the size of the environmental legacy of tropical deforestation is  dependent on both the magnitude and timing of past land cover changes , rather than the snapshot of forest cover that is directly observable today .
we used a validated regional data - constrained spatial model of tropical deforestation   to backcast deforestation from 2009 to 1950 in the three main tropical regions ( figure  s1 ) : the amazon , the congo basin , and southeast ( se ) asia , which was further divided into six sub - regional models ( see supplemental experimental procedures and data s1 ) .
our model provided estimates of deforestation rates for the 1980s , 1990s , and 2000s that fell within the ranges reported previously for all three tropical regions ( table s1 ) .
we estimate through our model that rates of tropical deforestation were very low in the 1950s and then accelerated first in the amazon in the 1970s , then in se asia in the 1990s and most recently in the congo basin ( figure  1 ) .
this pattern is in line with accepted histories for the regions [ 7 , 8 ] , as is the slowdown in deforestation in the amazon after 2004 that our model also captured . combining potential vegetation carbon maps with our simulated historical deforestation maps
, we estimated that the modern era of tropical deforestation resulted in cumulative emissions of 49.93 petagrams ( pg ) of vegetation carbon ( 1.99 pg , 95% confidence interval [ ci ] ) between 1950 and 2009 .
annual emissions from gross tropical deforestation rose sharply over the modern period to 2.30 pg of vegetation carbon per year ( 0.06 pg , 95% ci ) by 2009 ( figure  2a ) .
even if deforestation had stopped completely in 2010 , the vegetation carbon emissions debt of modern tropical deforestation ensured there was 8.6 pgc ( 2.24 pg , 95% ci ) of committed emissions still to be released , equivalent to roughly 510 years of global deforestation .
the legacy is highest in the amazon , where we estimated 3.72 pgc ( 1.10 pg , 95% ci ) was still to be released . in se asia and the congo basin , we estimated the legacies to be 3.54 pgc ( 1.50 pg , 95% ci ) and 1.34 pgc ( 0.34 pg , 95% ci ) , respectively , with the se asian legacy   concentrated in the present - day deforestation hotspots of sumatra and southern borneo ( figure  3 ) . the amazon is the largest remaining continuous tropical forest and accounts for 49% of total tropical forest carbon stock , with the remainder shared roughly evenly between se asia ( 26% ) and the congo basin ( 25% ) . over time
, 28%66% of the gross emissions came from the amazon , an estimated 25%62% from  se asia , and a much lower share of 9%14% from the congo basin ( supplemental experimental procedures and figure  s2 ) . in each of the three tropical regions , committed gross emissions by 2009 accounted for 60% of the carbon emissions in that year .
we estimated that modern gross deforestation has led to an extinction debt of 144 forest - specific vertebrate species ( 14 , 95% ci ) ( figure  2b ) , which is a number 20% larger than the total number of extinctions known to have occurred in vertebrate groups since 1900 ( n  = 124 ) . while se asia was responsible for the majority of this debt until the 1980s ( 50%70% ; figure 
s3 ) , from the 1990s onward this legacy has been dominated by land cover changes that have occurred in the amazon ( > 50% ) .
the congo basin still represents a low share ( 5% ) due to the slower rates of deforestation in this region . of the 4,125 forest - specific tropical vertebrate species ( mammals , birds , and amphibians ) ,
52% were found in the amazon , 38% in se asia , and 10% in the congo basin ( supplemental experimental procedures ) .
we estimated that a total of 41 vertebrate species ( 4 , 95% ci ) have already been driven irreversibly extinct , with the amazon being the region with the highest number of species lost by 2009 : 28 ( 2 , 95% ci ) , compared to 15 ( 3 , 95% ci ) in se asia and only 1 ( 0 , 95% ci ) in the congo basin .
our model predicted that 1.1% of tropical vertebrate forest - specific species would have gone extinct by 2010 , similar to the 1.2% of forest - specific species that are classified as extinct by the iucn , indicating our model is accurately recreating the pan - tropical patterns of extinction threat to forest - specific vertebrate species .
we found that within each tropical region , environmental legacies of past deforestation are not evenly distributed across space ( figure  3 ) . in the amazon ,
environmental legacies are broadly concentrated in the heavily deforested regions of the  arc of deforestation  along the southeastern rim of the amazon , whereas in the congo basin these are mainly concentrated in the south and eastern parts of the basin , where agricultural activity has been most intense .
in se  asia , there are large differences in the size of both environmental legacies among different island groups .
for example , intensive deforestation in mainland indochina and in the philippines mostly occurred earlier than elsewhere , meaning that more of the debt has already been paid compared to other areas , such as the islands of sumatra and borneo , where much of the deforestation has occurred more recently .
furthermore , we found that carbon and extinction debts are poorly correlated in all regions ( figure  4 ) , despite both being created by the same historical patterns of deforestation .
this occurs because the time delays in carbon emissions are shorter than those involved in species extinction , meaning that patterns of extinction debt reflect deforestation from earlier periods than the patterns of carbon emissions debt .
this same variation in time delays ensures that the proportional magnitude of the deforestation legacy is higher for biodiversity than it is for carbon ( figure  2 ) .
carbon dioxide emissions from tropical deforestation are already impacting the earth s atmosphere and climate and account for 10%20% of annual anthropogenic emissions .
furthermore , widespread habitat loss has already caused significant species losses globally , with important impacts on ecosystems .
here we have shown that the carbon debt is equivalent to almost one - fifth of all historical gross emissions from tropical deforestation over the 60-year period we modeled , and to the emissions of 510 years of global deforestation .
the extinction debt of vertebrate species , on the other hand , if paid , will increase the number of known extinctions in these groups since 1900   by 120% . in both cases these are substantial , and previously unquantified , debts that must be paid unless specific actions , including habitat restoration and targeted interventions for threatened species , are put in practice . to generate these estimates ,
we have utilized a model that has been validated on the basis of accurately simulating the time course of deforestation over time in tropical regions .
uncertainty was propagated throughout our study ( supplemental experimental procedures ) : in the relationship between deforestation and its drivers ( allowing parameter values to vary ) , when estimating carbon emissions ( both in the biomass maps and in the carbon bookkeeping parameters ) , and in the extinction debt estimates ( allowing both z and k values to vary ) . as a result of rigorously validating our model against multiple different datasets and accounting for multiple different sources of uncertainty , we believe we have produced the best current estimates of the environmental legacy of modern - day tropical deforestation .
our results show that reaching national and global emissions targets may , in practice , be more difficult than expected .
the carbon debt means that emissions in any one year are a function of deforestation over previous years .
for instance , the carbon debt in the amazon in 2010 is equivalent to the total carbon emissions from 3.5 years of deforestation at the average rate observed in the 2000s .
thus , changes in annual deforestation rates will initially have a smaller than expected effect on annual emission rates .
this time lag means , for example , that the 30% reduction in deforestation rates seen in the brazilian amazon between 2005 and 2010 has so far resulted in a reduction of just 10% of actual carbon emissions over the same time period . at the cancun conference of the parties of the united nations framework convention on climate change in 2010 , several tropical countries , where emissions from land use and land cover change often exceed those from the energy sector , voluntarily committed to reduce their carbon emissions : brazil aims to reduce its total greenhouse gases emissions by 36%39% from its  business as usual
 levels by 2020 , and indonesia aims to reduce its emissions by at least 41% between 2009 and 2020 .
recently , at the united nations sustainable development summit 2015 in new york , brazilian president dilma rousseff committed to a further  intended reduction  of brazil s emissions of 43% by 2030 .
reducing deforestation is the most immediate method available to meet these stringent targets , which is partially why , at the 2009 conference of the parties in copenhagen , brazil committed to reduce amazon deforestation rates by 80% relative to the 19952005 baseline .
however , our results demonstrate clearly that reductions in actual emissions will lag many years behind reductions in deforestation rate .
we necessarily assumed that the variables found to be driving deforestation in the 2000s also drove deforestation in  previous decades ( owing to the lack of data for previous decades ) , but this does not seem to have caused substantial bias in our results .
this appears to be because deforestation resulting from different causes ( e.g. , conversion to agricultural land or fires following timber extraction ) tends to generate similar spatial patterns of forest loss ( e.g. , occurring primarily along road networks ) .
this consistency in the deforestation patterns arising from different root causes , and our explicit approach of modeling the spatial expansion of deforestation directly , means that our simulations about the spatial and temporal patterns of deforestation history are relatively robust to uncertainty about the underlying processes .
deforestation activities evolved over time from small - scale slash - and - burn agriculture to large - scale industrial agriculture , which impacted the fractions of carbon immediately lost versus left to decay over time .
however , there are no spatial high - resolution datasets available with the full history of land use change in the tropics to take this into account
. our gross vegetation carbon emissions estimates are larger than those reported in other studies for all three tropical regions ( supplemental experimental procedures ) . in part , this can be explained by the fact that we used a potential vegetation carbon map , which included belowground carbon stored in roots , not just aboveground stems and leaves .
this map ignores the fact that some of the forests covered in our study could have an initial carbon stock lower than the potential carbon , for example as a result of harvesting or fire events . however , an important reason for the differences between our estimates and other recent regional estimates is that we included the additional time - delayed emissions of carbon , which in recent decades represent a substantial proportion of annual emissions .
initially , in the early years of deforestation ( i.e. , 19501970 ) , our estimates are similar to those in the literature ( supplemental experimental procedures ) . however , as the size of the carbon debt gradually increases through time , an increasing amount of emissions in a  given year are contributed by  legacy emissions  ( figure  2 ) .
importantly , our estimates for 20092010 ( 0.51   0.04 pgc / year ) are comparable to independent measurements made in the amazon ( 0.48   0.18 pgc / year , for 20092011 ) by sampling greenhouse gases in the lower troposphere , indicating that our model provides an accurate representation of deforestation - related carbon emissions .
the most commonly employed action to prevent species extinctions is to protect habitat , but that approach alone will do little to avoid paying an extinction debt that has already accumulated from historical habitat loss . under aichi target 12   of the convention on biodiversity ,
78 countries , 9 of which lie within the geographic bounds of this study , have made voluntary agreements at the national level to prevent the extinction of known threatened species and improve their conservation status by 2020 .
our results suggest , however , that tropical nations with large extinction debts will be unlikely to succeed in preventing the further loss of species without substantial investment in habitat restoration , as well as targeted conservation interventions for threatened species .
our estimates for species losses and extinction debt in the amazon are slightly higher than those previously estimated , but this is because our analysis encompasses the whole amazon basin , not just the brazilian amazon .
we are not aware of any other previous studies that have estimated extinction debt across all tropical forests with which to compare our results .
the total extinction debt , across all taxonomic groups present in these highly biodiverse tropical regions , is likely to be orders of magnitude larger than our estimate , which is based solely on three well - studied vertebrate groups .
nonetheless , species movements , adaptation , and mitigation strategies , which we did not consider in our study , would contribute to lower this debt .
previous analyses have demonstrated a poor correlation between stocks of carbon and biodiversity , leading to calls for developing combined carbon - biodiversity conservation strategies , which better resolve trade - offs between the two conservation aims [ 19 , 20 ] .
we have confirmed not only that is this true , but also that carbon and extinction debts are poorly correlated in space .
however , time delays in carbon emissions and extinctions create a potential window for habitat restoration and conservation actions to alleviate or even avoid having to pay the committed debts . just as strategies to simultaneously preserve stocks of carbon and biodiversity can be optimized through careful planning [ 19 , 20 ] , the ideal locations for habitat restoration actions to reverse the combined carbon - biodiversity debts will require detailed spatial planning to find cost - effective solutions .
frameworks for making these decisions , including the  incorporation of time lags , exist and have demonstrated the counterintuitive result that it can be more cost - effective for  conservation strategies to forego a sole focus on habitat protection in favor of restoring degraded areas .
these decision - making frameworks now need to be applied if we are to avoid paying the full cost of the environmental legacy of tropical deforestation .
we collected data from a variety of freely available sources , including annual global land cover maps from 2001 through 2010 derived from modis satellite imagery , and variables that could impact deforestation .
these included the location of roads , protected areas , and rivers ; population density ; altitude ; and climate .
we then used a data - constrained and validated spatial model of tropical deforestation   to backcast at 1  km resolution both the rates and spatial patterns of deforestation from 2009 to 1950 in the three main tropical regions : the amazon , the congo basin , and se asia ( supplemental experimental procedures ) . for each region
modeled , we combined our deforestation estimates with spatially explicit maps of potential living vegetation carbon   and a modified carbon bookkeeping model   to calculate the carbon emissions debt ( supplemental experimental procedures ; figures 2a , 3a3c , and s2 ) .
we applied the exponential decay rates provided by houghton et  al .   at each annual time step and used bookkeeping to calculate the emissions released in a given year , as well as carried over into the subsequent year .
unlike previous studies , our bookkeeping model allowed for uncertainty in the parameter determining the proportion of emissions release immediately following a deforestation event .
we obtained geographic range data [ 23 , 24 ] for forest - specific mammal , bird , and amphibian species ( table s2 ) and combined these with our spatially explicit trajectories of historical forest cover ( figure  s1 ) to estimate species losses and extinction debt in each region ( supplemental experimental procedures ; figures 2b , 3d3f , and s3 ) , following wearn et  al . .
the model uses the species - area relationship ( sar ) to predict the equilibrial species richness expected under habitat loss but extends the sar to include  a time - delayed community  relaxation  to equilibrium . by explicitly incorporating time , this model allowed for estimation of species loss and extinction debt at any point between 1950 and 2009 .
appropriate parameter values for the model were obtained using past studies , with uncertainty in these parameters accounted for using monte carlo simulations .
for the coarser regional - scale analysis , we aggregated all of our input data at the scale of eight broad regions ( amazon , congo basin , and the six sub - regions  of se asia ) , treating each region as a single cell .
we then used the temporal trajectories of forest cover simulated by our deforestation model to determine losses and extinction debt of forest - specific species in each unit .
the fine - scale analysis was done within 10   10  km cells .
we used cell - specific  trajectories of past forest loss ( figure  s1 ) to estimate the impact of modern deforestation on the levels of local species loss and extinction debt in each cell ( figures 3d3f ) .
i.m.d.r . assisted with formulation of the research question , generated code , conducted all the analyses and interpretation of results , and wrote the manuscript . m.j.s . obtained the potential carbon maps , helped with outputs interpretation , and provided critical manuscript revisions .
o.r.w . helped run the extinction debt model and interpret its results , and assisted with valuable reviews of the manuscript .
r.m.e . assisted with formulation of the research question , assisted in results interpretation , and provided critical revision of the manuscript .
 summarytropical deforestation has caused a significant share of carbon emissions and species losses , but historical patterns have rarely been explicitly considered when estimating these impacts [ 1 ] . 
 a deforestation event today leads to a time - delayed future release of carbon , from the eventual decay either of forest products or of slash left at the site [ 2 ] . 
 similarly , deforestation often does not result in the immediate loss of species , and communities may exhibit a process of  relaxation  to their new equilibrium over time [ 3 ] . 
 we used a spatially explicit land cover change model [ 4 ] to reconstruct the annual rates and spatial patterns of tropical deforestation that occurred between 1950 and 2009 in the amazon , in the congo basin , and across southeast asia . using these patterns , we estimated the resulting gross vegetation carbon emissions [ 2 , 5 ] and species losses over time [ 6 ] . 
 importantly , we accounted for the time lags inherent in both the release of carbon and the extinction of species . 
 we show that even if deforestation had completely halted in 2010 , time lags ensured there would still be a carbon emissions debt of at least 8.6 petagrams , equivalent to 510 years of global deforestation , and an extinction debt of more than 140 bird , mammal , and amphibian forest - specific species , which if paid , would increase the number of 20th - century extinctions in these groups by 120% . given the magnitude of these debts , commitments to reduce emissions and biodiversity loss 
 are unlikely to be realized without specific actions that directly address this damaging environmental legacy . 
Results
Discussion
Experimental Procedures
Author Contributions