Corresponding Author Email-Id: Mercedes@unb - BR: Version of Record Doi: 10.1111/gcb.13087

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2 Received Date : 11-Apr-2015
3 Revised Date : 23-Jul-2015
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Accepted Date : 19-Aug-2015
5 Article type : Research Review
9 Corresponding author email-id: mercedes@unb.br
10 Towards an integrated monitoring framework to assess the effects of tropical forest degradation
11 and recovery on carbon stocks and biodiversity
12 Abstract
13 Tropical forests harbor a significant portion of global biodiversity and are a critical
14 component of the climate system. Reducing deforestation and forest degradation contributes
15 to global climate-change mitigation efforts, yet emissions and removals from forest dynamics
16 are still poorly quantified. We reviewed the main challenges to estimate changes in carbon
17 stocks and biodiversity due to degradation and recovery of tropical forests, focusing on three
18 main areas: (1) the combination of field surveys and remote sensing; (2) evaluation of
19 biodiversity and carbon values under a unified strategy; and (3) research efforts needed to
20 understand and quantify forest degradation and recovery. The improvement of models and
21 estimates of changes of forest carbon can foster process-oriented monitoring of forest
22 dynamics, including different variables and using spatially explicit algorithms that account
23 for regional and local differences, such as variation in climate, soil, nutrient content,
24 topography, biodiversity, disturbance history, recovery pathways, and socio-economic
25 factors. Generating the data for these models requires affordable large-scale remote-sensing
26 tools associated with a robust network of field plots that can generate spatially explicit
27 information on a range of variables through time. By combining ecosystem models, multi-
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1 scale remote sensing, and networks of field plots, we will be able to evaluate forest
2 degradation and recovery and their interactions with biodiversity and carbon cycling.
3 Improving monitoring strategies will allow a better understanding of the role of forest
4 dynamics in climate change mitigation, adaptation and carbon cycle feedbacks, thereby
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reducing uncertainties in models of the key processes in the carbon cycle, including their
impacts on biodiversity, which are fundamental to support forest governance policies, such
7 as REDD+.
8 Introduction
9 In 2010, total anthropogenic GHG emissions reached 49 (±4.5) Pg CO 2 eq.yr-1, 76% of which
10 consisted of CO 2 emissions. Agricultural, Forest, and Other Land-Use sectors (AFOLU) account for 20 to
11 25% (~ 10–12 Pg CO 2 eq./yr) of net anthropogenic GHG emissions, of which 4.3–5.5 Pg CO 2 eq./yr is
12 from forestry and other land use (FOLU) (Smith et al., 2014). Estimates of emissions from indicate that
13 there has been a recent decline in CO 2 emissions, largely because the rate of tropical deforestation has
14 decreased but forest degradation is still poorly accounted for in current FOLU emissions and it is likely to
15 be an important source of emissions (Smith et al., 2014).
16 Globally, forest degradation affects approximately 100 million ha of forest per year (FAO, 2006;
17 Nabuurs et al., 2007). Indirect estimates of forest degradation, expressed as a percentage of emissions
18 from deforestation, are highly variable, ranging from 5% in the humid tropics to 25–42% in tropical Asia
19 and 132% in tropical Africa (see Houghton (2005) for a review). Conversely, regrowth of secondary
20 forests may remove considerable amounts of carbon from the atmosphere (Pan et al., 2011), and
21 extensive areas of regrowth have been reported in the tropics (e.g., Aide et al. 2013). Asner et al. (2010)
22 used high resolution (0.1 ha resolution) satellite imagery to analyze 4.3 million ha in the Peruvian
23 Amazon (19992009), and found that forest degradation added ≅ 47% more carbon to the atmosphere
24 than deforestation alone, and that secondary regrowth provided an 18% offset against total emissions in
25 Peru, a high forest cover, low deforestation country. Despite some attempts to estimate carbon losses
26 resulting from forest degradation (Achard et al., 2004; Berenguer et al., 2014), this is still a major
27 challenge for national carbon inventories. Carbon finance schemes, such as the UN-led Reducing
28 Emissions from Deforestation and Forest Degradation (REDD+), require accurate estimates of carbon
29 emissions and robust monitoring and reporting of changes in carbon stocks (UNFCCC, 2011; Andersson
30 et al., 2009).
31 Although satellite and airborne remote-sensing technologies associated with field measurements have
32 strong potential to assess large-scale (national and global) carbon stocks (DeFries et al., 2007; Goetz et

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1 al., 2009; Saatchi et al., 2011; Baccini et al., 2012), current methods and data cannot deliver the desired
2 precision to assess and monitor forest stocks and changes due to forest degradation and regrowth (Asner
3 et al. 2009; GOCF-GOLD, 2013). In fact, estimates of CO 2 emissions related to FOLU have uncertainties
4 of the order of 50 % (IPCC, 2014). Quantifying forest degradation and regrowth at large scales remains a
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major constraint in the implementation of REDD+ mechanisms (Aguiar et al., 2012; Mitchard et al.,
2014; Ometto et al., 2014).
7 Important consequences of deforestation and forest degradation include decreases in

8 environmental, social and economic functionalities (de Mendonça et al., 2004; Nepstad et al., 2001;
9 Tavani et al., 2009), increased vulnerability to fire (Cochrane & Schulze, 1999; Nepstad et al., 1999;
10 Matricardi et al., 2010; Alencar et al., 2011), and doubling of net carbon emissions from regional land-
11 use during severe El Niño episodes and other drought years (Chen et al., 2013; Aragão et al., 2014;
12 Alencar et al., 2006). Reducing deforestation and expanding secondary forests can increase forest
13 resilience to more frequent and severe droughts, which are projected by the latest generation of climate
14 models for some tropical forest regions, and increasing the risk from forest fires in coming decades. Thus,
15 reducing emissions from forest degradation, not only emissions from deforestation, is essential to mitigate
16 global climate change (Aragão & Shimabukuro, 2010) and its impacts on forests and other ecosystems.
17 Forest resilience, and therefore its ability to retain and accumulate carbon, depends on the composition
18 and key functional relationships between species. Anthropogenic disturbance degrades forests by
19 reducing taxonomic and functional diversity and ecological redundancy, and preventing recovery and
20 destabilizing forest ecosystems (Thompson et al., 2009). Forest biodiversity conservation is a critical
21 component in the development and implementation of REDD+ (Díaz et al., 2009; Convention on
22 Biological Diversity, 2011). REDD+ projects have strong potential to conserve biodiversity and
23 ecosystem services (Gardner et al. 2012). Biodiversity conservation is often assumed to be a co-benefit of
24 activities that reduce forest carbon degradation (Waldon et al., 2011), but REDD+ projects can have
25 detrimental impacts on biodiversity if low-carbon, high-biodiversity forests are replaced with high-
26 carbon, low-biodiversity land-uses, or if protection of high-carbon forests in one area leads to degradation
27 of areas with endemic species or high-diversity forests elsewhere. Thus, biodiversity monitoring within a
28 REDD+ framework is necessary to ensure that impacts, beyond carbon, are positive (Harrison et al.,
29 2012).
30 Future mitigation scenarios also rely on the central role of land-cover / land-use changes (Smith et al.,
31 2014). Therefore, monitoring systems for forest dynamics represent an important interface between
32 science and policy. To ensure that predictions of change for a given action can be reconciled with actual

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1 changes in C stocks, integrative and multiscale approaches are needed to make systems applicable for a
2 wide range of national realities and capabilities. One option for efficient and effective monitoring of
3 forest dynamics is wall-to-wall assessment and temporal reassessments, using short time intervals to
4 study forest recovery and resilience. Currently, monitoring systems provide classification with well-
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developed land-cover and change estimates but identification of changes in carbon stocks needs to be
based on more ground information.
7 Monitoring forest degradation and REDD+ monitoring, reporting and verification (MRV) systems
8 can be based on two components: activity data (AD), to assess changes in forest area over time (forest
9 cover loss in ha/yr); and emission factors (EF), to assess changes in average carbon stocks per unit area
10 over time (change in carbon stocks in Mg C/ha) (GOFC-GOLD, 2013). Activity data can be readily
11 obtained from remote sensing imagery to detect deforestation, but detecting forest degradation with these
12 data is still a challenge. Moreover, emission-factor estimates for tropical forest deforestation and
13 degradation are far more challenging to obtain (Plugge & Khol, 2009). Another important issue for
14 REDD+ and forest degradation is building appropriate reference scenarios. REDD+ requires a reliable
15 benchmark against which emission reduction can be calculated. This benchmark, sometimes termed a
16 baseline or reference emission scenario, refers to how much emission would occur in the absence of a
17 project. Credits will be based on the difference between this baseline and project net removals. However,
18 developing countries frequently lack consistent historical monitoring and land cover data. Therefore, in
19 assessing historical degradation, they are forced to rely strongly on remote sensing approaches mixed
20 with current field assessments of carbon stock changes (Herold et al., 2011). Given the lack of historical
21 biomass data for appropriate benchmarks and the limited capability for monitoring degradation using
22 remote sensing, Morales-Barquero et al. (2013) proposed that forest degradation is best measured against
23 a local benchmark that represents areas of low or no degradation and sharing comparable biophysical
24 characteristics.
25 Here, we review the main challenges to estimate changes both in GHG fluxes associated with
26 carbon stocks, and biodiversity due to tropical forest degradation and regrowth. Three main points are
27 stressed: (1) the combination of field inventories and remote sensing; (2) evaluation of biodiversity and
28 carbon values under a unified strategy; and (3) research efforts needed to understand and quantify forest
29 degradation and recovery. When combined, these three points can support the development and
30 implementation of public policies that ensure tropical nations compliance to international commitments
31 and efforts, such as those established by REDD+ national strategies.
32 Evaluating changes in forests: combination of field inventories and remote sensing

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1 Forest degradation can be defined as the reduction of the capacity of a forest to provide key
2 ecosystem services, such as carbon storage, and can be caused by natural (e.g. landslides and hurricanes)
3 or human disturbances (e.g. selective logging and understory fires) (Parrota et al., 2012). Forest
4 degradation, therefore, implies that quantifiable forest variables, such as canopy cover, remain above the
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threshold used to define deforestation. However, measuring carbon-stock changes due to different degrees
of forest degradation is more complex and more costly than measuring carbon loss due to deforestation.
7 This is because, while deforestation is highly visible for broadleaf tropical forests (i.e. the complete forest
8 cover of an area disappears), degradation can be cryptic both to remote sensing techniques and field
9 observation (Peres et al., 2006; Barlow et al., 2010; Berenguer et al., 2014). Furthermore, changes in
10 forest structure following disturbance may not be very pronounced (Pereira et al., 2002). Forest responses
11 to disturbance depend on the disturbance type, frequency, intensity, and extent, on intrinsic site
12 characteristics (e.g. climate, soil, topography, species composition and interactions), and on forest
13 management (Figure 1). Forest post-disturbance trajectories can vary widely, and this variation needs to
14 be considered in carbon accounting exercises, including patterns of regrowth over time (e.g. spatially
15 explicit map of secondary forest and their turnover, faunal diversity, nutrient availability). Events that are
16 associated with large changes in the forest C stock and areas where carbon-storage changes are greatest,
17 such as areas undergoing deforestation, degradation, and secondary forests dynamics, should be
18 identified, quantified, and monitored in detail, as well as their impacts on long-term changes in
19 community and key species composition.
20 Countries can measure current rates of forest degradation through field or remote sensing data, but
21 a combination of the two types of data can reduce uncertainties in regional and national estimates (Asner
22 et al., 2010). There is a direct relationship between an accurate and precise assessment of changes in
23 carbon stocks and cost, with costs of measuring changes in carbon stocks increasing as both precision and
24 landscape heterogeneity increase (IPCC, 2000). Therefore, trade-offs between measurement efforts and
25 uncertainty should be indicated when choosing spatial scales and measuring methods in carbon
26 accounting (Figure 2).
27 Although field assessment and monitoring of carbon stocks are relevant for small-scale projects,
28 they are impractical and too expensive at the national-scale. Still, field assessments and monitoring of
29 forest carbon can provide valuable information about local changes in carbon stocks due to human
30 disturbance (Barlow et al. 2003, Berenguer et al. 2014), which may not otherwise be detected. In many
31 cases, significant cost savings can be made by focusing on the largest stems, which store the largest
32 amount of carbon and are highly sensitive to disturbance (E. Berenguer et al., unpublished results).

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1 Additionally, if field-based carbon assessments and monitoring incorporate identification of plant species,
2 they can also deliver important information about changes in species composition (Laurance et al., 2006),
3 which in turn can feedback into biological safeguards of each carbon conservation project. This is
4 particularly important in secondary forests, where failure to incorporate species identity can incur an error
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in aboveground carbon estimates of about 30% (E. Berenguer et al. unpublished results).
6 Remote-sensing techniques can be a cost-effective option to assess forest carbon stocks over very
7 large areas (e.g. nation-wide). Depending on the technique used, remote sensing may provide data at
8 regular intervals, allowing countries to frequently monitor deforestation and degradation events, as well
9 as subsequent carbon loss (e.g. different systems used in Brazil for monitoring of the Amazon forest, such
10 as DEGRAD, PRODES, DETER). However, although optical sensors can be used to identify forest
11 degradation by selective logging and wildfires, as well as to estimate the extent of affected areas, (Souza
12 et al., 2005; Asner et al., 2005a; Herold et al., 2011; Morton et al., 2011), they can only detect changes
13 that affect canopy properties, thus neglecting changes in the understory. Furthermore, the ability to detect
14 changes in carbon stocks due to forest degradation varies according to the technique used, with some
15 being more accurate than others (Gibbs et al., 2007; DeFries et al., 2007).
16 Thus, changes in carbon stocks resulting from forest degradation rely on a combination of field
17 surveys (site-specific biophysical field attributes) and remote sensing. The choice of the method to
18 monitor forest degradation depends on multiple factors, such as type of degradation, available data,
19 capabilities and resources (Herold et al. 2011). Challenges associated with different methods include
20 temporal thresholds and spatial scales and integration of field and satellite data sets (Figure 3). Key issues
21 to consider are which biophysical parameters should be measured and which time windows are
22 appropriate to integrate the two approaches.
23 Remote-sensing methods for monitoring carbon-stock changes and forest degradation have been
24 extensively reviewed and discussed (Lambin, 1999; IPCC, 2003; Boyd & Danson, 2005; Gibbs et al.,
25 2007; DeFries et al., 2007; Frolking et al., 2009; Wertz-Kanounnikoff, 2008; Herold et al,. 2011; Goetz et
26 al., 2009; GOFC-GOLD, 2013). Gibbs et al. (2007) outlined the benefits and limitations of different
27 methods to estimate carbon-stock changes, concluding that there is no best method, and most are
28 complementary. In fact, the formula for an effective monitoring system is consensual and seems rather
29 simple: combining satellite (and/or airborne) remote sensing to (scale-up) allometric and statistical
30 models, developed and based on robust field-based datasets (Defries et al., 2007). Recently, this has been
31 successfully applied in Panama and Peru, resulting in high-fidelity carbon maps for both countries (Asner
32 et al., 2013; Asner et al., 2014). However, even though carbon dynamics in forests are far better

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1 understood than in other vegetation types (grasslands/drylands, wetlands/peatlands) (Negra, 2010),

2 uncertainties about forest-carbon stocks are still very high. Pelletier et al. (2011) synthesized the key
3 sources and associated explanations of uncertainty in the quantification of emissions from land-cover
4 change using Panama as study case (Table 1). The combination of errors drawn from allometric equations
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and sampling can be as large as 20–50% of the aboveground-biomass estimate. Other factors include
historical map quality, land-cover classification accuracy, the time interval between two land-cover
7 assessments, and the fallow C. That study did not address forest degradation or soil C estimates because
8 of the lack of robust information on these processes. Better ground observations that include long-term
9 field studies on soil C pools, which cannot be monitored from space but are relevant, would improve
10 emissions accounting and the understanding of forest dynamics.
11 Most methods combine remote-sensing analyses with field plots, which are limited (in number
12 and spatial distribution) and possibly biased (Saatchi et al., 2014; Marvin et al., 2014), resulting in many
13 divergent biomass maps in literature (Houghton et al., 2001; Houghton et al., 2009; GOFC-GOLD, 2013;
14 Mitchard et al., 2014; Ometto et al., 2014). Estimates of aboveground carbon stocks vary by over 100%
15 in African forests (Lewis et al., 2009) and by 60% in Amazonian forests (Houghton et al., 2000).
16 Emission estimates calculated from land-cover change in the Amazon remain markedly divergent, and are
17 largely due to differences among biomass maps (Aguiar et al., 2012; Ometto et al., 2014). Ometto et al.
18 (2014) emphasized the need for higher-resolution biomass maps, and for improving ground-truth data
19 (e.g. via field networks), and post-processing data to include variability, such as topography and soils.
20 Uncertainty associated with regional-scale values from different sources (to quantify biomass and fluxes)
21 is also high. Wright (2013) argued that Pan et al. (2011) overestimated terrestrial-carbon sinks because of
22 incompatibility between the sources used for forest area and carbon stocks. Forest area was based on
23 FAO’s Forest Resource Assessment (FAO-FRA), which defines forest as land with trees > 5 m of height
24 and canopy cover ≥ 10%. However, carbon stocks were derived from plots located in tall, closed canopy
25 forests, in which carbon stocks and changes are potentially much larger than in open forests (Wright,
26 2013).
27 Optical sensors can only detect changes that affect upper-canopy properties and have limited
28 ability to estimate C stocks and C-stock changes, especially for dense forests, because spectral indices
29 saturate at relatively low C stocks. Estimating forest biomass requires information on tree volume and
30 wood density. In contrast to passive optical sensors, active sensors from radar and LiDAR can provide
31 data to estimate biomass volume, but an estimate of wood density is still needed. Large-scale estimates of
32 forest biomass with active sensors have been hampered by costs or operational limitations. Despite these

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1 limitations, LiDAR is becoming a useful tool that scientists use to understand physical variation in
2 tropical forests across space and time (Mascaro et al., 2014). Recent and future developments will
3 increasingly allow large-scale surveys (e.g. cost reduction of airborne surveys and European Space
4 Agency satellite LiDAR to be launched by 2020). In order to take full advantage of such remote-sensing
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developments, well-sampled and precisely located ground-truth data are needed for calibration.
National forest inventories (NFI’s) often comprise a robust, large-scale (country-level) and
7 unbiased network of permanent plots and could help to provide much of the data needed for calibration
8 for LiDAR and radar derived properties (e.g. for estimating biomass stocks and their changes). For this
9 reason, they can help integrate remote sensing and field data on carbon changes, especially if location of
10 the plots is precisely recorded. For example, with approximately 2,000 measuring plots, the Peru National
11 Forest Inventory is designed as a multipurpose inventory including the state and valuation of forests,
12 deforestation, forests degradation, carbon sequestration and emissions, biodiversity and socioeconomic
13 relationship of forests. Similarly, the Brazilian NFI, currently underway, will provide continuously
14 updated estimates of forest carbon density, tree species composition, soil and socio-economic variables,
15 which are based on a massive sample size (15,000 clusters with four subplots each), in a systematic and
16 unbiased sampling design that is limited mainly by land-access issues. The Mexican NFI was based on
17 the United States and Canada’s NFI’s, and contains data on tree species, shrubs, and trees for every forest
18 vegetation type. In 2009, Mexico included a soil survey with the National Forest Inventory quantifying
19 organic soil-carbon pools and biomass-carbon ratios. Results are part of a national soil database.
20 Biomass maps should not be static but should be produced in time series, thereby capturing C-
21 stock evolution across time as consequence of observed events (or when time series are projected, using
22 dynamic modeling, reflecting the risks of biomass loss). Forest plots under different management
23 regimes, environmental conditions and disturbance trajectories are relevant for ecological studies
24 involving forest disturbance and recovery. Building an observational network of forest plots is a primary
25 need that requires careful planning, including landscape-level assessment, integration with initiatives
26 currently underway, and evaluation of time intervals for temporal reassessments needed to examine
27 recovery and resilience of forests. The coordination between detailed efforts (with more frequent and
28 detailed sampling) and national forest inventories that have less detail but cover larger areas (including
29 private lands) is highly desirable, considering information consistency.
30 An effective program of monitoring of forest dynamics must include the risk of fire, the fire
31 regime, and emissions-associated environmental impacts. Fires affect large areas in the tropics (Morton et
32 al., 2013) and have a wide range of effects on forest structure, carbon storage and biodiversity (Silveira et
33 al., 2013; Barlow & Peres, 2008; Oliveiras et al., 2014). In the Amazon, extreme droughts caused by
34 ENSO or other climatic phenomena boost fires (Aragão et al., 2007) and the combined effect of drought

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1 and forest fires may turn the Amazon into a carbon-source system (Aragão et al., 2014; Gatti et al., 2014).
2 For example, during the 1998 ENSO, forest fires affected an area twice as large as the average
3 deforestation in that decade, generating committed emissions of 0.16 Pg C, which is comparable to the
4 0.2 Pg C emitted by deforestation in that period (Alencar et al., 2006). Forest fires react to forest
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structure, drought and fragmentation, generating distinct spatial processes of degradation. Dense forests
burn more in ENSO years in small patches and at lower frequencies (up to 6 times in 24 years) compared
7 with transitional forest that burn in large patches at a higher frequency (up to 19 times in 24 years) (see
8 Asner & Alencar (2010) for a review). However, in the last decade (2000-2010), large forest fires were
9 observed even in non-ENSO years (Alencar et al., 2011; Morton et al. 2013). The carbon emissions due
10 to fires in Amazonia during 2010 and 2011, an extremely dry and wet year, respectively, were estimated
11 as 0.51±0.12 PgC yr-1 in 2010 and 0.25±0.14 PgC yr-1 in 2011. Additionally, forest degradation caused by
12 forest fires produces relevant amounts of non-CO 2 greenhouse gases. Forest fires release CH 4 , N 2 O,
13 ozone precursors and aerosols (including black carbon), whereas forest regrowth after fire absorbs only
14 CO 2 . Globally, in 2010, non‐CO 2 emissions from deforestation and forest-degradation fires totaled 0.1
15 PgCO 2 eq./yr, with forest management and peatland fires responsible for an additional 0.2 Pg CO 2 eq./yr
16 (Smith et al., 2014).
17 Despite the recent quantification of fire-affected areas by remote-sensing data, current

18 methodologies are unable to disentangle different fire intensities and their on-the-ground impacts on
19 forest structure and composition. In the Amazon region, understory fires burned more than 85,500 km2 in
20 the Amazon Basin south of the main course of the Amazon River between 1999 and 2010 (>80% in
21 Brazil). Only 2.6% of forests that burned between 1999 and 2008 were deforested for agricultural use by
22 2010 (Morton et al., 2013). Cumulative fire-induced forest degradation needs to be quantified over longer
23 time scales. Multiple fires in the same forest are rare but result in devastating effects on both forest
24 biomass and biodiversity (Barlow & Peres, 2004; Morton et al., 2013; Alencar et al., 2011). Fire-induced
25 tree mortality is highly variable (from 5 to 90%) (Balch et al., 2011; Brando et al., 2012) as are its effects
26 on carbon stocks and subsequent forest recovery. Key aspects to be developed for efficient and effective
27 monitoring programs of forest dynamics should include risk of fire (climate and topography, forest
28 structure and available fuel material, socio-economic drivers), fire regime (seasonality, frequency, human-
29 dominated fire regimes), associated emissions (carbon, trace gases, aerosols, committed vs. net emissions)
30 and ecosystem impacts (burned area and severity, mortality, post-fire succession, recovery). Table 2
31 presents a compilation of different remote-sensing products and some field studies.

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1 It is also important to consider that synergisms among simultaneous disturbance vectors

2 dramatically increase rates of forest degradation. The combined effects of drought and understory fires
3 can lead to abrupt and fundamental changes in vegetation structure and dynamics. In particular, droughts
4 can trigger fire-induced tree-mortality events that are large enough to substantially reduce forest carbon
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stocks (by killing trees and combusting woody debris) and accumulation, increase forest flammability (by
increasing air dryness), and facilitate forest invasion by flammable grasses (by increasing light
7 availability in the understory). Together, the modifications in forest structure and dynamics resulting
8 from drought-fire interactions can create positive feedbacks between fire and grass invasion that lead to
9 further degradation. For example, Silvério et al. (2014) showed that grass invasion following fire-induced
10 tree-mortality events can increase the occurrence of high-intensity fires, as grasses produce more fine fuel
11 than forests. These hot fires further increase tree mortality, the likelihood of grass invasion, and the
12 potential for subsequent high-intensity fires, even in the absence of droughts. Forest fragmentation
13 interacts with fire by creating flammable environments near forest edges that dry during prolonged dry
14 seasons, increasing the fuel load and fire probability (Cochrane, 2001; Brando et al., 2014).
15 Interactions between degradation drivers were also demonstrated in Eastern Amazonia (Berenguer
16 et al., 2014). In that study, forests submitted to both selective logging and understory fires became
17 structurally more similar to secondary forests and stored, on average, 40% less aboveground carbon than
18 undisturbed forests. The understanding of the impacts of selective logging as a degradation factor is still
19 very limited (Sist et al., 2014). Although some studies point to a high retention of the biomass and
20 biodiversity after logging (Putz et al., 2012), they mainly encompass planned timber harvesting rather
21 than the widespread unsustainable logging activities witnessed in the tropics. Addressing this knowledge
22 gap is important, especially considering the magnitude of the disturbances caused by unplanned-logging
23 operations (Asner et al., 2005). Furthermore, almost half of primary tropical forests (+400 million ha) are
24 considered for timber production by national forest services (Blaser et al., 2011).
25 In terms of natural disturbances, windstorms are another important ecological stressor that have
26 been shown to drive forest degradation, particularly when these events are associated with forest
27 fragmentation and fire disturbances. Although wind-related disturbances differ widely in terms of
28 magnitude and intensity across the Amazon (Espirito-Santo et al., 2014), they may drive substantial losses
29 in forest biomass (Negrón-Juárez et al., 2010; Espirito-Santo et al., 2014) and fragmented landscapes
30 (Benchimol & Peres 2015). These losses could be higher in previously burned areas, given that the
31 modifications in forest structure caused by fires increase the exposure of individuals to wind-related
32 damages. Although it is challenging and requires integration of different methods, quantifying the

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1 individual and combined effects of different drivers of forest degradation is key to obtaining accurate
2 estimates of their impacts on carbon stocks.
3 Monitoring carbon and biodiversity – need for a unified strategy
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Unifying carbon and biodiversity monitoring is important for two key reasons. First, although
biodiversity within (and often across) biomes is not necessarily correlated with carbon stocks (Strassburg
6 et al., 2010), there is growing evidence of a tighter link at local scales, where higher carbon stocks are
7 often associated with forests that contain more endemic species or species of conservation concern (Lima
8 et al., 2013; Gilroy et al., 2014). In this case, monitoring will be important to identify the extent to which
9 carbon conservation is delivering the expected biodiversity co-benefits, and to assess if the link may be
10 modulated by anthropogenic impacts such as hunting pressure (Peres & Palacios, 2007) or landscape-
11 level area and isolation effects, such as time lags to species extirpation or colonization (Gibson et al.,
12 2013). Second, concerns about integrating biodiversity and carbon are justified as there is growing
13 evidence that forest species composition and functional diversity are important for supporting forest
14 carbon sequestration (Bunker et al., 2005; Conti & Díaz, 2013) and key ecosystem functions, such as
15 secondary seed dispersal (Griffiths et al., 2015). In this case, monitoring may be required to evaluate the
16 abundance of functionally relevant sets of species such as seed dispersing mammals and birds, or to
17 examine how important ecosystem processes are mediated by biodiversity.
18 The many linkages between carbon and biodiversity mean that biodiversity monitoring should be
19 considered in every stage of the REDD+ process, from planning and design to implementation and
20 assessment (Gardner et al., 2012). This could be achieved through a common framework based on a
21 tiered approach partially analogous to the IPCC guidance on tiered-emissions reporting, where the
22 distribution of threats to biodiversity and the corresponding responses could be monitored simultaneously
23 with carbon. As well as answering important questions about carbon and biodiversity co-benefits, such
24 long-term monitoring efforts are also likely to be scientifically rewarding: some of the most important
25 insights regarding the ecological consequences of human actions have come from long-term assessments
26 of human impacts in tropical forests (e.g. Laurance et al., 2011, Gibson et al. 2013).
27 Nevertheless, designing effective biodiversity monitoring in degraded environments is challenging.
28 Many countries have developed standardized biodiversity monitoring schemes to examine ecological
29 change over time. These include the National Ecological Observatory Network (NEON) in the USA, and
30 the breeding bird survey in the UK. Within the tropics, existing biodiversity monitoring initiatives focus
31 mainly on undisturbed sites, e.g. “Tropical Ecology Assessment and Monitoring Network” (TEAM),
32 “Center for Tropical Forest Science” (CTFS), “Program for Biodiversity Research Studies” (PPBio).

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1 However, new initiatives are currently being established to monitor biodiversity in degraded primary
2 forests and secondary forests, such as ECOFOR in Brazil and Partners in Costa Rica. These initiatives
3 indicate that some taxa (e.g. frogs, birds, large vertebrates, trees, ferns, ants, dung beetles, stream fish and
4 crustaceans) are particularly suitable for monitoring over long time scales.
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Within degraded forests there is a tension between adopting standardized approaches, thereby
ensuring comparability across sites, and adopting methodological protocols that are best able to respond
7 to the most pertinent questions in the particular study landscape. RAPELD, a sampling strategy
8 combining rapid assessments and long-term ecological research, is the dominant long-term monitoring
9 methodology in Brazil, and has the advantage of providing a modular system that records many variables,
10 including those related to carbon dynamics (Magnusson et al., 2013). There are similar opportunities to
11 build on existing initiatives, such as the National Forest Inventories (e.g. Brazil, Peru, Colombia,
12 Mexico), and the PPBio in Brazil, Nepal and Australia. Alternative approaches involve organizing
13 monitoring activities around catchments, which is sensible where concerns about forest carbon are linked
14 to hydrological services or freshwater biodiversity. This was the approach taken by the Sustainable
15 Amazon Network that assessed responses of six taxonomical groups to gradients of forest disturbance
16 across thirty six 50-km2 catchments in Eastern Amazon (Gardner et al., 2013). This network has revealed
17 how forest degradation by fires, selective logging, and fragmentation can profoundly impact both
18 biodiversity and carbon (e.g. Moura et al. 2013; Berenguer et al., 2014), with cascading consequences for
19 the integrity of aquatic systems (Leal 2015). Whatever the chosen sampling design, it is important that it
20 captures the main anthropogenic stressors in the system of interest, which are likely to vary on a site by
21 site basis. Furthermore, monitoring efforts will need to be fully integrated with local institutions to ensure
22 longevity and adequate taxonomic support, and will often be reliant on strong and long-lasting
23 relationships with local landholders. None of these activities is trivial, and will often require local
24 training, capacity building as well as knowledge exchange and dissemination activities.
25 Biodiversity monitoring may be facilitated by using semi-automated approaches such as acoustic
26 monitoring and camera-trapping, which have several advantages in terms of cost-effectiveness over time
27 and links to data analysis (O’Brien et al., 2010; Aide et al., 2013). Waldon et al., (2011) proposed a
28 standardized protocol for monitoring biodiversity for REDD+ using camera-trapping for large vertebrates
29 and bioacoustics for bats. Camera-traps have several advantages: they are cost effective over time; they
30 can operate day and night (infrared), all year round, in nearly any landscape; batteries last for months;
31 photos are automatically date/time stamped; and images can be linked to data analysis tools (Waldon et
32 al., 2011). They may be particularly useful for REDD+ biodiversity monitoring programs, especially if
33 capture rates of target species are high, costs are relatively low, target species respond consistently and
34 rapidly to habitat condition changes, and suitable flagship conservation species exist that can be used to

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1 help raise the profile of a project. Bioacoustic monitoring of target species is another powerful tool for
2 estimating faunal biodiversity. Birds and bats have great potential as bioindicators for several reasons:
3 they have a broad pantropical distribution and comprise many species, including threatened ones; they
4 show taxonomic stability; they provide important ecosystem services and respond predictably to changes
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in habitat conditions; and they can reflect changes in arthropod prey communities and/or availability of
fruit (Jones et al., 2009; Harrison et al., 2012; Waldon et al., 2011). Automated digital recording systems
7 can monitor a wide range of animal populations, and web applications facilitate data management and
8 tools for creating species-specific algorithms to automate the identification of birds, amphibians, and
9 insects (Aide et al., 2013). Such studies of soundscapes can provide useful information on biotic,
10 environmental and human activities change through time (Pijanowski et al., 2011).
11 These technological solutions are not without their problems. The operational requirements and
12 costs of running camera-trapping or bioacoustics surveys programs may limit their utility by REDD+
13 project stakeholders (Harrison et al., 2012), and it can be difficult to deploy expensive equipment such as
14 camera traps in human-modified landscapes where traps can be stolen or vandalized by hunters and other
15 forest users. Bioacoustic monitoring is also limited at present: ultrasonic acoustic detectors cannot detect
16 non-echolocating bats, and many forest-dependent tropical species use relatively quiet and short-duration
17 echolocation pulses, which are difficult to detect. Location-specific and species-specific solutions are
18 required to overcome such constraints, such as additional monitoring of calls in the non-ultrasonic,
19 physical trapping, and camera traps (Harrisson et al., 2012). Finally, bioacoustics and related field-based
20 biodiversity monitoring approaches retain a spatial mismatch with most habitat remote sensing methods
21 (Boelman et al., 2007).
22 While many modern methods can be very effective, there are many uncertainties in biodiversity
23 monitoring that have little to do with technological or statistical aspects (Magnusson, 2014). Efforts have
24 been made to provide efficient methods suitable for community-based (Angelsen et al., 2012) and
25 participatory forest monitoring of carbon and biodiversity for REDD+ (Casarim et al., 2013), including
26 smartphone applications for community-based biomonitoring (Moran et al., 2014). Yet, all fieldwork-
27 based efforts will be constrained by the challenges of covering huge spatial areas and the limited expertise
28 in species identification. Remote-sensing techniques have been experiencing some advance in recent
29 years and may provide solutions to some of these issues. In particular, airborne-spectranomics approaches
30 (Asner & Martin, 2009) based on the leaf chemistry, physics, and the taxonomy of canopy trees that are
31 opening new paths for tropical forests monitoring, including plant diversity. Recent technologies can map
32 chemical and structural traits of plant canopies and are promising for monitoring vegetation biodiversity,
33 species range and functional traits (Schimel et al., 2013). Additionally, a more coherent collection of field

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1 trait data together with proximal and remote sensing observations will allow us to understand the
2 interaction between plant structural, physiological, biochemical, phenological and spectral properties, and
3 then to develop robust scaling schemes to support airborne and satellite-based methods of trait estimation
4 (Homolová et al., 2013). Technologies such as imaging spectroscopy and LiDAR can innovate airborne,
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tropical-forest diversity mapping. Recently, Asner et al. (2015), using visible-to shortwave infrared
(VSWIR) imaging spectroscopy with LiDAR, assessed the foliar traits of Amazonian and Andean tropical
7 forest canopies. This new airborne approach could address limitations and sampling biases associated
8 with field-based studies of forest functional traits in complex tropical canopies.
9 While indirect approaches using remote sensing offer valuable information (derived from
10 biophysical characteristics and environmental parameters) about diversity patterns, other approaches are
11 addressing direct remote sensing of certain aspects of biodiversity (Pettorelli et al., 2005; Turner et al.,
12 2003). Protocols that can integrate remote sensing and on-the-ground biodiversity assessments can be
13 effective to evaluate both structural and functional degradation. Cryptic mechanisms of forest
14 degradation, such as overhunting, could reduce the strength and diversity of ecological interactions before
15 more detectable patterns of forest degradation occur (Peres et al., 2006). Future development should
16 consider how to integrate requirements and protocols for carbon accounting, socio-cultural/socio-
17 economic impacts, and biodiversity outcomes.
18 A network of sites distributed across the tropics would help to answer questions about trends in
19 terrestrial tropical biodiversity and calibration/validation of remote sensing tools if each site captured
20 landscape variation using a spatially-explicit system, such as RAPELD (Costa & Magnusson, 2010).
21 These sites could be used for a variety of purposes, but would need to have a minimum set of essential
22 biodiversity variables (EBVs) measured at each site (Pereira et al., 2013). The cost of setting up such sites
23 is moderate depending on the practicalities of logistical access, how frequently surveys are repeated, and
24 which vertebrate, invertebrate and plant taxonomic groups are sampled (e.g. Gardner et al., 2008). For
25 example, the installation of a 5-km2 RAPELD sampling module in Brazil by a team of five experienced
26 technicians is currently about US$10,000, but varies depending on transport costs to the site. This
27 compares favorably with one-off or repeated standardized line-transect surveys of medium- to large-
28 bodied vertebrates, including understory mist-netting of birds, in many remote forest sites of lowland
29 Amazonia, each of which cost an average of US$6,000 (C.A. Peres, unpubl. data). Monitoring of a suite
30 of EBVs could be done for less than US$20,000 in general operating costs per site per year because most
31 EBVs can be efficiently measured at intervals of 2-5 years. However, as with any in-situ system, the
32 highest costs are associated with maintenance of scientific presence and training. Inclusion of local
33 researchers and students not only reduces costs, but is typically critical to the success of the sampling

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1 program. Many tropical countries resent recent experiences with colonial domination and intellectual
2 imperialism, and are unlikely to allow foreign researchers access if there are no perceived capacity-
3 building benefits to the country beyond those of possible global governance of environmental changes.
4 Based on current costs in Brazil, the cost of maintaining a field team capable of installing infrastructure
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and providing capacity building for five sites per year is about US$1,500,000. Costs could possibly be
reduced by use of previously installed capacity in countries such as Australia and Nepal. There is also
7 much capacity already installed for data management and analysis in networks such as Data
8 Observational Network for Earth (DataOne), Amazon Forest Inventory Network (RAINFOR) and
9 Amazon Tree Diversity Network (ATDN). These preliminary cost estimates indicate that it is feasible for
10 the world community to meet most of its obligations relating to biodiversity under REDD+, maximize the
11 use of new remote sensing tools, and undertake the most ambitious capacity-building program in
12 biodiversity that has ever been undertaken.
13 Integrating monitoring and ecosystem modeling: move towards more process oriented
14 approaches
15 A better understanding of forest dynamics requires the transition from the concept of carbon stock
16 change towards a more process-oriented description of forest dynamics (recruitment, mortality, growth
17 dynamics and species composition), and how these processes are modified by direct anthropogenic
18 disturbances (e.g. fire, logging, edge effects, land conversion) and extreme climatic events (e.g. severe
19 droughts, floods, and storms). Accounting for environmental impacts on forests over long time periods (at
20 least several years) requires the consideration of not only external environmental changes (e.g. climate,
21 deposition) but also changes in the vegetation itself that affect microclimatic conditions and carbon
22 allocation (Grote et al., 2011). Allocation in trees is often modeled under the assumption that the ratios
23 between leaves, stem, and roots remain constant, within certain boundaries depending on species, and that
24 tree height is the main parameter describing the effects of site-specific growing conditions. Even though
25 allometric functions describe total biomass as a function of height and diameter over a surprisingly large
26 range of conditions (Wirth et al., 2004), these functions do not predict tree age, which is important for
27 estimating carbon turnover (Schulze, 2014), or wood density, critical for carbon content.
28 Forest inventories and eddy-covariance measurements contribute to sustainability assessments as

29 well as carbon accounting. A differentiation between ecosystem compartments of carbon, such as soil and
30 vegetation, or above- and below-ground storages nevertheless requires further empirical estimates or
31 model simulations. However, models to estimate carbon balances often do not account for carbon export
32 during logging or the direct and indirect impacts of forest management (Grote et al., 2011). In addition,

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1 observational or experimental studies of ecosystems focus on local scales of less than a hectare for
2 measurements of vegetation and less than 1 km2 when using flux towers. The extrapolation to landscapes
3 remains uncertain, because we do not know the spatial variation in environmental conditions and how this
4 might affect ecosystem processes. Thus, there is a scaling problem when moving from plot-scale studies
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to landscapes. Scaling could be facilitated by the use of remotely derived variables, such as leaf area
index from NDVI-data (Schulze, 2014).
7 The integration of ecosystem models on a spatially explicit basis with monitoring systems
8 represents a promising pathway to move towards a more process-oriented description of forest dynamics.
9 Figure 4 represents the integration of field and remotely sensed data and ecosystem modeling to
10 understand forest degradation and recovery. In many cases, the modeling framework exists, but
11 appropriate parameterizations and data assimilation are still needed as more explicit representation of
12 soil/plant water relations (from “big leaf” to tree model) and stand dynamics (e.g. demography models) to
13 allow the treatment of recruitment/mortality, and forest structure. These models will be more diagnostic
14 and not prognostic, but could be appropriate for understanding C-balance change in the kind of
15 operational mode described here (e.g. spatially explicit, with ecosystem models improving estimates of
16 fluxes).
17 An analysis of the approaches currently underway with focus on carbon stocks and fluxes,
18 biodiversity and drivers of forest degradation indicate that the major limitations for all model types are
19 the lack of data for parameterization and the cost to run models at high spatial resolution. This brings the
20 question about the appropriate spatial resolution. Current book-keeping approaches provide land use
21 transition and estimates of C emission/regeneration at spatial scales of 5 km resolution (e.g. INPE-EM,
22 Aguiar et al., 2012). Although some book-keeping models include socioeconomic information, such as
23 repeated cutting of secondary vegetation, they do not consider climate interaction or soil fertility. Fire
24 models are also spatially explicit but provide emissions only. The application of ecological models at this
25 scale would add information on nutrient limitation, decomposition rates and growth rates, among other
26 variables for the estimation of spatial variation in NPP and regrowth dynamics. Nevertheless, data
27 assimilation capability is not currently implemented in ecosystem models.
28 Quantitative models are frequently employed to address the complexities associated with
29 disturbance processes. Seidl et al. (2011) reviewed the variety of approaches to modeling natural
30 disturbances in forest ecosystems (from single events to integrated disturbance regimes) in relation to
31 disturbance agents and mechanisms. The number of disturbance-modeling approaches emerging over the
32 last 15 years has increased strongly but statistical concepts for descriptive modeling are still largely

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1 prevalent over mechanistic concepts for explanatory and predictive applications that are crucial for
2 understanding and coping with change in forest ecosystems. The authors also identified the current
3 challenges for disturbance modeling in forest ecosystems as the following: (i) to overcome remaining
4 limits in process understanding, (ii) to further a mechanistic foundation in disturbance modeling, (iii) to
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integrate multiple disturbance processes in dynamic ecosystem models for decision support in forest
management, and (iv) to bring together scaling capabilities across several levels of organization with a
7 representation of system complexity that captures the emergent behavior of disturbance regimes.
8 Modification of current models to first address the largest unknowns should be prioritized,
9 recognizing that different model development/information streams will be required for a synthesis
10 framework. Advances in the current state of knowledge involve complementary efforts for field collection
11 to supply needed parameters, the use of already installed permanent plots to support functional-trait based
12 approaches, as well as the use of available data bases (e.g. converting taxonomic information into
13 functional groups, trait data bases) and the analysis of what traits could be extracted from new data
14 streams (e.g. LiDAR, hyperspectral data). Soil data from forest inventories could be used to improve the
15 analysis of spatial and temporal variation in soil nutrients. Significant efforts need to be put toward model
16 development/validation, especially toward exploring how to better apply data assimilation.
17 A synthesis of data from areas identified as being most dynamic in terms of biomass change is
18 also relevant for understanding the spatial configuration of biomass loss. Biomass data will ultimately be
19 provided by remote sensing (e.g. ESA Biomass mission will provide data after 2020, LiDAR in 2019) but
20 the models have to contribute to explanations of why the biomass is distributed the way it is and also how
21 biomass relates to function, resilience to disturbance, and biodiversity metrics. Rates of biomass
22 accumulation following disturbance and how those are influenced by climatic and soil parameters as well
23 as the pattern of landscape disturbance (e.g. distance to seed source) affects how much C is released (net
24 emissions).
25 Research priorities for forest monitoring systems
26 The determination of ecosystem carbon balances is a major issue in environmental research.

27 Research on disturbances inducing forest degradation and subsequent recovery is necessary to understand
28 the causal factors related to C stock changes and associated emissions. Although the assessment of
29 deforestation due to clear-cutting is well developed, monitoring of degradation, regeneration of forests
30 and their environmental consequences also requires greater efforts. Current monitoring methods (remote
31 sensing and field data) have shortcomings in the assessment of temporal changes of forest inventories

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1 associated with degradation, as well as forest regeneration. The limitations on the quantification of
2 degradation and forest recovery remain major constraints for the verification of results required by the
3 REDD+ mechanism. Additional research efforts could help augment long-term monitoring efforts with a
4 focus on important aspects of the carbon loss pathways (e.g. combustion, decomposition, and soil carbon
5 Author Manuscript
dynamics) and on direct manipulation experiments or space-for-time studies.
6 It is crucial to quantify and reduce uncertainties in relation to fire effects and their impacts. Future
7 research should move to improve validation (active fires, burned area, emissions ratios, fire effects - short
8 and long term), downscaling (higher resolution mapping, attribution to specific land-cover types and
9 processes of degradation/deforestation/management) and data integration (scales, models, networks
10 linking ground data, national monitoring efforts, and also international networks of fire research).
11 Forest monitoring captures human impacts and other biotic and abiotic influences on forests.
12 Detailed data is collected at stand level, often integrated in larger forest-observation networks, which
13 feeds into forest-ecosystem models. However, forests exist in a constantly changing societal context and
14 the direct or indirect impact of human activity has become a crucial driver of all types of ecosystems
15 (Daume et al., 2014). History of disturbance / regrowth / deforestation depends on social, economic and
16 climate drivers. Socioeconomic drivers are also important to determine the future trajectories of land use
17 and, thus, should be coupled to dynamic ecosystem models. Socioeconomic drivers (e.g. the advance of
18 the agricultural frontier, the installation of infrastructure projects or population movements) (Perz &
19 Skoleb, 2003; Perz et al., 2011; Walker et al., 2013) also require research and perhaps can be modeled
20 more explicitly in concert with ecological models. Emissions are often more dependent on socioeconomic
21 causes than natural ones. In order to explicitly refine estimations, these factors need to be spatialized.
22 Monitoring must be consistent and continuous. There are new perspectives both with regard to
23 the availability of data, and processing approaches and capacity. In particular, there is the expectation
24 about the synergy between the Landsat 8  began normal operations on May 2013 and provides seasonal
25 coverage of the global landmass at a spatial resolution of 30 meters (visible, NIR, SWIR); 100 meters
26 (thermal); and 15 meters (panchromatic) (Roy et al., 2014)  and the two new Sentinel 2 satellites
27 (Sentinel 2a was successfully launched on June 23rd, 2015 and Sentinel 2b should be released in April,
28 2016) (Drusch et al., 2012). Working as a constellation, they could provide data for the same area over
29 five to ten days (the sensors of these three satellites were previously pre-calibrated). This means that the
30 temporal resolution of MODIS (via time series) will be replicated to a spatial resolution (at least) 64 times
31 higher. Data of this nature will be extremely useful to map processes related to plant-traits and cryptic
32 degradation. As for the processing capacity, platforms using cloud computing (e.g. Google Earth Engine)

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1 can process Landsat 8 images rapidly and could improve spatial resolutions of models and interactions
2 involving a much larger number of variables. While potential contributions from new satellite missions
3 are recognizable, we also must be realistic about how some of these future efforts will be translated in
4 operational forest monitoring systems (e.g., a 1-year GEDI LiDAR mission in 2018-2020). However, the
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combination of field inventories and ecosystem modelling with new remote-sensing tools can open new
opportunities for faster progress of operational systems. Complementary efforts of field collection are
7 needed to provide more precise parameters and contribute to the explanation of how the growth
8 performance is influenced by climate and soil aspects. The ecological modeling should add information
9 on processes that influence the responses of forests to disturbances, such as nutrient limitation,
10 decomposition rates and growth rates.
11 A way forward to an integrated framework

12 While assessment of deforestation is well developed, forest degradation is neither well assessed nor
13 validated adequately. Forest degradation (unlike deforestation) is not binary, but rather a continuum.
14 Monitoring systems for forest degradation, whether based on in-situ or remotely sensed data (or more
15 likely a combination) depend upon operational definitions limited by the sensitivity of the measurement
16 approaches employed. Current degradation estimates differ due to the interaction between different
17 processes, such as logging and fire, temporal mismatch, scale of analysis and threshold effects. Successful
18 monitoring of degradation will have to be linked to viable quantitative-measurement approaches. A
19 summary of the main points on how to move forward with the scientific agenda and implementation of
20 improved monitoring systems of forest dynamic is presented in Table 3. The recommendations were
21 divided in the following topics: 1. Mobilization of stakeholders and scientific community to include an
22 integrated framework in the political agenda, 2. Harmonization of national monitoring programs and
23 existing initiatives, 3. Integration and optimization of ecosystem models to improve process-level
24 understanding carbon and forest dynamics, 4. Development of a permanent plot field network to calibrate,
25 validate and combine multiscale sampling and monitoring methods. 5. Improvement of the understanding
26 of forest drivers and post-disturbance trajectories, 6. Inclusion of parameters related to forest fire drivers
27 and impacts in a monitoring program, 7. Evaluation of biodiversity and carbon values under a unified
28 strategy
29 Building an integrated monitoring framework requires adequate and long-term financing. Strong
30 efforts are needed to include it in the political agenda and stimulate the scientific collaboration
31 community and harmonize existing monitoring programmes. The development of such framework can be
32 separated into four main strategies: 1) integration and optimization of ecosystem models to improve
33 process-level understanding; 2) development of a permanent plot field network to calibrate, validate and

20
1 combine multiscale sampling and monitoring methods; 3) optimizing scaling up methods to extrapolate
2 estimates for larger scales; and 4) defining how a monitoring system will assist public policy actions.
3 Efficient monitoring systems must have the following characteristics: representative spatial
4 coverage, standard sampling, long-term, consistency, precision, calibration, openness/transparency, and
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good documentation. Many monitoring systems are designed for specific purposes (such as reporting for
specific variables) and, thus, include a limited number of variables or parameters. Harmonization will
7 require changes to monitoring programs and inventory systems, which might lead to resistance, due to
8 lack of funding or institutional barriers (Magnusson et al., 2013). At the country level, harmonizing
9 monitoring programs into a national system, instead of independent initiatives, would be helpful to
10 minimize such barriers. It is important to open up pathways to discuss future synergistic efforts (e.g.
11 biodiversity and other variables in field surveys, integrating field-based systems to remote sensing efforts,
12 opportunities and trade-offs for multi-taxa field surveys).
13 Important recommendations to foster new monitoring strategies to address to new environmental

14 and societal needs are a comprehensive survey of different ongoing initiatives (e.g. national forest
15 inventories), improvement of technical and scientific exchange to gather the information available and
16 definition of how to use them in the development of integrative approaches. In this context, developers
17 and end-users need to interact to establish clear guidelines for the development of reliable products.
18 Validation and calibration of monitoring systems are an essential part and should include an appropriate
19 and robust design (number of points, areas – including those with existing studies, cover all biomes) as
20 well as the verification of outputs of each model ensuring the quality and transparency of results.
21 The design of monitoring programs must also consider that in addition to capturing valuable
22 information, it is central to inform communities and social groups, and so encourage their qualified
23 participation in decision-making processes relating to the environment. Attributes to ensure the
24 effectiveness of monitoring programs include explicit articulation of how the monitoring will inform
25 environmental policies and programs, clear specification of thresholds that affect the implementation of
26 strategic interventions from monitoring programs and a precise quantification of the ability to achieve
27 early detection of changes being monitored.
28
29 Acknowledgments: This document is based on the discussions held during the Workshop on
30 Monitoring Forest Dynamics: carbon stocks, greenhouse gas fluxes and biodiversity, in Brasilia, Brazil
31 (September 2–4, 2014) financed by Climate Land Use Alliance. Susan Trumbore and Douglas Morton

21
1 acknowledge the financial support from the Science Without Borders Program (CNPq). Mercedes
2 Bustamante and Iris Roitman acknowledge the financial support of the Rede Clima of Brazilian Ministry
3 of Science, Technology and Innovation. J.B and E.B were supported by a grant from the NERC
4 (NE/K016431/1). The authors are grateful to Toby Gardner for valuable comments on previous version of
5 this paper. Author Manuscript
6 References
7 Achard F, Eva HD, Mayaux P, Stibig H-J, Belward A (2004) Improved estimates of net carbon emissions
8 from land cover change in the Tropics for the 1990’s. Global Biogeochemical Cycles, 18, GB2008.
9 Aguiar APD, Ometto JP, Nobre C et al. (2012) Modeling the spatial and temporal heterogeneity of
10 deforestation-driven carbon emissions: the INPE-EM framework applied to the Brazilian Amazon. Global
11 Change Biology,16, 3346–3366.
12 Aide TM, Clark ML, Grau HR, et al. (2013) Deforestation and reforestation of Latin America and the
13 Caribbean (2001-2010). Biotropica 45, 262-271
14 Aide TM, Corrada-Bravo C, Campos-Cerqueira M, Milan C, Veja G, Alvarez R (2013). Real-time

15 bioacoustics monitoring and automated species identification. PeerJ, 1,e103, doi: 10.7717/peerj.103.
16 Alencar A, Asner GP; Knapp G, Zarin D (2011) Temporal variability of forest fires in eastern Amazonia.
17 Ecological Applications, 21(7), 2397 – 2412.
18 Alencar A, Nepstad D, Diaz M del CV (2006) Forest understory fire in the Brazilian Amazon in ENSO
19 and non-ENSO years: area burned and committed carbon emissions. Earth Interactions, 10(6), 1–17.
20 Andersson K, Evans TP, Richards KR (2009) National forest carbon inventories: policy needs and
21 assessment capacity. Climatic Change, 93, 69–101.
22 Angelsen A, Brockhaus M, Sunderlin WD, Verchot LV (eds) ( 2012) Analysing REDD+:Challenges and
23 choices, CIFOR, Bogor, Indonesia.
24 Aragão LEOC, Malhi Y, Roman-Cuesta RM, Saatchi S, Anderson LO, Shimabukuro YE (2007) Spatial
25 patterns and fire response of recent Amazonian droughts. Geophysical Research Letters, 34, L07701.

22
1 Aragão LEOC, Poulter B, Barlow JS, Anderson LO, Malhi Y, Saatchi S, Phillips OL, Gloor E (2014)
2 Environmental change and the carbon. Balance of Amazonian forests. Biological Reviews, doi:
3 10.1111/brv.12088.
4 Aragão LEOC, Shimabukuro YE (2010) The Incidence of Fire in Amazonian Forests with Implications
Author Manuscript
5 for REDD. Science, 4(328), 5983:1275–1278.
6 Asner GP, Alencar A (2010) Drought impacts on the Amazon forest: the remote sensing perspective. New
7 Phytologist, 187, 569–578.
8 Asner, GP, Rudel TK, Aide M, Defries R, Emerson R (2009) A contemporary assessment of change in
9 humid tropical forests. Conservation Biology 23, 1386-1395.
10 Asner GP, Knapp DE, Broadbent EN, Oliveira PJC, Keller M, Silva JN (2005a) Selective logging in the
11 Brazilian Amazon. Science 310, 480–81.
12 Asner GP, Knapp DE, Cooper AN, Bustamante MMC, Olander LP (2005b) Ecosystem Structure
13 throughout the Brazilian Amazon from Landsat Observations and Automated Spectral Unmixing. Earth
14 Interactions, 9(7), 1–31.
15 Asner GP, Knapp DE, Martin RE et al. (2014) Targeted carbon conservation at national scales with high-
16 resolution monitoring. Proceedings of the National Academy of Sciences, 111(47), E5016–E5022.
17 Asner GP, Martin RE (2009) Airborne spectranomics: mapping canopy chemical and taxonomic diversity
18 in tropical Forests. Frontiers in Ecology and Environment, 7, doi:10.1890/07015
19 Asner GP, Martin RE, Anderson CB, Knapp DE (2015) Quantifying forest canopy traits: Imaging
20 spectroscopy versus field survey. Remote Sensing of Environment, 158, 15–27
21 Asner GP, Mascaro J, Anderson C et al. (2013) High-fidelity national carbon mapping for resource
22 management and REDD+. Carbon Balance and Management, 8(1), 7.
23 Asner GP, Powell GVN, Mascaro J et al. (2010) High-resolution forest carbon stocks and emissions in
24 the Amazon. Proceedings of the National Academy of Sciences of the United States of America, 107(38),
25 16738–16742.
26 Baccini A, Goetz SJ, Walker WS et al. (2012) Estimated carbon dioxide emissions from tropical
27 deforestation improved by carbon-density maps. Nature Climate Change, 2, 182–185.

23
1 Balch JK, Nepstad DC, Curran LM et al. (2011) Size, species, and fire behavior predict tree and liana
2 mortality from experimental burns in the Brazilian Amazon. Forest Ecology and Management, 261, 68–
3 77.
4 Barlow J, Peres C (2008) Fire-mediated dieback and compositional cascade in an Amazonian forest.
5 Author Manuscript
Philosophical Transactions of Royal Society of London B, 363(1498), 1787–1794.
6 Barlow J, Peres CA, Lagan BO, Haugaasen T (2003) Large tree mortality and the decline of forest
7 biomass following Amazonian wildfires. Ecology Letters, 6(1), 6–8.
8 Barlow J, Silveira JM, Cochrane MA (2010) Fire scars on Amazonian trees: exploring the cryptic fire
9 history of the Ilha de Maracá. Biotropica, 42(4), 405–409.
10 Benchimol M. & Peres CA (2015). Edge‐mediated compositional and functional decay of tree
11 assemblages in Amazonian forest islands after 26 years of isolation. Journal of Ecology 103, 408-420.
12 Berenguer E, Ferreira J, Gardner TA et al. (2014) A large-scale field assessment of carbon stocks in
13 human-modified tropical forests. Global Change Biology, 20(12), 3713–3726.
14 Blaser J, Sarre A, Poore D, Johnson S (2011) Status of tropical forest management 2011. ITTO Technical
15 Series No. 38. International Tropical Timber Organization, Yokohama, Japan.
16 Boyd DS, Danson FM (2005) Satellite remote sensing of forest resources: three decades of research.
17 Progress in Physical Geography, 29, 1–26.
18 Brando PM, Balch JK, Nepstad DC et al. (2014) Abrupt increases in Amazonian tree mortality due to
19 drought-fire interactions. Proceeding of the National Academy of Science USA, 111, 6347–6352.
20 Brando PM, Nepstad DC, Balch JK, Bolker B, Christman MC, Coe M, Putz FE (2012) Fire-induced tree
21 mortality in a neotropical forest: the roles of bark traits, tree size, wood density and fire Behaviour.
22 Global Change Biology, 18, 630–641.
23 Bunker, DE, Declerck F, Bradford JC, Colwell RK, Perfecto I., Phillips OL, Naeem S (2005) Species loss
24 and aboveground carbon storage in a tropical forest. Science, 310 (5750), 1029–1031.
25 Casarim FM, Walker SM, Swan SR, Sharma BD, Grais A, Stephen P (2103) Participatory Carbon
26 Monitoring: Operational Guidance for National REDD+ Carbon Accounting. SNV - The Netherlands
27 Development Organisation, REDD+ Programme, Ho Chi Minh City.

24
1 Chen Y, Morton DC, Jin Y et al. Long-term trends and interannual variability of forest, savanna and
2 agricultural fires in South America. Carbon Management, 4(6), 617–638.
3 Cochrane MA (2001) Synergistic Interactions between Habitat Fragmentation and Fire in Evergreen
4 Tropical Forests. Conservation Biology, 15, 1515–1521.
Author Manuscript
5 Cochrane MA, Schulze MD (1999) Fire as a recurrent event in tropical forests of the eastern Amazon:
6 effects on forest structure, biomass, and species composition. Biotropica, 31, 2–16.
7 Conti G, Díaz S (2013) Plant functional diversity and carbon storage: an empirical test in semi-arid forest
8 ecosystems. Journal of Ecology, 101(1), 18–28.
9 Convention on Biological Diversity (2011) REDD-plus and Biodiversity. Technical series no. 59.
10 Secretariat of the Convention on Biological Diversity, Montreal.
11 Costa FRC, Magnusson WE (2010) The need for large-scale, integrated studies of biodiversity. The
12 experience of the Program for Biodiversity Research in Brazilian Amazonia. Natureza & Conservação, 8,
13 1–5.
14 Daume S, Albert M, von Gadow K (2014) Forest monitoring and social media– Complementary data
15 sources for ecosystem surveillance? Forest. Ecology and Management, 316, 9–20.
16 de Mendonça MJC, Diaz MDV, Nepstad D, da Motta RS, Alencar A, Gomes JC, Ortiz RA (2004) The
17 economic cost of the use of fire in the Amazon. Ecological Economics, 49, 89–105.
18 DeFries R, Achard F, Brown C, Herold M, Murdiyarso D, Schlamadinger B, Souza C (2007) Earth

19 observations for estimating greenhouse gas emissions from deforestation in developing countries.
20 Environmental Science & Policy, 10, 385–394.
21 Díaz S, Hector A, Wardle DA (2009) Biodiversity in forest carbon sequestration initiatives: not just a side
22 benefit. Current Opinion in Environmental Sustainability, 1, 55–60.
23 Drusch M, Del Bello U, Carlier S et al. (2012) Sentinel-2: ESA's Optical High-Resolution Mission for
24 GMES Operational Services. Remote Sensing of Environment, 120, 25–36.
25 Espírito-Santo FDB, Gloor M, Keller M et al. (2014) Size and frequency of natural forest disturbances
26 and the Amazon forest carbon balance. Nature Communications, 5, 3434.
27 FAO (2006) Global forest resources assessment 2005: progress towards sustainable forest management.
28 Forestry Paper 147. United Nations Food and Agriculture Organization, Rome .

25
1 Frolking S, Palace M, Clark DB, Chambers JQ, Shugart HH, Hurtt GC (2009) Forest disturbance and
2 recovery - a general review in the context of space-borne remote sensing of impacts on aboveground
3 biomass and canopy structure. Journal of Geophysical Research, 114, G00E02.
4 Gardner TA, Barlow J, Araujo IS et al. (2008) The cost-effectiveness of biodiversity surveys in tropical
Author Manuscript
5 forests. Ecology Letters, 11, 139–150.
6 Gardner TA, Ferreira J, Barlow J et al. (2013) A social and ecological assessment of tropical land uses at
7 multiple scales: the sustainable Amazon network. Philosophical transactions of the Royal Society of
8 London B, 368(1619), 20120166.
9 Gardner, TA, Burgess ND, Aguilar-Amuchastegui N et al. (2012) A framework for integrating
10 biodiversity concerns into national REDD+ programmes. Biological Conservation, 154, 61–71.
11 Gatti L, Gloor G, Miller M et al. (2014) Drought sensitivity of Amazonian carbon balance revealed by
12 atmospheric measurements. Nature, 506, 76–80.
13 Gibbs HK, Brown S, Niles JO, Foley JA (2007) Monitoring and estimating tropical forest carbon stocks:
14 making REDD a reality. Environmental Research Letters, 2, 045023.
15 Gibson L, Lynam AJ, Bradshaw CJA et al. (2013) Near-Complete extinction of native small mammal
16 fauna 25 years after forest fragmentation. Science, 341(6153), 1508–1510.
17 Gilroy JJ, Woodcock P, Edwards FA et al. (2014) Cheap carbon and biodiversity co-benefits from forest
18 regeneration in a hotspot of endemism. Nature Climate Change, 4, 503–507.
19 Goetz AFH, Vane G, Solomon JE, Rock BN (1985) Imaging spectrometry for Earth remote sensing.
20 Science, 228, 1147–53.
21 Goetz S J, Baccini A, Laporte NT et al. (2009) Mapping and monitoring carbon stocks with satellite
22 observations: a comparison of methods. Carbon Balance and Management Review, 4, 2.
23 GOFC-GOLD, 2013. A sourcebook of methods and procedures for monitoring and reporting
24 anthropogenic greenhouse gas emissions and removals associated with deforestation, gains and losses of
25 carbon stocks in forests remaining forests, and forestation. GOFC-GOLD Report version COP19-1.
26 GOFC-GOLD Land Cover Project Office, Wageningen University, The Netherlands.

26
1 Griffiths HM, Louzada J, Bardgett RD, Beiroz W, França F, Tregidgo D, Barlow J. (2015) Biodiversity
2 and environmental context predict dung beetle mediated seed dispersal in a tropical forest field
3 experiment. Ecology 96, 1607–1619.
4 Grote R, Kiese R, Grünwald T, Ourcival J-M., Granier A (2011) Modelling forest carbon balances
Author Manuscript
5 considering tree mortality and removal. Agricultural and Forest Meterorology, 151(2), 179–190.
6 Harrison ME, Boonman A, Cheyne SM, Husson SJ, Marchant NC, Struebig MJ (2012) Biodiversity
7 monitoring protocols for REDD+: can a one-size-fits-all approach really work? Tropical Conservation
8 Science, 5(1), 1–11.
9 Haughland DL, Hero J-M, Schieck J et al. (2010) Planning forwards: biodiversity research and
10 monitoring systems for better management. Trends in Ecology and Evolution 25, 199–200.
11 Herold M, Román-Cuesta RM, Mollicone D et al. (2011) Options for monitoring and estimating historical
12 carbon emissions from forest degradation in the context of REDD+. Carbon Balance and Management, 6,
13 13.
14 Homolová L, Malenovský Z, Clevers JGPW, García-Santos G, Schaepman ME (2008). Review of

15 optical-based remote sensing for plant trait mapping. Ecological Complexity, 15, 1–16.
16 Houghton R A, Skole DL, Nobre CA, Hackler JL, Lawrence KT, Chomentowski WH (2000) Annual
17 fluxes of carbon from deforestation and regrowth in the Brazilian Amazon. Nature, 403, 301–304.
18 Houghton RA (2005) Aboveground Forest Biomass and the Global Carbon Balance. Global Change
19 Biology, 11, 945–958.
20 Houghton RA, Hall F, Goetz SJ (2009) Importance of biomass in the global carbon cycle. Journal of
21 Geophysical Research, 114, 1–13.
22 Houghton RA, Lawrence KT, Hackler JL, Brown S (2001) The spatial distribution of forest biomass in
23 the Brazilian Amazon: a comparison of estimates. Global Change Biology, 7, 731–746.
24 IPCC (2000) Methods for measuring and monitoring. Summary for policy makers. In: Land use, land-use
25 change and forestry (eds Watson RT, Noble IR, Bolin B, Ravindranath NH, Verardo DJ, Dokken J, pp
26 375, Cambridge University Press, Cambridge.
27 IPCC (2014) Summary for Policymakers. In: Climate Change 2014, Mitigation of Climate Change.
28 Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on

27
1 Climate Change (eds Edenhofer O, Pichs-Madruga R, Sokona Y. et al.) Cambridge University Press,
2 Cambridge.
3 IPCC 2003. Definitions and Methodological Options to Inventory Emissions from Direct Human-induced
4 Degradation of Forests and Devegetation of Other Vegetation Types (eds Penman J, Gytarsky M,
Author Manuscript
5 Hiraishi T et al.), Institute for Global Environmental Strategies, Japan.
6 Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as
7 bioindicators. Endangered Species Research, 8, 93–115.
8 Lambin EF (1999) Monitoring forest degradation in tropical regions by remote sensing: some
9 methodological issues. Global Ecology and Biogeography, 8, 191–198.
10 Laurance WF, Camargo JLC, Luizão RCC et al. (2011) The fate of Amazonian forest fragments: A 32-
11 year investigation. Biological Conservation, 144, 56–67.
12 Laurance WF, Nascimento HEM, Laurance SG et al. (2006) Rapid decay of tree-community composition
13 in Amazonian forest fragments. Proceedings of the National Academy of Sciences of the United States of
14 America, 103(50), 19010–19014.
15 Leal CG (2015) Multiscale anthropogenic impacts on stream condition and fish assemblages in
16 Amazonian landscapes. PhD Thesis, Dual PhD Universidade Federal de Lavras, Brazil, and Lancaster
17 University, United Kingdom.
18 Lewis SL, Lopez-Gonzalez G, Sonk B et al. (2009) Increasing carbon storage in intact African tropical
19 forests. Nature, 457,1003–1007.
20 Lima RF, Olmos F, Dallimer M, Atkinson PW, Barlow J (2013) Can REDD+ Help the Conservation of
21 Restricted-Range Island Species? Insights from the Endemism Hotspot of São Tomé. PLoS ONE, 8(9),
22 e74148.
23 Magnusson W, Braga-Neto R, Pezzini F et al. (2013) Biodiversity and Integrated Environmental

24 Monitoring. Áttema Editorial. Manaus, Brazil.
25 Magnusson WE (2014) Uncertainty and the design of in-situ biodiversity-monitoring programs. Nature
26 Conservation, 8, 77–94.

28
1 Marvin DC, Asner GP, Knapp DE, Anderson CB, Martin RE, Sinca F, Tupayachi R (2014) Amazonian
2 landscapes and the bias in field studies of forest structure and biomass. Proceedings of the National
3 Academy of Science of the United States, 111, E5224–E5232.
4 Mascaro J, Asner GP, Davies S, Dehgan A, Saatchi S (2014) These are the days of lasers in the jungle.
5 Author Manuscript
Carbon Balance and Management, 9,7.
6 Matricardi EAT, Skole DL, Pedlowski MA, Chomentowski W, Fernandes LC (2010) Assessment of
7 tropical forest degradation by selective logging and fire using Landsat imagery. Remote Sensing of
8 Environment, 114, 1117–1129.
9 Mitchard, ETA, Feldpausch TR, Brienen RJW et al. (2014) Markedly Divergent Estimates of Amazon
10 Forest Carbon Density from Ground Plots and Satellites. Global Ecology and Biogeography, 23(8), 935–
11 946.
12 Morales-Barquero L, Skutsch M, Jardel-Peláez EJ, Ghilardi A, Kleinn C, Healey JR (2014)

13 Operationalizing the Definition of Forest Degradation for REDD+, with Application to Mexico. Forests,
14 5, 1653–1681.
15 Moran S, Pantidi N, Rodden T et al. (2014) Listening to the Forest and its Curators: Lessons Learnt from
16 a Bioacoustic Smartphone Application Deployment. In: Proceeding CHI 14 Proceedings of the SIGCHI
17 Conference on Human Factors in Computing Systems, pp2387-2396, ACM New York,
18 Morton DC, DeFries RS, Nagol J, Souza Jr CM, Kasischke ES, Hurtt GC, Dubayah R (2011) Mapping
19 canopy damage from understory fires in Amazon forests using annual time series of Landsat and MODIS
20 data, Remote Sensing of Environment, 115(7), 1706–1720.
21 Morton DC, Le Page Y, DeFries R, Collatz GJ, Hurtt GC (2013) Understorey fire frequency and the fate
22 of burned forests in southern Amazonia. Philosophical Transactions of the Royal Society B, 368,
23 20120163.
24 Moura NG, Lees AC, Andretti CB et al. (2013) Avian biodiversity in multiple-use landscapes of the
25 Brazilian Amazon. Biological Conservation, 167, 339–348.
26 Nabuurs GJ, Masera O, Andrasko K. et al. (2007) Forestry. In: Climate Change 2007: Mitigation.
27 Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental Panel on
28 Climate Change (eds Metz B, Davidson OR, Bosch PR, Dave R, Meyer LA), Cambridge University
29 Press, Cambridge.

29
1 Negra C (2010) Roadmap for Terrestrial Carbon Science - Research Needs for Carbon Management in
2 Agriculture, Forestry and Other Land Uses. Terrestrial Carbon Group.
3 Negrón-Juárez RI, Chambers JQ, Guimaraes G et al. (2010) Widespread Amazon forest tree mortality
4 from a single cross-basin squall line event. Geophysical Research Letters, 37, n/a–n/a,
Author Manuscript
5 doi:10.1029/2010GL043733.
6 Nepstad DC, Moutinho P, Markewitz RS (2001) The recovery of biomass, nutrient stocks, and deep-soil
7 functions in secondary forests. In: The Biogeochemistry of the Amazon Basin (eds McClain ME, Victoria
8 RL, Richey JE), pp. 139 –155, Oxford University Press, New York.
9 Nepstad DC, Veríssimo A, Alencar A et al. (1999) Large-scale impoverishment of Amazonian forests by
10 logging and fire. Nature, 398, 505–508.
11 O'Brien TG, Baillie JEM, Krueger L, Cuke M (2010) The Wildlife Picture Index: monitoring top trophic
12 levels. Animal Conservation, 13:335–343.
13 Oliveiras I, Anderson LO, Malhi Y (2014) Application of remote sensing to understanding fire regimes
14 and biomass burning emissions of Tropical Andes. Biogeochemical Cycles, 28, 480–496.
15 Ometto JP, Aguiar AP, Assis T et al. (2014) Amazon forest biomass density maps: tackling the uncertainty
16 in carbon emission estimates. Climatic Change, 124(3), 545–560.
17 Pan Y, Birdsey RA, Fang J et al. (2011) A Large and Persistent Carbon Sink in the World’s Forests.
18 Science, 333, 988–993.
19 Parrotta JA, Wildburger C, Mansourian S (2012) Understanding relationships between biodiversity ,

20 carbon , forests and people: the key to achieving REDD+ objectives. A global assessment report.
21 International Union of Forest Research Organizations (IUFRO), Vienna, Austria.
22 Pelletier J., Ramankutty N, Potvin C (2011) Diagnosing the uncertainty and detectability of emission
23 reductions for REDD+ under current capabilities: an example for Panama. Environmental Research
24 Letters, 6, 024005.
25 Pereira HM, Ferrier S, Walters M et al. (2013) Essential Biodiversity Variables. Science 339, 277–278.
26 Pereira R, Zweede J, Asner GP, Keller M (2002) Forest canopy damage and recovery in reduced-impact
27 and conventional selective logging in eastern Para, Brazil. Forest Ecology and Management, 168(1-3),
28 77–89.

30
1 Peres CA, Palacios E (2007) Basin-wide effects of game harvest on vertebrate population densities in
2 Amazonian forests: implications for animal-mediated seed dispersal. Biotropica, 39(3), 304–315.
3 Peres CA, Barlow J, Laurance W (2006) Detecting anthropogenic disturbance in tropical forests. Trends
4 in Ecology and Evolution, 21, 227–229.
Author Manuscript
5 Perz SG & Skoleb DL (2003) Social determinants of secondary forests in the Brazilian Amazon. Social
6 Science Research, 32(1), 25–60.
7 Perz SG, Shenkin A, Barnes G, Cabrera L, Carvalho LA, Castillo J (2011) Connectivity and resilience: a
8 multidimensional analysis of infrastructure impacts in the southwestern Amazon. Social Indicators
9 Research , 106(2): 259–285.
10 Pettorelli N, Vika JO, Mysterud A, Gaillard J, Tucker CJ, Stenseth NC (2005) Using the satellite-derived
11 NDVI to assess ecological responses to environmental change. Trends in Ecology and Evolution, 20(9),
12 503–510.
13 Pijanowski BC, Villanueva-Rivera LJ, Dumyahn SL, Farina A, Krause BL, Napoletano BM, Gage SH,
14 Pieretti N (2011) Soundscape ecology: the science of sound in the landscape. BioScience, 61, 203–216.
15 Plugge D, Köhl M (2012) Estimating carbon emissions from forest degradation: implications of
16 uncertainties and area sizes for a REDD+ MRV system. Canadian Journal of Forert Research, 42, 1996–
17 2010.
18 Putz FE, Zuidema PA, Synnott T et al. (2012) Sustaining conservation values in selectively logged
19 tropical forests: the attained and the attainable. Conservation letters, 5(4), 296–303.
20 Roy DP, Wulder MA, Loveland TR et al. (2014) Landsat-8: Science and product vision for terrestrial
21 global change research. Remote Sensing of Environment, 145, 154–172.
22 Saatchi S, Mascaro M, Xu L et al. (2014) Seeing the forest beyond the trees. Global Ecology and
23 Biogeography, doi: 10.1111/geb.12256.
24 Saatchi SS, Harris NL, Brown S et al. (2011) Benchmark map of forest carbon stocks in tropical regions
25 across three continents. Proceedings of the National Academy of Sciences of the United States of
26 America, 108(24), 9899–9904.

31
1 Schimel DS, Asner GP, Moorcroft P (2013) Observing changing ecological diversity in the
2 Anthropocene. Frontiers in Ecology and the Environment, 11,129–137.
3 Schulze, E. D. (2014). Large-scale biogeochemical research with particular reference to forest
4 ecosystems, an overview. Forest Ecology and Management, 316, 3–8.
5
Author Manuscript
Seidl R, Fernandes PM, Fonsecad TF et al. (2011) Modelling natural disturbances in forest ecosystems: a
6 review Ecological Modelling, 222, 903–924.
7 Silveira JM, Barlow J, Andrade RB et al. (2013). The responses of leaf litter ant communities to wildfires
8 in the Brazilian Amazon: a multi-region assessment. Biodiversity and Conservation, 22(2), 513–529.
9 Silvério DV, Brando PM, Balch JK., Putz FE, Nepstad DC., Oliveira-Santos C, Bustamante MMC
10 (2013). Testing the Amazon savannization hypothesis : fire effects on invasion of a neotropical forest by
11 native cerrado and exotic pasture grasses. Philosophical Transactions of the Royal Society of London B,
12 368, doi:10.1098/rstb.2012.0427.
13 Sist P, Rutishauser E, Peña-Claros M et al. (2015) The Tropical managed Forests Observatory: a research
14 network addressing the future of tropical logged forests. Applied Vegetation Science. Applied Vegetation
15 Science, 18(1), 171–174.
16 Smith P, Bustamante M, Ahammad H et al. (2014) Agriculture, Forestry and Other Land Use (AFOLU).
17 In: Climate Change 2014: Mitigation of Climate Change. Contribution of Working Group III to the Fifth
18 Assessment Report of the Intergovernmental Panel on Climate Change (eds Edenhofer O., Pichs-Madruga
19 R, Sokona Y et al.), Cambridge University Press, Cambridge.
20 Souza CM, Roberts DA, Cochrane MA (2005) Combining spectral and spatial information to map canopy
21 damage from selective logging and forest fires. Remote sensing of the environment, 98, 329–343.
22 Strassburg BBN, Kelly A, Balmford A et al. (2010) Global congruence of carbon storage and biodiversity
23 in terrestrial ecosystems. Conservation Letters, 3, 98–105.
24 Tavani R, Saket M, Piazza M, Branthomme A, Altrell D (2009) Case studies on measuring and
25 monitoring forest degradation through national forest monitoring assessment. Forest Resource
26 Assessment Working Paper 172, FAO, Rome.
27 Thompson I, Mackey B, McNulty S, Mosseler A. (2009) Forest Resilience, Biodiversity, and Climate
28 Change. A synthesis of the biodiversity/resilience/ stability relationship in forest ecosystems. Technical
29 Series no. 43. Secretariat of the Convention on Biological Diversity, Montreal.

32
1 Turner W, Spector S, Gardiner N, Fladeland M, Sterling E., Steininger M (2003) Remote sensing for
2 biodiversity science and conservation. Trends Ecology and Evolution, 18, 306–314.
3 UNFCCC (2011) Report of the Conference of the Parties on its sixteenth session , held in Cancun from 29
4 November to 10 December 2010. Part one: Proceedings. United Nations Framework Convention for
Author Manuscript
5 Climate Change. Conference of the Parties, Cancun, Mexico,
6 Waldon J, Miller BW, Miller CM (2011) A model biodiversity monitoring protocol for REDD projects.
7 Tropical Conservation Science , 4(3), 254–260.
8 Walker R, Arima E, Messina J et al. (2013) Modeling spatial decisions with graph theory: logging roads
9 and forest fragmentation in the Brazilian Amazon. Ecological Applications, 23, 239–254.
10 Wertz-Kanounnikoff S (2008) Estimating the costs of reducing forest emissions. A review of methods.
11 Working Paper No. 42. Center for International Forestry Research (CIFOR), Bogor, Indonesia.
12 Wirth C, Schumacher J, Schulze E-D (2004) Generic biomass functions for Norway spruce in Central
13 Europe – a meta-analysis approach toward prediction and uncertainty estimates. Tree Physiology, 24,
14 121–139.
15 Wright SJ (2013) The carbon sink in intact tropical forests. Global Change Biology, 19, 337–339.
16 Yang CY, Morton DC, Jin Y, et al. (2013) Long-term trends and interannual variability of forest, savanna
17 and agricultural fires in South America. Carbon Management, 4(6), 617–638.
18
19
20 List of figures
21 Figure 1. Possible trajectories of forests under different levels of disturbance (intensity, frequency and
22 extent). Blue arrows represent disturbances and green arrows indicate regrowth of forests.
23
24 Figure 2. Relationship between accuracy and costs and time of measuring forest carbon stocks and
25 biodiversity.
26

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Figure 4. Spatially-based, multi-scale integrative framework for monitoring and modeling carbon stocks
Figure 3. Spatial scale and temporal resolution of different methods for monitoring forest carbon stocks

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and biodiversity.
and biodiversity.
1
2
4
5
Table 1. Key sources of uncertainty and their associated difference with the Reference Level
for REDD+. From: Pelletier et al. (2011).
Sources of error % Explanation

Mature forest C density 54.5 No standardized methodology and error-prone allometric
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Deforested area 2.2-19.1
equations or biomass emission factors
Error in land-cover classification / Lack of classification
accuracy assessment
Snapshot effect 19.3 Long time interval between two maps / Lack of knowledge
on land-cover dynamics
Land-cover map quality 15.6 – 35.2 Map based on a mosaic of satellite image from very
different years
(9 yr and 8 yr)
Low availability of useable satellite imagery (cloud cover,
long revisiting time, seasonality)
Coarse-resolution imagery (e.g. MODIS or AVHRR) with

more frequent revisit times would not produce accurate
estimates of deforestation
Lack of receiving station for Central America and Central

Africa
Fallow C density 22.4 Lack of data availability for fallow land
Likely to affect countries where fallow occupies a

significant fraction of the territory

Table 2: Components of a fire monitoring system associated to current capabilities
and future needs of research and development.
Current Capabilities Gaps/future needs

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Forecast NASA/UCI (SST)
INPE- Fire Danger Forecast
Short-term forecast (1 week) data
integration w/weather forecast
(South America) -Economic forecast
-Fragmentation, landscape-level
risk for fire spread
-Characterization of fire regime
(expected frequency, seasonality,
intensity, etc.)
Active Fires INPE – Monitoring of -Limited ~1km late afternoon
vegetation fires coverage
-Small fires
-Algorithms for understory fires
Burned Area NASA (MODIS): MCD64A1, -Attribution (separate by land

MCD45, Understory (250m) cover and process)
INPE, DEGRAD, -Agricultural fires, Pasture
PanAmazonia burning, deforestation process,
connecting BA to legal/permitted
fires,
-Higher resolution mapping,
-Routine mapping of understory
fires, validation/omission
Emissions GFED4 *Spatiotemporal variability in
INPE-GMAI (Group combustion completeness,
Modeling of the Atmosphere mortality; *trace gas emissions
and its Interfaces) (South ratios and their diurnal/seasonal
America) variability),
NASA-QFED *fire duration (e.g., smoldering),
*fire return interval (fuel loads),
*validation (MOPITT, OCO-2,
NO2, airborne, in situ, and tower),
*resolution,
*missing fire types
Post-fire recovery and -Tanguro Fire Experiment- Chronosequence of fire ages,
impacts IPAM (Brazil) intensities; post-fire mortality,

-INPE/Embrapa (Amazonian biodiversity (phylogenetic and
states, Brazil) functional diversity, too)
-IBAMA, PPCerrado
-LiDAR-Embrapa Socioeconomic impacts (public
-Cerrado Fire Experiment- health, transportation, etc.)
Author Manuscript UNB, USP (Brazil)
-RR—Embrapa
Ecological impacts
-IPEA/IPAM
(Socioeconomic, health)
-Global Canopy Program
(2005, Socioeconomic/health)

Table 3: Summary of research priorities and practical recommendations to help
achieve an integrated framework.
Mobilization of stakeholders and scientific community to include an integrated

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framework in the political agenda.
a) Define objective-oriented research efforts (problem and goals) in an integrated

framework.
b) Survey institutions, researchers, and ongoing research projects to capitalize on
proven monitoring strategies and accompany testing of new, state-of-the-art
methods.
c) Solicit input through workshops of experts and stakeholders to hone the design
of multi-purpose monitoring programs, with careful attention to implementation
networks at national, regional, and local scales.
d) Secure funding for long-term monitoring efforts, based on key products and
outcomes of the integrated framework.
e) Develop specific proposals and defining possible products and outcomes.
f) Establish a program within the network that can be integrated with other
objectives and goals.
g) Establish a national-level, long-term program involving different government
levels, research institutions and international cooperation.
h) Include explicit articulation of how the monitoring programs will inform
environmental policies.
i) Specify thresholds that should guide the implementation of strategic
interventions from monitoring programs (periodic reviews of protocols and
achievements)
j) Foster local capacity and integrate monitoring efforts with local institutions and
communities in order to inform and encourage communities and social groups to
participate in decision-making processes related to the environment.
Harmonization of national monitoring programs and existing initiatives
a) Make a comprehensive survey of different ongoing initiatives.

b) Improve technical and scientific exchange to gather and process information for
integrative approaches.

c) Promote the interaction of developers and end-users of monitoring programs to
establish clear guidelines for the development of monitoring systems and their
products.
d) Promote free data access by data use policy.
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Integration and optimization of ecosystem models to improve process-level
understanding carbon and forest dynamics.
a) Identify primary modelling research needs: which models are needed and which
data are required to parameterize, calibrate and validate models.
b) Promote combined efforts for model development/validation, especially toward
exploring how to best apply data assimilation.
c) Integrate ecosystem models on a spatially explicit basis with monitoring systems.
d) Use taxonomic data from installed permanent plots to support functional-trait
based approaches.
e) Determine traits that could be extracted from new data streams (e.g. LiDAR,
hyperspectral data).
Development of a permanent plot field network to calibrate, validate and
combine multiscale sampling and monitoring methods.
a) Survey of existing permanent plot networks and important information to build

upon existing initiatives, such as spatial location of plots, network objectives,
variables, sampling methods, frequency, institutions, publications, etc.
b) Use remote sensing and ancillary data to help select strategic areas and stratify
areas of interest, such as degraded forests, according to research and modelling
needs, knowledge gaps, and regional differences.
c) Select areas and plots for multiple purpose field surveys (forest structure, soil,
social and economic data, landscape, etc.), and for validation of airborne and
satellite remote sensing.
d) Integrate airborne and satellite campaigns on selected plots for calibration and
validation.
Improvement of the understanding of forest drivers and post-disturbance
trajectories
a) Identification, quantification, and monitoring of forests undergoing deforestation,

degradation, and recovery.

b) Develop a spatially explicit map of secondary forest and their turnover, plant and
faunal diversity, and nutrient availability.
c) Evaluate appropriate time intervals for temporal reassessments needed to examine
recovery and resilience of forests.
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d) Make wall-to-wall assessments and temporal reassessments, using appropriate time
intervals to study forest recovery and resilience.
e) Include socioeconomic drivers of land use trajectories to dynamic ecosystem
models.
f) Determine how climatic and soil parameters and landscape disturbance affect post
disturbance dynamics.
g) Quantify combined effects of different drivers of forest degradation, such as effects
of drought and understory fires on forest degradation and dynamics.
h) Determine the impacts of unplanned logging operations as a degradation vector.
Inclusion of parameters related to forest fire drivers and impacts in a monitoring
program
a) Improve validation (active fires, burned area, emissions ratios, fire effects - short
and long term) and
b) Include risk of fire parameters (climate and topography, forest structure and
available fuel material, socio-economic drivers) and fire regimes (seasonality,
frequency, human-dominated fire regimes).
c) Determine associated emissions: carbon, trace gases, aerosols; committed vs. net
emissions.
d) Assess ecosystem impacts: burned area and severity, mortality, post-fire
succession, recovery.
Evaluation of biodiversity and carbon values under a unified strategy
a) Determine opportunities and trade-offs for multi-taxa field surveys.

b) Establish a common framework based on a tiered approach, where the distribution
of threats to biodiversity and the correspondent responses could be monitored
simultaneously to carbon.
c) Integrate carbon accounting, socio-cultural/socio-economic impacts, and
biodiversity outcomes.

(forest cover < 10%)
high
low
Non-forest
Disturbance (frequency, intensity and extent)

Carbon, biodiversity and ecosystem services
Degraded forest
gcb_13087_f1.pdf

Secondary forest
Disturbed forest
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Mature forest
low
high
Biodiversity estimation
Biomass estimation
gcb_13087_f2.pdf

Cost and time of field sampling
high
Low
Uncertainty
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gcb_13087_f3.pdf
high Accuracy low
Fine
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(30-60 mins) satellite
optical
hyperspectral
radar
Temporal resolution
lidar
airborne
optical
radar
lidar
field
camera traps
acoustic recording
national forest inventories
biodivesity and other surveys
Coarse
(1-5 yrs)
Regional
Local Global
Fine Spatial scale (coverage) and resolution Coarse
(individual tree) (0.25° - 1°)

gcb_13087_f4.pdf
Data gathering
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Remote sensing
optical
Multi-scale data integration
land-use classes
Carbon-ecosystem monitoring system
carbon: activity data and emission factors
Calibration, validation, scaling up
canopy height forest productivity (C assimilation rate)

radar
lidar volume biodiversity and ecosystem functions
hyperspectral functional traits

canopy species Ecosystem models
Field-based Disturbance-response dynamics
species and volume
forest inventories wood density Climate change models
Local, regional, and global models
soil sampling soil carbon
soil fertility
biodiversity surveys Public policies
functional diversity
Environment and climate mitigation
other site surveys physiographic and Food security
socioeconomic data Forest management
Level of developement
Natural ecosystems high
medium
low

Corresponding Author Email-Id: Mercedes@unb - BR: Version of Record Doi: 10.1111/gcb.13087

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1

2 Received Date : 11-Apr-2015

3 Revised Date : 23-Jul-2015

5 Article type : Research Review

9 Corresponding author email-id: mercedes@unb.br

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7 Important consequences of deforestation and forest degradation include decreases in

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32 Evaluating changes in forests: combination of field inventories and remote sensing

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1 understood than in other vegetation types (grasslands/drylands, wetlands/peatlands) (Negra, 2010),

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17 Despite the recent quantification of fire-affected areas by remote-sensing data, current

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1 It is also important to consider that synergisms among simultaneous disturbance vectors

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3 Monitoring carbon and biodiversity – need for a unified strategy

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28 Forest inventories and eddy-covariance measurements contribute to sustainability assessments as

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25 Research priorities for forest monitoring systems

26 The determination of ecosystem carbon balances is a major issue in environmental research.

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11 A way forward to an integrated framework

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13 Important recommendations to foster new monitoring strategies to address to new environmental

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14 Aide TM, Corrada-Bravo C, Campos-Cerqueira M, Milan C, Veja G, Alvarez R (2013). Real-time

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18 DeFries R, Achard F, Brown C, Herold M, Murdiyarso D, Schlamadinger B, Souza C (2007) Earth

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14 Homolová L, Malenovský Z, Clevers JGPW, García-Santos G, Schaepman ME (2008). Review of

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23 Magnusson W, Braga-Neto R, Pezzini F et al. (2013) Biodiversity and Integrated Environmental

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12 Morales-Barquero L, Skutsch M, Jardel-Peláez EJ, Ghilardi A, Kleinn C, Healey JR (2014)

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19 Parrotta JA, Wildburger C, Mansourian S (2012) Understanding relationships between biodiversity ,

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Sources of error % Explanation

Coarse-resolution imagery (e.g. MODIS or AVHRR) with

Lack of receiving station for Central America and Central

Likely to affect countries where fallow occupies a

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Current Capabilities Gaps/future needs

Burned Area NASA (MODIS): MCD64A1, -Attribution (separate by land

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