LETTERSRecuperation of nitrogen cycling in Amazonianforests following agricultural abandonmentEric A. Davidson1, Cla´udio J. Reis de Carvalho2, Adelaine Michela Figueira3, Franc¸oise Yoko Ishida3,Jean Pierre H. B. Ometto3, Gabriela B. Nardoto3, Renata Tuma Saba´2, Sanae N. Hayashi4, Eliane C. Leal4,Ima Ce´lia G. Vieira4& Luiz A. Martinelli3Phosphorus (P) is generally considered the most common limitingnutrient for productivity of mature tropical lowland forests grow-ing on highlyweatheredsoils1–5. It is often assumedthatP limitationalso applies to young tropicalforests, but nitrogen (N) losses duringland-use change may alter the stoichiometric balance of nutrientcycling processes. In the Amazon basin, about 16% of the originalforest area has been cleared6, and about 30–50% of cleared land isestimated now to be in some stage of secondary forest successionfollowing agriculturalabandonment7. Here we use forestage chron-osequences to demonstrate that young successional forests growingafter agricultural abandonment on highly weathered lowland trop-ical soils exhibit conservative N-cycling properties much like thoseof N-limited forests on younger soils in temperate latitudes. Assecondary succession progresses, N-cycling properties recoverand the dominance of a conservative P cycle typical of mature low-land tropical forests re-emerges. These successional shifts in N:Pcycling ratios with forest age provide a mechanistic explanation forinitially lower and then gradually increasing soil emissions of thegreenhouse gas nitrousoxide (N2O). The patternsof N and P cyclingduring secondary forest succession, demonstrated here over deca-dal timescales, are similarto N- and P-cycling patternsduring prim-ary succession as soils age over thousands and millions of years, thusrevealing that N availability in terrestrial ecosystems is ephemeraland can be disrupted by either natural or anthropogenic distur-bances at several timescales.Ecologists have long noted that tropical forests growing on highlyweathered soils exhibit conservative P-cycling processes, whereasconservative N-cycling properties are more common on youngersoils, including most temperate forests and montane forests1,2. Thispattern was demonstrated along a soil age chronosequence in theHawaiian Islands3, where N, which is derived primarily from theatmosphere, is in short supply in the youngest volcanic soils andgradually accumulates as soils age. In contrast, rock-derived P is moreabundant in young soils but becomes bound in unavailable forms tosoil minerals as soil weathering proceeds over thousands and millionsof years. In global-scale analyses, the N:P ratios of green foliage4andlitterfall5of mature forests have been shown to increase with decreas-ing latitude, indicating generally increasing P conservation anddecreasing N conservation with soil age.Although these stoichiometric generalizations seem robust formature forests, accelerating land-use change is altering tropical land-scapes worldwide, and the consequences for nutrient cycling in second-ary forests are unclear8. Secondary tropical forests are playing anincreasingly important part in maintaining genetic diversity9andhydrological functioning of altered landscapes10, but biogeochemicalprocesses remain poorly studied in tropical secondary forest succession.Forest clearing causes an initial loss of nutrients from Amazonianterrestrial ecosystems through fire, erosion, soil emissions of gases,harvesting of timber and hydrologic leaching of nutrients8,11.Additional losses occur as cattle or crops are harvested and as fireis used as a management tool to prepare fields for planting and tocontrol pasture weeds12. Both N and P can be lost as particulatesduring biomass burning13, but, in contrast to P, N is also volatilizedas a gas. Nitrate also generally leaches from soils more readily thandoes phosphate. As a consequence of these N losses, net N miner-alization, net nitrification, nitrate leaching and soil efflux of N2Ooften decline as tropical cattle pastures age14–17. Fertilization canmaintain agricultural productivity, but where fertilization is not eco-nomically viable, the cleared land is often abandoned and a secondaryforest begins to grow. Aggrading forests create a strong demand foressential plant nutrients. The objective of this study was to use space-for-time substitutions in secondary forest age chronosequences todescribe patterns in the indicators of N and P nutrient cycling duringtropical secondary forest succession.Three forest-age chronosequences, including stands ranging in agefrom 3 to 70 yr and remnant mature forests, were established in theBrazilian state of Para´, in eastern Amazonia. A complete set of sevenindicators of N-cycling rates was obtained for the chronosequence inour main study site in the municipality of Sa˜o Francisco do Para´.Toprovide true replication, a second chronosequence was established inthe municipality of Capita˜oPoc¸o, and a third chronosequence wasconstructed from previously published studies on a ranch in the muni-cipality of Paragominas. The Sa˜o Francisco do Para´and Paragominasmunicipalities are about 200 km apart, with Capita˜oPoc¸o roughly inthe middle. Not all of the indicators could be measured in the secondand third chronosequence, but each indicator is represented by at leasttwo replicate chronosequences. Soil texture varied among the chrono-sequences, but was relatively uniform within each chronosequence(Supplementary Table 1). The dominant vegetation of the regionwas once moist lowland tropical forest, but is now a mosaic of sec-ondary forests, agricultural fields, cattle pastures and tree crops18(seeSupplementary Information for more site information).All of the indicators derived from analysis of green foliage, litter-fall, soil and trace gas emissions are consistent with a conservative Ncycle in the young successional forests, recovery of N-cycling pro-cesses as succession proceeds, and a leaky N cycle in advanced stagesof secondary succession and in mature forests (Fig. 1). The log-linearrelationships indicate that the largest changes in N-cycling indicatorsoccur early during succession and that the rate of change declines asthe secondary forests mature.The first indicator, foliar15N, increases with increasing forest agein both Sa˜o Francisco do Para´and Capita˜o Poc¸o chronosequences1The Woods Hole Research Center, 149 Woods Hole Road, Falmouth, Massachusetts 02540-1644, USA.2EMBRAPA Amazoˆnia