Drought Sensitivity of the Amazon Rainforest

Science, March 6, 2009,

Oliver L. Phillips,^1* Luiz E. O. C. Aragão,² Simon L. Lewis,¹ Joshua B. Fisher,² Jon Lloyd,¹ Gabriela López-González,¹ Yadvinder Malhi,² Abel Monteagudo,³ Julie Peacock,¹ Carlos A. Quesada,^1,4 Geertje van der Heijden,¹ Samuel Almeida,⁵ Iêda Amaral,^4,6 Luzmila Arroyo,^7,8 Gerardo Aymard,⁹ Tim R. Baker,¹ Olaf Bánki,¹⁰ Lilian Blanc,¹¹ Damien Bonal,¹² Paulo Brando,^13,14 Jerome Chave,¹⁵ Átila Cristina Alves de Oliveira,⁴ Nallaret Dávila Cardozo,¹⁶ Claudia I. Czimczik,¹⁷ Ted R. Feldpausch,¹ Maria Aparecida Freitas,⁵ Emanuel Gloor,¹ Niro Higuchi,¹⁸ Eliana Jiménez,¹⁹ Gareth Lloyd,²⁰ Patrick Meir,²¹ Casimiro Mendoza,²² Alexandra Morel,² David A. Neill,^8,23 Daniel Nepstad,^24,25 Sandra Patiño,^1,11 Maria Cristina Peñuela,¹⁹ Adriana Prieto,²⁶ Fredy Ramírez,¹⁶ Michael Schwarz,^1,27 Javier Silva,² Marcos Silveira,²⁸ Anne Sota Thomas,²⁹ Hans ter Steege,³⁰ Juliana Stropp,³⁰ Rodolfo Vásquez,³ Przemyslaw Zelazowski,² Esteban Alvarez Dávila,³¹ Sandy Andelman,⁶ Ana Andrade,⁴ Kuo-Jung Chao,¹ Terry Erwin,³² Anthony Di Fiore,³³ Eurídice Honorio C.,³⁴ Helen Keeling,¹ Tim J. Killeen,⁷ William F. Laurance,^4,35 Antonio Peña Cruz,³ Nigel C. A. Pitman,³⁶ Percy Núñez Vargas,³⁷ Hirma Ramírez-Angulo,³⁸ Agustín Rudas,³⁹ Rafael Salamão,⁵ Natalino Silva,⁴⁰ John Terborgh,⁴¹ Armando Torres-Lezama³⁸

Amazon forests are a key but poorly understood component of the global carbon cycle. If, as anticipated, they dry this century, they might accelerate climate change through carbon losses and changed surface energy balances. We used records from multiple long-term monitoring plots across Amazonia to assess forest responses to the intense 2005 drought, a possible analog of future events. Affected forest lost biomass, reversing a large long-term carbon sink, with the greatest impacts observed where the dry season was unusually intense. Relative to pre-2005 conditions, forest subjected to a 100-millimeter increase in water deficit lost 5.3 megagrams of aboveground biomass of carbon per hectare. The drought had a total biomass carbon impact of 1.2 to 1.6 petagrams (1.2 x 10¹⁵ to 1.6 x 10¹⁵ grams). Amazon forests therefore appear vulnerable to increasing moisture stress, with the potential for large carbon losses to exert feedback on climate change.

¹ Ecology and Global Change, School of Geography, University of Leeds, Leeds LS2 9JT, UK.
² Environmental Change Institute, School of Geography and Environment, Oxford University, Oxford OX1 3QY, UK.
³ Jardín Botánico de Missouri, Oxapampa, Pasco, Peru.
⁴ Instituto Nacional de Pesquisas na Amazônia, Av. Andre Araujo, 1753 CP 478, 69060-011 Manaus AM, Brasil.
⁵ Museu Paraense Emílio Goeldi, Av. Perimetral, 1901 Terra Firme, CEP: 66077-830 Belém PA, Brasil.
⁶ Tropical Ecology Assessment and Monitoring Network (TEAM), Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA.
⁷ Museo de Historia Natural Noel Kempff Mercado, Casilla 2489, Av. Irala 565, Santa Cruz, Bolivia.
⁸ Missouri Botanical Garden, Box 299, St. Louis, MO 63166, USA.
⁹ Programa de Ciencias del Agro y del Mar, Herbario Universitario (PORT), Universidad Nacional Experimental de Los Llanos Occidentales Ezequiel Zamora, Mesa de Cavacas, Portuguesa 3350, Venezuela.
¹⁰ Nationaal Herbarium Nederland, W.C. van Unnikgebouw, Heidelberglaan 2, 3584 CS Utrecht, Netherlands.
¹¹ Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UMR EcoFoG, Campus Agronomique, BP 709, 97387 Kourou Cedex, French Guiana.
¹² Institut National de la Recherche Agronomique (INRA), UMR EcoFoG, Campus Agronomique, BP 709, 97387 Kourou Cedex, French Guiana.
¹³ Instituto de Pesquisa Ambiental da Amazônia, Avenida Nazaré 669, CEP-66035, Belém PA, Brasil.
¹⁴ Department of Botany and School of Natural Resources and Environment, University of Florida, P.O. Box 118526, Gainesville, FL 32611, USA.
¹⁵ Laboratoire EDB, Université Paul Sabatier, Bâtiment 4R3, 31062 Toulouse, France.
¹⁶ Universidad Nacional de la Amazonía Peruana, Iquitos, Loreto, Perú.
¹⁷ Department of Earth System Science, University of California, Irvine, CA 92697, USA.
¹⁸ Departamento de Silvicultura Tropical, Manejo Florestal, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936 Petrópolis, Manaus AM, Brasil.
¹⁹ Universidad Nacional de Colombia, Kilómetro 2 Via Tarapacá, Leticia, Amazonas, Colombia.
²⁰ National Australia Bank, UB2211, 800 Bourke Street, Docklands, VIC 3008, Australia.
²¹ School of Geosciences, University of Edinburgh, Edinburgh EH8 9XP, UK.
²² FOMABO (Manejo Forestal en las Tierras Tropicales de Bolivia), Sacta, Bolivia.
²³ Jatun Sacha Foundation, Casilla 17-12-867, Avenida Rio Coca 1734, Quito, Ecuador.
²⁴ Woods Hole Research Center, Falmouth, MA 02540, USA.
²⁵ Gordon and Betty Moore Foundation, P.O. Box 29910, San Francisco, CA 94129, USA.
²⁶ Instituto Alexander von Humboldt, Claustro de San Agustín, Villa de Leyva, Boyacá, Colombia.
²⁷ Bayreuth Center of Ecology and Environmental Research, University of Bayreuth, 95440 Bayreuth, Germany.
²⁸ Depto de Ciências da Natureza, Universidade Federal do Acre, Rio Branco AC 69910-900, Brasil.
²⁹ Faculty of Agriculture and Horticulture, Humboldt University of Berlin, Phillipstrasse 13, 10557 Berlin, Germany.
³⁰ Institute of Environmental Biology, Department of Biology, Faculty of Science, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, Netherlands.
³¹ Facultad de Ingeniería Forestal, Universidad del Tolima, 546 Ibagué, Colombia.
³² Department of Entomology, National Museum of Natural History, Smithsonian Institution, MRC 187, P.O. Box 37012, Washington, DC 20013, USA.
³³ Center for the Study of Human Origins, Department of Anthropology, New York University, New York, NY 10003, USA.
³⁴ Instituto de Investigaciones de la Amazonía Peruana, Av. José A. Quiñones km. 2.5, Apartado Postal 784, Loreto, Perú.
³⁵ Smithsonian Tropical Research Institution, Roosevelt Avenue, Tupper Building 401 Balboa, Ancón, Panamá, República de Panamá.
³⁶ Centro de Investigación y Capacitación del Río de Los Amigos, Madre de Dios, Perú.
³⁷ Universidad Nacional San Antonio Abad del Cusco, Av. de la Cultura 733, Cusco, Apartado Postal N° 921, Perú.
³⁸ INDEFOR, Facultad de Ciencias Forestales, Universidad de Los Andes, Mérida, Venezuela.
³⁹ Instituto de Ciencias Naturales, Universidad Nacional de Colombia, Apartado 7495, Bogotá, Colombia.
⁴⁰ Serviço Florestal Brasileiro, SCEN Trecho 2, Ed. Sede do IBAMA Bloco H, 70.818-900 Brasília DF, Brasil.
⁴¹ Center for Tropical Conservation, Duke University, Box 90381, Durham, NC 27708, USA.

^* To whom correspondence should be addressed. E-mail: o.phillips@leeds.ac.uk ; Internet: www.rainfor.org

Old-growth forests in Amazonia store 120 Pg (1.2 x 10¹⁷ g) of carbon in their biomass (1), and through photosynthesis and respiration they process 18 Pg C annually (2), more than twice the rate of anthropogenic fossil fuel emissions. Relatively small changes in Amazon forest dynamics therefore have the potential to substantially affect the concentration of atmospheric CO₂ and thus the rate of climate change itself. A key parameter in determining the magnitude of this effect is the sensitivityor resilienceof tropical forests to drought. Increased moisture stress is a dominant feature of some modeled 21st-century climate scenarios for Amazonia, particularly for southern Amazonia (35), and there is some evidence that this has already commenced (6). Prolonged tropical droughts can kill trees (710), and some models predict climate-induced Amazon dieback this century (4, 11, 12). But it has also been suggested that dry conditions may cause Amazon forests to "green up" (13, 14) and that increases in solar radiation during drier periods boost tropical productivity (1517). Large-scale on-the-ground assessments of the ecological impacts of tropical droughts are completely lacking, precluding tests of these ideas.

In 2005, large areas of the Amazon Basin experienced one of the most intense droughts of the past 100 years (18), providing a unique opportunity to directly evaluate the large-scale sensitivity of tropical forest to water deficits. The 2005 event was driven not by El Niño, as is often the case for Amazonia, but by elevated tropical North Atlantic sea surface temperatures (18), which affected the southern two-thirds of Amazonia and especially the southwest through reduced precipitation as well as higher-than-average temperatures (18, 19). Both the anomalous North Atlantic warming and its causal link to Amazon drought are reproduced in some recent modeled scenarios for 21st-century climates (5, 12), and thus the event of 2005 may provide a proxy for future climate conditions. Through a large long-term research network, RAINFOR, we have monitored forest plots across the basin for 25 years. After the drought we conducted an emergency recensus program covering all major Amazon nations, climates, soils, and vegetation types. Here we report the results of this large-scale natural experiment to assess the impact of tropical drought on the ground.

By 2005 the RAINFOR network consisted of 136 permanent plots located in old-growth forest distributed across 44 discrete landscapes ("sites") (20). We used tree diameter, wood density, and allometric models to compute biomass at each point in time, as well as rates of biomass gain ("growth") and loss ("mortality") between censuses, correcting for possible sampling effects (20). To establish the pre-2005 Amazon baseline, we first determined the long-term biomass changes in our plots. To assess drought impacts, we focused on the 2005 event, evaluating net biomass change, growth, and mortality and the differences in these relative to earlier records, focusing on the 55 plots that were regularly censused both before and after the drought. To estimate the moisture stress at each location, we compiled meteorological data sets and determined the maximum dry-season intensity for each year in the 2005 measurement interval and for each year in the entire pre-2005 measurement period. Forest sensitivity to drought was then determined by relating the change in biomass dynamics to the change in mean maximum moisture stress. The results presented below are based on the sampling unit of individual plots; in (20) we explore the sensitivity of our findings to varying both the spatial scale of the sampling unit and the method of estimating moisture stress.

Before 2005, plots recorded a long-term net increase in aboveground (dry-weight) biomass, weighted by sampling effort, of 0.89 Mg ha^1 year^1 (bootstrapped 95% confidence intervals: 0.65, 1.12). This increase occurred through a multidecadal period spanning dry and wet episodes, including several El Niño events. The net biomass gain was widespread and is not a sampling artifact (20). These results confirm previous measured and modeled indications of a persistent biomass carbon sinknow based on a much larger data setand are consistent with Amazon forest productivity increasing with time (2125).

By contrast, through the 2005 drought period there was no net biomass increase in monitored plots [net rate of change 0.71 (1.93, +0.30) Mg ha^1 year^1; n = 55, interval mean 1.97 years]. Before 2005, 76% of plots (93 of 123) gained biomass, but during the 2005 interval only 51% did so (28 of 55); this difference is highly significant (P < 0.01, Mann-Whitney U test). To assess whether biomass changes were drought-related, we developed meteorological and soil data sets to estimate evapotranspirational demand and soil moisture stress (20). For plots with longer and more intense moisture deficits than normal, there were clear net losses [1.62 (3.16, 0.54) Mg ha^1 year^1; n = 38, interval mean 1.96 years]. The distribution through time of all measured biomass dynamics (Fig. 1) reveals that the drought coincided with the first substantial decline in measured biomass in Amazonian plots since measurements started. However, fingerprinting the drought impact is complicated by switching among plots being monitored, the nonequilibrium initial conditions, divergent climatologies and soils, and contrasting conditions in 2005 itself. Within-plot analyses help to control for such effects and confirm the drought's impact: Relative to their extended period of earlier biomass gains, plots monitored through 2005 experienced negative change [difference = 1.50 (3.01, 0.44) Mg ha^1 year^1; n = 43]. Among the 28 plots with longer and more severe water deficits than normal during 2005, the rate of aboveground woody biomass accumulation declined by 2.39 (1.12 to 3.97) Mg ha^1 year^1, whereas by contrast the 15 nondroughted plots continued to gain [difference = +0.76 (0.78, +2.00) Mg ha^1 year^1].

The Amazon forest spans a large climatic range, from the almost aseasonal high-precipitation northwest to the strongly seasonal southern fringes with frequent prolonged moisture deficits (26, 27). Distributions of neotropical trees reflect their drought sensitivity (28), so we hypothesized that any drought impacts will be experienced by plants as a function of relative departure from their long-term environmental conditions. For each site, we therefore estimated the magnitude of the drought experienced during the 2005 interval relative to local, long-term estimates of water balance. We find that relative drought is indeed strongly implicated as the driver of the network-wide shift in forest behavior (Fig. 2) but that the absolute intensity of the 2005 dry period was only weakly related to biomass dynamics (fig. S5): Those forests experiencing the most elevated moisture stress relative to their long-term mean tended to lose the most biomass relative to their pre-2005 trend (Fig. 2). These losses were driven by occasionally large mortality increases and by widespread but small declines in growth. Our method may fail to capture growth impacts well because intervals were longer than the period of potential moisture constraint, thereby masking its effects (drought can kill trees but can only temporarily stop growth). Analysis at the site level confirms that the relationship between forest response and droughting is not driven by a few anomalous plots (20), and accounting for local soil water-holding capacity, temperature, humidity, and radiation shows this relationship to be robust regardless of how the moisture balance is estimated (20). Moreover, just as the earlier net gains were widespread across the basin, the 2005 declines were well distributed spatially (Fig. 3). From Fig. 2, and assuming a proportional impact on smaller trees and lianas (20), we estimate that an average forest hectare subject to a 100-mm increase in maximum water deficit lost 5.3 Mg of aboveground biomass carbon over the average 1.97-year drought census interval relative to pre-2005 conditions (bootstrapped confidence intervals 3.0, 8.1).

We also recorded the identity of trees that died. Fast-growing, light-wooded trees may be especially vulnerable to drought by cavitation or carbon starvation (7, 2931), and consistent with this, trees dying during the 2005 period had lower wood densities than those dying before. In 25 drier-than-average plots with dead trees identified, trees recorded as dead in 2006 were 5% lighter than in previous censuses [mean wood density of dead trees fell from 0.60 to 0.57 g cm^3 (P = 0.02) (20)]. Apparently, Amazon drought kills selectively and therefore may also alter species composition, pointing to potential consequences of future drought events on the biodiversity in the Amazon region.

Relative to the predrought sink, we estimate a total impact of 1.21 Pg C (2.01, 0.57) by simply scaling the per-plot impact by the total droughted area ( 3.3 x 10⁸ ha) and assuming that nonmeasured components of biomass were equally affected. Scaling the per-site impact yields slightly greater values (20). Alternatively, we can scale the observed relationship between relative biomass change in plots and droughting (Fig. 2) by the moisture deficits across Amazonia estimated from remotely sensed rainfall data (19, 20). This suggests an even greater impact on the biomass carbon balance of the droughted area: 1.60 Pg C (2.63, 0.83). Site-based scaling-up indicates similar values (20). Although better understanding of soils is needed to determine the local effects of meteorological drought, the magnitude and consistency of these estimates demonstrate Amazonia's vulnerability to drought and the potential for changes in tropical climates to have large carbon cycle impacts. Our on-the-ground data reveal that, despite apparent "greening up" during dry periods (13, 14), Amazon drought accelerates mortality over large areas (Fig. 2B) (20).

The exceptional growth in atmospheric CO₂ concentrations in 2005, the third greatest in the global record (