Forest Ecology and Management 462 (2020) 117972

Contents lists available at ScienceDirect

Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Brazil’s forest restoration, biomass and carbon stocks: A critical review of T

the knowledge gaps
Fernando Ravanini Gardona, , Rozely Ferreira dos Santosa, , Ricardo Ribeiro Rodriguesb
⁎ ⁎

a
Department of Ecology, Institute of Biosciences, University of São Paulo, Rua do Matão, Travessa 14, 321, Cidade Universitária, São Paulo CEP: 05508-900, Brazil
b
Laboratory of Forest Ecology and Restoration, Department of Biological Sciences, University of São Paulo, Escola Superior de Agricultura “Luiz de Queiroz”, Av. Pádua
Dias, 11, CEP 13418-900, P.O. Box 9, Piracicaba, São Paulo, Brazil

1. Introduction theoretic-methodological scientific knowledge for generalizations of the

biomass stock in restored forests throughout the Brazilian territory.
Globally, tropical forests have been regarded as diversity pools and
carbon sinks, and its conservation plays an important role in the context 2. Methods
of climate change mitigation (IPCC, 2005; Chazdon et al. 2016; Poorter
et al. 2016). Estimates suggest that forests store up to 80% of terrestrial 2.1. Studies searches and selection
carbon (Houghton, 2008), and throughout tropical regions, forest re-
storation has become a conservation tool to reestablish ecological We conducted a systematic and integrative review to search for
processes as biomass and carbon accumulation, and the delivery of biomass or carbon evaluations conducted in Brazilian Passive
regulating ecosystem services, as reducing the effects of climate change Restoration (PR) and Active Restoration (AR) sites. A systematic qua-
(Chazdon, 2008; Locatelli et al. 2015; Meli et al. 2017). litative and quantitative literature review is a robust and replicable
The potential of restored forests in sequestering atmospheric carbon method, based on a comprehensive and detailed search strategy, able to
is closely attained to ecological aspects, as forest type, restoration identify boundaries around generalizations and important geographic,
method and management, landscape context, and environmental con- scalar, theoretical and methodological gaps in the literature (Pickering
ditions (Chazdon, 2014; Chazdon et al. 2016; Crouzeilles et al. 2017; and Byrne, 2014; Torraco, 2016). We compiled information related to
James et al. 2018). Despite the particular biotic and abiotic features of the geographic distribution of the studies, the methods used to estimate
each restoration, restoring forests by any method (planting seedlings or AGB/carbon stocks, existing bias in the researches, the main factors
assisting natural regeneration) drives to a local increment in biomass influencing AGB/carbon recovery, and trends and limitations of the
and carbon stocks (Benini and Adeodato, 2017). Since biomass accu- researches carried out in Brazil. We selected only scientific studies
mulation can be the main driver of plant community changes during available in indexed bibliographic databases and published in English
tropical forest succession (Lohbeck et al. 2015), and forest restoration is or Portuguese.
a global strategy for climate change mitigation, ensuring the re- The searches were performed in Scopus and Web of Science data-
establishment of this ecological processes could afford both restoration bases for all years available, with the last view on October 2019. We
success and vital regulating ecosystem services. selected the search terms to account for studies that evaluated AGB/
In Brazil, country which holds the second largest amount of natural carbon stocks in restoration sites implemented by active (planting
forest in the globe (SFB, 2013), many restoration projects have been seedlings and seeding) and passive (natural regeneration and assisted
implemented due to the legal obligation imposed by the Forest Code regeneration) restoration methods in Brazil. The selected terms were
(Federal Law, 12.651), and this activity became a potential agribusiness forest* (ecosystem), regrowth OR regener* OR restor* OR recover* OR
productive chain instead of just a visionary and romantic concern reforest* OR reveget* (processes involved in the ecosystem recovery),
(Benini and Adeodato, 2017). Thus, a robust scientific knowledge re- biomass OR carbon (targeted ecological process), and Brazil (studies
lated to biomass accumulation in forest restoration is expected to sup- geographic distribution). As Wortley et al. (2013), the terms “reclama-
port robust evaluations of the real contribution of these systems to tion” or “rehabilitation” were not included, in order to focus on studies
carbon ecosystem services (Van der Gaast et al. 2018). that were in line with the Society for Ecological Restoration (SER) defi-
In this context, we aimed to conduct a systematic review in the field nition of ecological restoration. Besides that, standardization of re-
of aboveground biomass recovery and carbon sequestration by forest storation terms still in process (McDonald et al. 2016), and, for this
restorations in Brazil. We highlight the limitations of the accumulated reason, terms as “reforestation” and “recovery” were also included to

⁎
Corresponding authors.
E-mail addresses: [email protected] (F.R. Gardon), [email protected] (R.F.d. Santos), [email protected] (R.R. Rodrigues).

https://doi.org/10.1016/j.foreco.2020.117972
Received 1 November 2019; Received in revised form 13 January 2020; Accepted 5 February 2020
Available online 17 February 2020
0378-1127/ © 2020 Elsevier B.V. All rights reserved.
F.R. Gardon, et al. Forest Ecology and Management 462 (2020) 117972

account for more published studies. Because we used the query “forest”,
we highlight that our results are representative of the Brazilian forest

Landscape; Forest attributes; Restoration implementation;

formations embedded in Amazon, Atlantic Forest, Caatinga (Tropical
Dry Forest) and Cerrado (Savanna) biomes.

AGB etimate; Past land-use; Soil properties; Plant

We refined the search by identifying the studies that addressed the
following criteria: (i) studies carried out exclusively in the Brazilian
territory; (ii) empirical studies, field surveys of observational data

Factors of influence on AGB recovery

(excluding reviews, meta-analyses, perspectives, modeling, GIS assess-
ments, and scenarios papers); (iii) studies that directly or indirectly
estimated biomass or carbon in restoration sites; (iv) studies conducted
in areas previously forested, where native vegetation was removed for
human interventions (agriculture, pasture, clear-cut, etc.) and then

interaction; Climate
naturally regenerated or restored by other methods; and (v) excluded
areas of selective logging, assessment of gap dynamics, studies con-
ducted in greenhouses, experimental sites, commercial plantations,
monocultures, and agroforestry.
We selected only the studies that evaluated live and/or dead AGB
and/or carbon (i.e. litterfall and plants aerial parts). We decided to

plants); AGB or carbon equation; Plot size and total area sampled/site;
restrict our study to aboveground stock because most of the below-

Criteria of plant individuals’ inclusion (minimum diameter or height);

Life-forms evaluated (e.g. trees, shrubs, palms, lianas, and herbaceous
ground (soil) studies found did not included roots contribution, but soil
carbon contents and microbial biomass. For this reason, we kept our
review aligned with aboveground compartments, since plants structures
were not the main target of belowground biomass studies.

2.2. Studies classification

Wood specific gravity and carbon factor usage

Studies included in the final list were classified within criteria en-
closed in Table 1.
The geographic position of all sites sampled in the selected studies
was mapped to the most detailed scale provided in the article (co-
ordinates, locality, municipality, state). Where it was possible to iden-
tify the same site in more than one article it was mapped once, thus we
Evaluation methods

found 35 replicated sites. The biome was determined based on the

Brazilian Biomes Map provided by the Brazilian Institute of Geography
and Statistics (IBGE 2004) in 1:5 000 000 scale. All mapping procedures
were conducted in QGIS (Version 3.4.12). Past land-use was determined
only if the information contained in the article was local, not the sur-
roundings. Some articles defined thresholds in the plant individuals’
size (diameter and height) to be included in their database, and we
Restoration age; Restoration method (passive

obtained this information for all articles. We defined as passive re-

Location; Forest Biome; n° areas evaluated;

storations sites areas where forest was cleared, used or not for human
activities, and then abandoned for natural regeneration recovery, that
is, secondary forests. On the other hand, active restorations were de-
fined as sites previously forested, used or not for human activities, but
recovered by human interventions, as planting seedlings and direct
seeding.
active); Past land-use
Site information

2.3. Aboveground biomass temporal analysis

We extracted the AGB/carbon values and age of the restoration sites

Categories and subcategories of studies classification.

from the texts, tables, and figures available in the selected publications.
We included in the analyses AGB values obtained by the use of allo-
metric and volume equations or destructive methods to estimate the
publication; Author’s institutions
Year of publication; Journal of

AGB stored in the plant individuals. We only attained information from

restorations of age < 30y, since this is the most common age class of
the restoration sites found among the studies (> 90%).
Due to the impossibility in determining the exact age or AGB stock
Publication detail

for some of the restorations sites studied in the articles, the data set is
composed of individual and grouped (average age or AGB) values.
Thus, we obtained both AGB and age for 177 events. Data presented as
carbon values were converted to biomass by the carbon conversion
factor given in the particular study.
Because AGB recovery over time is a non-linear process and is ex-
Subcategory

pected to be different among restoration methods (Holl and Zahawi,

Table 1

2014), we estimate sites’ AGB stocks (MgAGB.ha−1) as a function of age

ensuring an asymptotical shape in the AGB accumulation pattern. We

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F.R. Gardon, et al. Forest Ecology and Management 462 (2020) 117972

Fig. 1. Publications per year evidencing a 10y gap of published studies and the year that each biome was first evaluated.

built second-degree individual polynomial models for each restoration

method (passive and active). The quality of the model was evaluated
based on the adjusted R squared (R2), residuals standard error (RSE),
and F-statistics (p-value).
All data and graphics were manipulated using R 3.5.1 (R Core Team
2017).

3. Results

3.1. Publication’s details

We found 843 studies, whose 792 studies that did not match the
adopted criteria of inclusion were removed and 51 studies that eval-
uated aboveground biomass and/or carbon stocks in AR and PR sites in
Brazil were retained (Fig. A.1). The first article found was published in
1988 (Uhl et al. 1988), thus displaying a range of 31 years of pub-
lications (Fig. 1), with an average of 1.6 article per year, with 65% of
the articles published between the years 2009–2019. The biome
Amazon was the first Brazilian forest formation to be evaluated for AGB
(Uhl et al. 1988). Only after the year 2000, biomass was evaluated at
restorations of different forest types, as the Atlantic Forest, Cerrado,
and Caatinga biomes (Fig. 1).
Over the last three decades (1988–2019), 31 journals published the Fig. 2. Distribution of the studied restoration sites found among Brazilian
51 studies included in our database, and only 21% of them published biomes and the restoration method implemented. The color of the circles re-
more than one article (Table A.1; Fig. A.2). The journal “Forest Ecology presents the restoration method evaluated, where white circles are the location
and Management” had the highest number of publications, almost 14% of active restoration, and black circles are passive restorations. Restoration sites
of the articles (n = 7). Articles published by Brazilian journals re- of the same study, located in the same biome and close to each other are
present 23% (Table A.1). We identified 73 institutions linked to the grouped to improve sites’ distribution visualization. The size of the circles re-
presents the number of restoration sites.
authors of the articles (Table A.1). These institutions are distributed in
eight countries of three continents (America, Europe, and Oceania).
Brazilian (57%), American (20%), and British (11%) institutions are the (68%; n = 400), followed by the Atlantic Forest (20%; n = 116)
main contributors to the scientific knowledge accumulated. (Fig. 2). Cerrado and Caatinga were the biomes with less studied re-
storations, comprising only 12% of the restoration sites evaluated for
3.2. Restoration site’s information biomass (Fig. 2).
PR sites recovered by natural regeneration comprise almost 68% of
The 51 articles found encompassed 582 “restoration sites”, that is, the studied sites and are distributed throughout the four biomes iden-
individual areas under restoration process. Restorations ranged from 1 tified by the systematic review (Fig. 2). Besides almost 70% of the
to 70 years after its implementation, but only 35% of the articles stu- studied restorations are in the Amazon range, only one study of AGB in
died restorations older than 30y. Sites are distributed among four ARs was found in this biome. Atlantic Forest is the biome where AR
(Atlantic Forest, Amazon, Caatinga, and Cerrado) of the six Brazilian have been more studied, comprising > 50% of the whole AR sites
biomes (Fig. 2). Amazon is by far the biome with more studied sites identified (Fig. 2). Only 8% of the articles evaluated ARs and PRs of

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F.R. Gardon, et al. Forest Ecology and Management 462 (2020) 117972

similar conditions and at the same time (Ferreira et al. 2015; César et al. and weighed plants ranged from > 0 to 212 cm and the number of
2018). individuals from 14 to 4004, but only 32% of these equations presented
We identified a variety of human land-uses practiced among sites plant individuals with diameter ≥100 cm, and 56% felled and weighed
before restorations implementation, ranging from clear-cut to a com- ≥100 plant individuals.
bination of agriculture, pasture, and burning (Table A.2). Agriculture Just 31% of the articles that estimated AGB in plant individuals
and pasture were the most common past land-uses among restoration accounted for wood specific gravity (Table A.3), as a constant factor
sites, handled in 57% of the articles. Almost 23% of the studies eval- (Lindner and Sattler, 2012; da Silva et al. 2014; Galvão et al. 2015;
uated burned sites, and all of them were conducted in PRs, mainly in Silva et al. 2016; da Silva et al. 2017), or averaged values for specific
Amazon (75%). PRs derived from silviculture as past land-use activity species, genus and botanical family (Uhl et al. 1988; Steininger, 2000;
were also found in Atlantic Forest (César et al. 2018; Almeida et al. de Souza et al. 2011; Imaña-Encinas et al. 2012; Robinson et al. 2015;
2019; Rosenfield and Müller, 2019a; Rosenfield and Müller, 2019b), Silva et al. 2015; Sansevero et al. 2017; César et al. 2018).
and an actively restored site previously degraded by hydropower dam Carbon stored in plants biomass was evaluated only in 25% of the
construction was also found in this biome (Silva et al. 2015). studies, whose assumed that 45%, 47%, or 50% of the AGB values
correspond to carbon elements (Markewitz et al., 2010; de Melo and
Durigan, 2006; de Souza et al. 2011; Berenguer et al. 2014; Sattler et al.
3.3. Methodological criteria adopted by the studies to estimate AGB
2014; Robinson et al. 2015; Moura et al. 2016). Destructive methods
and laboratory procedures to calculate carbon concentration in dif-
To estimate AGB of plants aerial parts, studies used an averaged
ferent species were also observed (Feldpausch et al. 2004; Fearnside
total area sampled per site of 2363.2 m2. Among studies, the total area
et al. 2007; Silva et al. 2015; Pereira et al. 2016).
sampled per site ranged from 75 m2 to 13000 m2 (Table A.3). Some of
Biomass stored in litter compartment has also being evaluated at
them used additional sample plots to calculate the biomass of shrubs,
different forest types, conditions and restoration methods. We found
herbs and small plants (< 1 m height) by destructive methods. The
that litter biomass was evaluated in 23% of the articles (Table A.3),
criteria for inclusion of the plant individuals used in the articles were
75% of them conducted in PRs (Gama-Rodrigues et al. 2003; Markewitz
diameter and height. For plant diameter, the minimum size ranges
et al., 2010; Gama-Rodrigues et al. 2007; Vendrami et al. 2012;
from > 0.2 to ≥10 cm, and for height from > 1 to > 2 m (Table A.3).
Berenguer et al. 2014; Moura et al. 2016; Pereira et al. 2016; Peixoto
Moreover, 37% of the articles that evaluated AGB in plant aerial parts
et al. 2017; de Azevedo et al. 2018; Froufe et al. 2019; Rosenfield and
included only individuals of DBH ≥ 5 cm.
Müller, 2019a, 2019b). Litter stocks were most evaluated in Atlantic
Fifty-five allometric equations were used among studies to estimate
Forest, at both PRs and ARs.
AGB, and one to direct estimate carbon (Table A.4). Of these allometric
equations, 45% were developed based on weighing mixed species and
54% of them derived from Brazilian forests, distributed in the Amazon 3.4. Factors of influence on AGB recovery
(n = 6), Atlantic Forest (n = 3), Caatinga (n = 4), and Cerrado (n = 1)
biomes (Table A.4). Only 28% of the mixed species equations used We observed that 70% of the articles related AGB to one, or more,
among the studies derived from restored forests, all of them were de- biotic and abiotic factors. Forest attributes were the factors of influence
veloped in PRs (naturally regenerated) of Amazon and Atlantic Forest most related to AGB among the studies, including forest age, vegetation
biomes. We observed that Amazon was the Brazilian biome with the type, plant community condition and composition (Table 2). Restora-
largest set of equations, with 43% of the Brazilian mixed species tion age, that is, the time elapsed since restoration implementation, was
equations found in the studies, and the two mixed species equations the factor most evaluated among restoration studies, and our temporal
most used among the articles were derived from this biome (Uhl et al. analysis of AGB revealed that sites restored by different methods pre-
1988; Nelson et al. 1999). We found seven mixed species equations sent divergent patterns of AGB accumulation in the middle/long term
developed in PRs, and no equation derived from sites restored by AR (Fig. 3).
methods (Table A.4).
We also found 30 equations specific for 16 species, four plant genus, 4. Discussion
different life-forms (lianas, palms, and shrubs), and the Araliaceae bo-
tanical family (Table A.4). However, only 41% of the studies included 4.1. Distribution of AGB recovery studies among brazilian biomes and
non-tree life-forms in the AGB estimates (e.g. shrubs, lianas, palms, restoration methods: The impacts to national-scale generalizations
bamboo, and herbaceous plants) (Table A.3). Almost all studies that
accounted for different life-forms were conducted in PR sites, with only International commitments for the recovery of degraded lands, the
one study conducted in ARs. We also found an equation to estimate the rise of carbon credit markets, the pressure to reduce CO2 emissions by
leaf biomass in Caatinga plants (de Souza et al. 2012). forest conservation and restoration has been on the government’s
The allometric equations used to estimate AGB in the articles are agendas for more than 40 years, since the First United Nations
based in plant’s attributes, as trunk diameter, diameter plus height, Conference on the Human Environment in 1972, and the First World
basal area plus height, basal area, crown area or a combination of Climate Conference in 1979. Along this period, political marks as the
diameter, height and wood specific gravity (Table A.4). Among the United Framework Convention on Climate Change (1992), the Kyoto
mixed species equations used in the articles, the diameter of the felled Protocol (1997) and the Intergovernmental Panel on Climate Change

Table 2
Factors of influence and parameters related to AGB recovery found in the articles.
Factors of influence on AGB recovery Parameters % articles

Landscape edge effect; amount of adjacent forest; slope, and elevation 10% (n = 5)
Forest attributes age; forest type; successional phase; diversity (richness, Simpson, and Shannon); plant density; and life-form 45% (n = 23)
Restoration implementation restoration method (passive, active); and nutrient addition 8% (n = 4)
Past land-use type and time of land-use and site degradation level 16% (n = 8)
Soil soil type and soil properties 16% (n = 8)
Plant interaction herbivory 2% (n = 1)
Climate Annual precipitation 2% (n = 1)

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F.R. Gardon, et al. Forest Ecology and Management 462 (2020) 117972

AGB recovery is not aligned with the restoration methods most needed
and practiced in Brazil.
The fact that we found only one study that evaluated AGB stock in
ARs implemented by direct seeding, an efficient restoration method
cheapest than planting seedlings and able to trigger initial successional
processes (Freitas et al. 2019), evidence another bottleneck in the field.
However, this result can be a consequence of the focus of our study -
forests, seen that direct seeding is a restoration method used in most of
the Brazilian biomes, but mainly implemented in non-forest ecosystems.
Due to agricultural expansion, Brazil is one of the major con-
tributors to deforestation and to land‐use change emissions (Zarin et al.
2016) and the trend is that Brazilian biomes will continue to be de-
forested (Soares-Filho et al. 2014; Rochedo et al. 2018), increasing the
need for restoration efforts. In this sense, our results support the need
for scientific evaluations of AGB accumulation in regions with weak
information about the recovery of this ecological process, beyond
Amazon and Atlantic Forest biomes. This is crucial to the effective
achievement of the restoration goals, based on realistic site conditions.
Better understanding temporal changes in the process of AGB/carbon
Fig. 3. Predictive polynomial models fitted to estimate AGB stock (MgAGB.ha-1) in accumulation among restored sites, could leverage the improvement of
active (adjusted R2 = 0.82; p < 0.05; Residual Standard Error = 26.3 MgAGB.ha- AGB/carbon monitoring protocols, allowing a confident interpretation
1
; n = 37; AGB = −19.35058 + 4.00302 * age + 0.21641 * (age^2)) and passive about the large-scale potential of forest restorations in mitigating cli-
(adjusted R2 = 0.23; p < 0.05; Residual Standard Error - RSE = 49.5 MgAGB.ha-1; mate change.
n = 140; AGB = 10.0731 + 7.3956 * age − 0.1158 * (age^2)) restorations as a
response of age. The dark shaded line is the trend of AGB stock recovery over time 4.2. Methodological divergencies in AGB and carbon stocks estimates in
observed in passive restorations among biomes, and the lightly shaded line is the Brazilian restored forests
trend for active restorations. The shaded areas along the predictive lines represent
the confidence interval (95%) for the model. Data points were categorized by biome:
The rigorous selection of the appropriate allometric equation is
AF (circle) – Atlantic Forest; AM (triangle) – Amazon; CA (square) – Caatinga; and
CE (cross) – Cerrado. fundamental to a reliable AGB estimate and studies have shown that the
main source of error is attained to the choice of the allometric model,
once not representative equations of a targeted forest can lead to sub-
stantial errors in AGB estimates. Even in areas with similar conditions,
(IPCC) lead global governments to prioritize climate change mitigation
as climate, soil, forest type, restoration method, and age, major errors
and to preserve and recovery natural ecosystems. For this reason, we
can be introduced (Chave et al.2004; Lindner and Sattler, 2012; Sileshi,
were expecting to observe an earlier increase in the number of studies
2014; Silva et al. 2015). In tropical forests from Central America, Chave
related to AGB recovery by restored forests, improving the knowledge
et al. (2004) found that different allometric models can estimate AGB
and supporting political decisions over the years, instead of only in the
with a variation of 246 MgAGB.ha−1, even when applied to the same
last decade.
plot. In Amazonian PR sites, using eight different models to estimate
In 2008–2009 the National Plan on Climate Change and the
AGB stock, Wandelli and Fearnside (2015) observed that the mean error
National Politic on Climate Change were implemented in Brazil (Brazil,
of estimates for accumulated biomass varied from 5.6% to 57.5%. These
2008, 2009). This can explain a late and slight increase in the number
studies highlight the need for a representative set of allometric equa-
of publications/year, reaching the peak in 2019 (Fig. 1). Although
tions of the many tropical forest formations.
ecological restoration in Brazil present a solid and growing scientific
Thus, it is to be assumed that these issues were taken into account
production, with almost 300 articles published over the last 30 years
by AGB recovery studies, but our results show major divergences.
(Guerra et al. 2020), specific evaluations of AGB/carbon recovery in
Studies of AGB recovery in restored forests of Brazil have used equa-
these systems does not keep up with the increasing political decisions
tions derived from Brazilian natural forests and also from tropical for-
and appealing discussions related to forest restoration and climate
ests of other countries to estimate AGB (Table A.4), forests which may
change. Furthermore, because the Brazilian post-graduation network
present evident differences from the targeted one. The few equations
present solely almost 300 programs directly related to biodiversity and
derived from restored forests (28%) are not representative of the many
environmental sciences researches (Souza and Fernandes, 2013) we
forest formations and restoration methods used in Brazil, and we did
expected to find a more diversity of institutions improving scientific
not find in our database any equation derived from AR sites.
knowledge related to AGB recovery.
The similarity between the ecosystem that the equation derived and
We argue that the continuous improvement of the general knowl-
where it will be applied is important, but the equation inputs must also
edge could be attained to the broad range geographic distribution of
be considered. The allometric equations used in the studies are based on
scientific studies, allowing to predict AGB recovery patterns of different
plant’s trunk diameter and height, but basal area, crown area or a
forests restored by different methods. However, we observed an un-
combination of diameter, height and wood specific gravity are also used
balance in the restoration methods evaluated among biomes, where
to estimate AGB (Saldarriaga et al. 1988; Deans et al. 1996; Chave et al.
outcomes of AGB recovery from restored forests lack for some parts of
2005; Chave et al. 2014; Robinson et al. 2015). Chave et al. (2005)
Brazil and only 23% of the studies evaluated AGB recovery in ARs.
observed that the inclusion of height in the equations reduced the error
Guerra et al. (2020) observed that AR (seedling planting) is the most
of individual tree biomass estimation from 16% to 6%. In contrast,
used restoration method among Brazilian biomes, but we found an
Hunter et al. (2013) argue that height measurements in tropical forests
expressive predominance of PR sites among the studies of AGB/carbon
are labor and present potentially large errors, related to forest condi-
(Fig. 2). In addition, studies have shown that 78% of the land allocated
tions (e.g. dense understory vegetation, tall canopies, and closed-ca-
for restoration projects in the Atlantic Forest, Atlantic Forest/Cerrado
nopies), observer experience, and the equipment used.
ecotone and Amazon was designed for AR (Brancalion et al. 2016).
The performance of allometric models is also highly associated with
Together, these arguments evidence that scientific knowledge related to
the diameter range and the number of weighted plants included in their

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F.R. Gardon, et al. Forest Ecology and Management 462 (2020) 117972

database, and equations developed from a small number of individuals also important issues to ensure robust AGB estimates. Chave et al.
and small diameter range should be avoided (Chave et al. 2004). (2004) proposed that plots should size 2500 m2 to estimate AGB with
Among studies, we found seven equations encompassing ≥ 100 good confidence, representing the spatial variability of forests AGB. In
weighed plants and individuals with large diameters (≥100 cm), but general, the average plot size found is smaller than that for studies
only one of these equations was derived from a Brazilian forest, an conducted in Brazil, and this pattern seems to be widespread among
Amazonian natural forest (dos Santos, 1996; Ferreira and Prance, tropical restoration sites − 947 m2, average size for ~1468 plots of
1999). Despite some equations enable the inclusion of small-sized Neotropical secondary forests (Poorter et al. 2016).
plants, 37% of the studies included in their AGB estimations only plant The conversion of AGB on carbon stocks also need to be highlighted.
individuals ≥ 5 cm diameter. We observed that carbon concentration in dry AGB, used as an carbon
Of course, individuals within this range represent the most share of conversion factor among studies, varied from 45% to 50%. However, it
AGB in mature tropical forests, but in young restorations (2-4y re- is known that different forests, with different species composition, can
generation) 100% of the AGB can be stored in the 1–5 cm DBH class, present disparities in average values of carbon (IPCC, 2006). Obviously,
decreasing to less than 10% in older restorations (12–14y) (Feldpausch generalizations are important, especially to conduct large-scale studies,
et al. 2005). Thus, biomass evaluations in restored forests should be but these methodological aspects might be rigorously thought, once it
aware of the contribution of these small-sized individuals to AGB re- can result in not confident estimates of carbon stocks and CO2 se-
covery and, depending on restoration method and the successional questration potential by restorations.
stage, neglecting small plants can cause misleading interpretations of It is known that technical and legal issues can bar building allo-
the AGB stored in restored forests. metric equations in restored forests and, for a while, authors are re-
This issue can be extended to the limitation of using wood specific stricted to the few equations indicated for AGB estimations in these
gravity, due to the scarce availability of experts able to identify species areas. For example, costs related to destructive methods of AGB esti-
in field campaigns. In spite of that, besides wood specific gravity be also mation can reach US$ 11.00 per plant individual (Silva, 2007), af-
recognized as an important specie’s attribute to reliably estimating AGB fecting the viability of fitting new equations based on large datasets.
stock on forest stands (Brown et al. 1989; Chave et al. 2006; Chave et al. Nevertheless, some advances for estimating AGB stocks in AR sites has
2014), the majority of the studies in Brazilian restored forests have risen in the Atlantic Forest biome (Miranda et al. 2011; Nogueira Júnior
neglected this attribute. et al. 2014; Ferez et al. 2015; Ré et al. 2015; Zanini, 2019). We state
Another highlight we found is that the number of species used to that our goal was not to evaluate the whole set of equations available
develop the Brazilian’s mixed species allometric equations is not even for Brazilian forests, but those that have been most used among studies
close to the plant diversity of these tropical forests. The importance of to estimate AGB in restoration sites.
including more species and life-forms in the allometric models relies on
the processes of weighing plant’s components (trunk, canopy, leaves), 4.3. The main drivers of AGB recovery studied among Brazilian restored
while species store different amount of biomass among their compo- sites
nents. The concern of including more species in the allometric equa-
tions also involves accounting for different life-forms. Besides trees Forest attributes (45%), past land-use (16%), soil properties (16%),
share the highest proportion of AGB stocks in tropical forests (Ligot and landscape metrics (10%), were the most factors related to biomass,
et al. 2018; Meakem et al. 2018), other life-forms can play important comprised in 65% of the studies. Among the forest attributes, time
roles in ecological processes and functions, as forest productivity elapsed since restoration starts (e.g. age) was related to AGB stocks in
(Gerwing and Farias, 2000; Schnitzer and Bongers, 2002; Gehring et al. 29% of the studies conducted in Brazil. Restoration age is important
2005; Alves et al. 2012). For example, in Amazon, shrubs can corre- because enough time is needed to forests succession and ecological
spond to 74% of the total AGB stored in 2–4y regenerated pastures processes, as AGB accumulation, to reestablish (Crouzeilles et al. 2016).
(Feldpausch et al. 2005), and among different forests in the Atlantic Besides that, age is more correlated to AGB stocks in ARs (R2 = 0.82)
Forest biome, lianas, palms, tree ferns, bamboo, and epiphytes can than PRs (R2 = 0.22) (Fig. 3), suggesting that in PR other factors
share more than 10% of the AGB (Vieira et al. 2008). present high influences on the AGB stock.
Despite the share of different life-forms on AGB stocks, only four Plant community composition has a relevant importance on AGB
equations and less than half of the studies included non-tree life-forms stocks in restoration, since fast-growing species present a higher con-
in their database. Moreover, no AR site was evaluated within this tribution during the early years (< 37 years), but the contribution of
concern. The contribution of different species and life-forms to AGB slow-growing is significant at later stages of succession (Shimamoto
accumulation in tropical forests cannot be neglect, and this issue is et al. 2014). This suggests that AGB accumulation patterns is not con-
accentuated by the urgent need to include more diversity of species and stant over time, and is related to the changes in the plant composition
life-forms in AR projects (Rodrigues et al. 2009). along the restorations successional trajectory.
Studies are selecting equations not well fitted with their objectives, In this context, forest type and successional stage are also related to
or even their forest types or stage, suggesting the lack of multiple AGB stocks (Lu et al. 2003; Santos et al. 2003). Costa et al. (2014)
equations adjusted for restored forests and at different conditions, observed that Caatinga PR sites of dense forests and at advanced suc-
which can lead to unreliable AGB estimates. In a first effort to overlap cessional stages accumulate more than 2-fold the AGB stock of open
this gap, wide and robust allometric models must be available for forests at early regeneration stages (45.8 and 20.7 Mg ha−1, respec-
generalizations in each biome. Whenever possible, these general models tively). Similar results were also observed for different vegetation types
should encompass data from the different vegetation types of each at different successional stages in Cerrado biome, where sites of Cer-
biome, as the Atlantic Forest formations recognized as Ombrophilous radão (the Brazilian Forested Savanna) presented more AGB stocks than
(Dense, Mixed, and Open) and Seasonal (Semidecidual and Decidual) grasslands and typical Savannas (de Miranda et al. 2014; Roquette,
forests, or even the forested Savannas formations (Cerradão). Other 2018). Because Brazilian biomes comprise a mosaic of vegetation types,
studies could regard the inclusion of allometric equations fitted for these results imply in a huge challenge to understand how AGB is re-
vegetation associated with water courses, and also mangroves located covered by restoration actions in a full range of situations.
at costal zones (Ferreira et al. 2015; Ferreira et al. 2019), since this The influence of plant diversity (species richness, Shannon and
proximity directly influence the vegetation patterns (structure and Simpson index) on AGB stocks was accessed in 9% of the studies,
composition) at different biomes (Coutinho, 2016; IBGE, 2012). conducted in Amazon, Atlantic Forest and Caatinga biomes, pointing to
Because evaluations of AGB stocks in forests are based on the ex- a positive relationship with AGB recovery (Vieira et al. 2003; de Aguiar
trapolation of data collected at plot scale, plot size and plot position are et al. 2013; Robinson et al. 2015; Rosenfield et al. 2019b). The positive

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relationship between plant community diversity and biomass pro- The litter compartment and its contribution to total biomass stocks
ductivity occurs due to the coexistence of species that ensure a greater in restoration sites also depends on factors as restoration age, structure
complementarity and facilitation in forested ecosystems, and conse- and composition. In Amazon (19y secondary forest), Atlantic Forest
quently a better efficiency in the use of resources (Wright, 2002; (40y secondary forest), and Cerrado (22y secondary forest) biomass
Nakamura, 2008; de Aguiar et al. 2013). For example, de Aguiar et al stocks in litterfall was estimated to reach 67 Mg.ha−1, 7.3 Mg.ha−1,
(2013) estimated that enhancing species richness from 1 to 10 species, and 3.9 Mg.ha−1, respectively (Markewitz et al., 2010; Gama-
PR sites of Caatinga (6-9y) annual AGB increment can increase Rodrigues et al. 2007; Peixoto et al. 2017). In Caatinga (30y re-
5.1 Mg.ha−1.y-1. These results have a direct effect on restoration stra- generated forest), annual production of litterfall biomass can reach 6.1
tegies, providing the subsidy for restoration ecology, which is the basis MgAGB.ha−1.y-1 (Pereira et al. 2016). In secondary Atlantic Forests at
for any ecological restoration. different regeneration stages, annual production of litterfall biomass
The AGB recovery rate also depends on the site’s conditions, as past was higher in early stages of natural regeneration than in more ad-
land-use, adjacent forest cover, climatic water deficit, and other social vanced forests, and this is attained to the high proportion of pioneer
and political drivers (Chazdon et al. 2016; Crouzeilles et al. 2016; species in young secondary forests, where species present higher leaf
Chazdon et al. 2017). Studies have found that, in restoration sites at flat turnover than late successional species (Vendrami et al. 2012). Besides
terrains and embedded in landscapes with high forest coverage, the we found a few studies of litter stock, they are also high concentrated in
AGB recovery is more efficient for both PR and AR methods (Sattler PRs. Only three studies evaluated litter stock in ARs, exclusively in the
et al. 2014; Robinson et al. 2015; Toledo et al. 2018). Sattler et al. Atlantic Forest biome (de Azevedo et al. 2018; Rosenfield and Müller,
(2014) found evidence that AR sites located on sloped terrains stock less 2019a; Rosenfield and Müller, 2019b).
than half the carbon (17.5 Mg.ha−1) stored by similar restorations on
flat terrains (37.6 Mg.ha−1) in Atlantic Forest biome. 4.4. Temporal analysis of AGB recovery in Brazilian forest restorations
Throughout the landscapes, the amount and distribution of sur-
rounding forests are the main regulators of seed dispersal with a strong In recent years, studies have focused on to determine which one, PR
effect in early-successional trajectories, while flat terrains are asso- or AR methods, is more successful in recovering AGB stocks, vegetation
ciated with high water retention, being both relevant drivers of AGB structure and biodiversity (Brancalion et al. 2016; Crouzeilles et al.
accumulation (Osman and Barakbah, 2011; Uriarte et al. 2011; Holl and 2017, Meli et al. 2017). We found only two articles that compared AGB
Zahawi 2014; Sattler et al. 2014; Robinson et al. 2015). In 30y Atlantic of AR and PR sites at similar conditions (Ferreira et al. 2015; César et al.
Forest PRs, Robinson et al. (2015) observed that the amount of adjacent 2018). César et al. (2018) studying AGB recovery in Atlantic Forest,
forest and slope are predictors with the large effects on biomass stock, found that PR sites derived from pasture stock 45% (91.3 MgAGB.ha−1)
positively and negatively correlated to AGB, respectively. less AGB of native species than AR sites (132.2 MgAGB.ha−1) from 7 to
Edge effects were also studied, and sample plots near to the forest 20-year-old. In an Atlantic Forest mangrove, Ferreira et al. (2015) also
edge presented low AGB stocks (Berenguer et al. 2014), result that can found this pattern of AGB recovery in 5-year-old restored sites, but AGB
be explained by the decline observed in AGB within 100 m from forest stock in AR (60 Mg.ha−1) was 3-fold the AGB of PR sites (20 Mg.ha−1).
fragments edges, where tree mortality is increased by microclimatic Our model estimated that PRs of 30y can stock 38% (127 Mg.ha−1) of
changes and wind disturbances (Laurance et al. 1997). Regarding these the AGB estimated for ARs of the same age (334 Mg.ha−1) (Fig. 3).
evidences and the fact that a significant part of the environmental debt Other studies have found that AGB recovery in 30y PR sites can
encompasses legally protected forests at riparian and sloped areas reach 98.5 MgAGB.ha−1 in Amazon and 43.3 MgAGB.ha−1 in Caatinga
(Federal Law, 12.651; Soares-Filho et al. 2014), which can be limited to sites, while 25y PRs in Atlantic Forest can accumulate 158.8
strips of 5 m width and steep slopes, restorations success and goals can MgAGB.ha−1 (de Souza et al. 2011; Galvao et al. 2015; Pereira et al.
be hampered. 2016). ARs in Atlantic Forest and Cerrado can present AGB stock higher
Land-use type, degradation level, time since last disturbance and than PRs of the region and similar age (de Melo and Durigan, 2006; de
under land-use, were observed to have significant effects on AGB. Time Souza et al. 2011; César et al. 2018). While AGB stocks of AR sites of the
since last fire event presented positive effects on AGB recovery, while Atlantic Forest can reach 222 MgAGB.ha-1 at 25 years after restoration
grazing, time under land-use, and land-use intensities negatively af- implementation (Durigan et al. 2016), 25 years-old PRs of the same
fected AGB recovery in Amazonian PR sites (Uhl et al. 1988; Feldpausch biome can stock from 73 to 159 MgAGB.ha−1 (de Souza et al. 2011).
et al. 2007; Gehring et al. 2005; Berenguer et al. 2014). In Amazon, PR The results corroborates the pattern of AGB accumulation between
sites (< 15y) previously used for agriculture presented faster AGB ac- restoration methods, where ARs present better outcomes than PRs. In
cumulation than PR sites regenerated from pasture lands (Wandelli and general, it can be observed that the processes of AGB accumulation in
Fearnside 2015). However, 7–20y PRs regenerated from pastures in the first years of restoration are similar at both active and passive re-
Atlantic Forest can store 43% more AGB of native species than re- storations (Fig. 3), but after 5–10 year AGB accumulation restoration
generated sites of similar age derived from Eucalyptus sp. plantations methods start to present divergences. However, to compare PR and AR
(César et al. 2018). The number of burns also negatively affect AGB outcomes depends on how restorations data sets are categorized as
(Wandelli and Fearnside 2015; Sansevero et al. 2017). passive and active methods, and controlling for key factors as past
Soil parameters presented important effects on AGB stocks among disturbance, landscape metrics, climatic patterns, and restoration age is
Brazilian restored forests. In PRs derived from pastures in Atlantic fundamental (Crouzeilles et al. 2017; Reid et al. 2018). Nevertheless,
Forest, soil sand and clay content presented negative and positive ef- comparative studies of different restoration methods are important to
fects on AGB recovery, respectively (Robinson et al. 2015; Toledo et al. know what to expect from each strategy, but the selection of the re-
2018). These properties are related to soil water retention capacity, an storation method for a particular site must be based on its natural re-
important driver for plant growth and AGB recovery (Lu et al. 2002). silience, past land-use history, and the surrounding landscape matrix
Higher AGB stocks were observed in Atlantic Forest ARs at fertile and (Holl and Aide, 2011).
clayish soils than the same restorations at sandy and poor soils (de Melo It is important to highlight that remote sensing (e.g. LiDAR and
and Durigan, 2006). Moran et al. (2000) also found significant effects of optical sensors) are useful tools that have been utilized among Brazilian
soil type on AGB stocks in passively restored forests in Amazon. Besides biomes to the monitoring of AGB recovery, especially due to the pos-
soil fertilization play an important role on any plant growth, undesired sibility of long-term temporal analysis (Luckman et al. 1997; Santos
outcomes as benefiting aggressive and invasive species may negatively et al. 2003; Vieira et al. 2003; da Silva et al. 2014; Galvão et al. 2015;
affect AGB accumulation, but control interventions present positive Almeida et al. 2019). Also, although allowing quick data collection of
effects in these cases (Siddique et al. 2010, Ferez et al. 2015) forest structural attributes, remote methods are supported by field

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Declaration of Competing Interest G.A.L., Bongers, F., Vester, H., Lohbeck, M., Brancalion, P.H.S., Saldarriaga, J.G.,
Mora, F., Vieira, I.C.G., Steininger, M.K., Schwartz, N.B., Hall, J.S., DeWalt, S.J.,
Junqueira, A.B., Orihuela-Belmonte, E., Peña-Claros, M., Almeida-Cortez, J.S.,
The authors declare that they have no known competing financial Balvanera, P., Swenson, N.G., Aide, T.M., Becknell, J.M., Letcher, S.G., Romero-
Pérez, I.E., de Jong, B., Rozendaal, D.M.A., Craven, D., Williamson, G.B., Espírito-
interests or personal relationships that could have appeared to influ-
Santo, M.M., Jakovac, C.C., van der Wal, H., Veloso, M.D.M., Ruíz, J., Martínez-
ence the work reported in this paper. Ramos, M., Fandino, M.C., 2016. Carbon sequestration potential of second-growth
forest regeneration in the Latin American tropics. Sci. Adv. 2, e1501639. https://doi.
org/10.1126/sciadv.1501639.
Acknowledgment Costa, T.L., Sampaio, E.V.S.B., Sales, M.F., Accioly, L.J.O., Althoff, T.D., Pareyn, F.G.C.,
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