sites in the New World: A review. Bot. Rev. 67, 309-350 (2001). 77. R. J. Seibert, The uses of Hevea for food in relation to its domestication. Ann. Missouri Bot. Gard. 35, 117-121 (1948). 78. A. C. Roosevelt et al., Paleoindian cave dwellers in the Amazon: the peopling of the Americas. Science 272, 373-384 (1996). 79. P. B. Cavalcante, Ed., Frutas comestíveis na Amazônia (Museu Paraense Emílio Goeldi, 2010).
source (country.shp, rivers.shp): ESRI (http://www.esri.com/data/basemaps, © Esri, DeLorme Publishing Company.
Shield; EA, eastern Amazonia). Black circles show the observed values of absolute abundance (A) and relative abundance (B), ranging from 0-292 individuals of domesticated species per 1 ha and 0-61 % of the total number of individuals, and the observed values of absolute richness (C) and relative richness (D), ranging from 0-19 domesticated species per plot and 0-19 % of the total number of species. The white-green background shows the interpolation of the observed values (in %) in each plot modelled as a function of latitude and longitude on a 1o-grid cell scale using loess spatial interpolation (17). Maps were created with custom R scripts. Base map source (country.shp, rivers.shp): ESRI (http://www.esri.com/data/basemaps, © Esri, DeLorme Publishing Company).
southern Amazonia; CA, central Amazonia; GS, Guiana Shield; EA, eastern Amazonia). Red circles indicate negative effects and blue circles positive effects. Standardized coefficients are presented only for significant relations analyzed in the models (p ≤ 0.05). Adjusted r2 and significant codes (p values: ≤ 0.001 ‘***’; ≤ 0.01 ‘**’; ≤ 0.05 ‘*’; > 0.05 ‘ns’) are presented for the effect of regions at the Amazonia-wide level (All) and all regression models.
coefficients at the Amazonia-wide level (All) and region-level regression models (NWA, northwestern Amazonia; SWA, south-western Amazonia; SA, southern Amazonia; CA, central Amazonia; GS, Guiana Shield; EA, eastern Amazonia). Red circles indicate negative effects and blue circles positive effects. Standardized coefficients are presented only for significant relations analyzed in the models (p ≤ 0.05). Adjusted r2 and significant codes (p values: ≤ 0.001 ‘***’; ≤ 0.01 ‘**’; ≤ 0.05 ‘*’; > 0.05 ‘ns’) are presented for the effect of regions at the Amazonia-wide level (All) and all regression models.
Fig. 5. Relative contributions of human and environmental variables for explaining variation in relative abundance and richness of domesticated species in Amazonian forests. The figure shows the partitioning of variation in relative abundance (A) and relative richness (B) of domesticated species uniquely explained by environmental (dark gray) or human factors (light gray), and the variation jointly explained by both (gray). Variance partitioning was conducted over the results of multiple regression analyses presented in Fig. 3. Amazonia was divided in six geological regions (NWA, north-western Amazonia; SWA, south-western Amazonia; SA, southern Amazonia; CA, central Amazonia; GS, Guiana Shield; EA, eastern Amazonia).
grants to RAINFOR from the Natural Environment Research Council-NERC (UK) and the Gordon and Betty Moore Foundation European Union. OP is supported by a European Research Council Advanced Grant and a Royal Society Wolfson Research Merit Award. We thank Jerome Chave, Alberto Vincentini and Corine Vriesendorp, Umberto Lombardo and Heiko Prümers for providing data, and Bernardo Monteiro Flores for constructive comments on the manuscript. ABJ and EKT thank all archaeologists who contributed with archaeological coordinates. All data described in the paper are present in the main text and the supplementary materials and custom R scripts used in analyses are provided in the supplementary materials. Additional data related to this paper can be obtained by contacting authors.

References: V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V. 
 V.