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Altered dynamics of forest recovery under a changing climate

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Forest regeneration following disturbance is a key ecological process, influencing forest structure and function, species assemblages, and ecosystem-climate interactions. Climate change may alter forest recovery dynamics or even prevent recovery, triggering feedbacks to the climate system, altering regional biodiversity, and affecting the ecosystem services provided by forests. Multiple lines of evidence-including global-scale patterns in forest recovery dynamics; forest responses to experimental manipulation of CO2 , temperature, and precipitation; forest responses to the climate change that has already occurred; ecological theory; and ecosystem and earth system models-all indicate that the dynamics of forest recovery are sensitive to climate. However, synthetic understanding of how atmospheric CO2 and climate shape trajectories of forest recovery is lacking. Here, we review these separate lines of evidence, which together demonstrate that the dynamics of forest recovery are being impacted by increasing atmospheric CO2 and changing climate. Rates of forest recovery rates generally increase with CO2 , temperature, and water availability. Drought reduces growth and live biomass in forests of all ages, having a particularly strong effect on seedling recruitment and survival. Responses of individual trees and whole-forest ecosystems to CO2 and climate manipulations often vary by age, implying that forests of different ages will respond differently to climate change. Furthermore, species within a community typically exhibit differential responses to CO2 and climate, and altered community dynamics can have important consequences for ecosystem function. Age- and species-dependent responses provide a mechanism by which climate change may push some forests past critical thresholds such that they fail to recover to their previous state following disturbance. Altered dynamics of forest recovery will result in positive and negative feedbacks to climate change. Future research on this topic and corresponding improvements to earth system models will be key to understanding the future of forests and their feedbacks to the climate system. © 2013 Blackwell Publishing Ltd.
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REVIEW ARTICLE
Altered dynamics of forest recovery under a changing
climate
KRISTINA J. ANDERSON-TEIXEIRA*,ADAMD.MILLER, JACQUELINE E. MOHAN§,
TARA W. HUDIBURG**, BENJAMIN D. DUVAL†† and EVA N H. DELUCIA**
*Conservation Ecology Center, Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA, USA
Smithsonian Institution Global Earth Observatory-Center for Tropical Forest Science, Smithsonian Tropical Research Institute,
Panama, Repu
´blica de Panama
´Institute for Genomic Biology, University of Illinois, §Odum School of Ecology, University of
Georgia, Athens, GA, USA Energy Biosciences Institute, University of Illinois, at Urbana-Champaign, Urbana, IL, USA **Plant
Biology, University of Illinois, at Urbana-Champaign, Urbana, IL, USA ††US Dairy Forage Research Center, USDA-ARS,
Madison, WI 53706, USA
Abstract
Forest regeneration following disturbance is a key ecological process, influencing forest structure and function, spe-
cies assemblages, and ecosystemclimate interactions. Climate change may alter forest recovery dynamics or even
prevent recovery, triggering feedbacks to the climate system, altering regional biodiversity, and affecting the ecosys-
tem services provided by forests. Multiple lines of evidence including global-scale patterns in forest recovery
dynamics; forest responses to experimental manipulation of CO
2
, temperature, and precipitation; forest responses to
the climate change that has already occurred; ecological theory; and ecosystem and earth system models all indicate
that the dynamics of forest recovery are sensitive to climate. However, synthetic understanding of how atmospheric
CO
2
and climate shape trajectories of forest recovery is lacking. Here, we review these separate lines of evidence,
which together demonstrate that the dynamics of forest recovery are being impacted by increasing atmospheric CO
2
and changing climate. Rates of forest recovery generally increase with CO
2
, temperature, and water availability.
Drought reduces growth and live biomass in forests of all ages, having a particularly strong effect on seedling recruit-
ment and survival. Responses of individual trees and whole-forest ecosystems to CO
2
and climate manipulations
often vary by age, implying that forests of different ages will respond differently to climate change. Furthermore, spe-
cies within a community typically exhibit differential responses to CO
2
and climate, and altered community dynam-
ics can have important consequences for ecosystem function. Age- and species-dependent responses provide a
mechanism by which climate change may push some forests past critical thresholds such that they fail to recover to
their previous state following disturbance. Altered dynamics of forest recovery will result in positive and negative
feedbacks to climate change. Future research on this topic and corresponding improvements to earth system models
will be a key to understanding the future of forests and their feedbacks to the climate system.
Keywords: biogeochemistry, climate feedback, FACE, irrigation, regime shift, succession, throughfall manipulation, warming
Received 19 December 2012 and accepted 29 January 2013
Introduction
The dynamic process of forest regeneration following
disturbance is of key importance, with ramifications on
several scales. On a local level, forest recovery involves
wholesale rearrangement of vegetative structure,
carbon (C) and nutrient cycling, ecosystem physiology,
and community structure (Table 1). On a landscape
level, disturbancerecovery dynamics play an impor-
tant role in the maintenance of species diversity, as
different species use forests of different ages as habitat
patches. On a regional to global level, secondary forests
are consequential for their role in climate regulation.
Forests recovering from disturbance (secondary forests)
are strong C sinks and play an important role in the
global C cycle (Running, 2008; Pan et al., 2011). For
instance, in recent years (20002007), regrowth of tropi-
cal forests following agricultural abandonment took up
an estimated 1.7 Pg C yr
!1
(Pan et al., 2011), which is
equivalent to ca. 20% of annual global fossil fuel emis-
sions. Beyond their influence on climate through their
role in the global carbon cycle, secondary forests also
influence climate through biophysical mechanisms (Liu
Correspondence: Kristina J. Anderson-Teixeira, Smithsonian
Conservation Biology Institute, National Zoological Park, 1500
Remount Rd., Front Royal, VA 22630 USA, tel. 1 540 635 6546, fax
1 540 635 6506, e-mail: TeixeiraK@si.edu
Published 2013. This article is a U.S. Government work and is in the public domain in the USA. 1
Global Change Biology (2013), doi: 10.1111/gcb.12194
et al., 2005; Maness et al., 2012; O’Halloran et al., 2012);
for example, in northern regions albedo decreases with
forest age and strongly shapes the net climate regula-
tion services of secondary forests (Randerson et al.,
2006; Jin et al., 2012; O’Halloran et al., 2012).
A large and growing proportion of forests have been
affected by major disturbances. Globally, secondary for-
ests recovering from anthropogenic disturbances such
as agriculture and wood harvesting cover an estimated
27 million km
2
(Hurtt et al., 2011), and an estimated
1.2 million km
2
are in use as forestry plantations
(Kirilenko & Sedjo, 2007). In addition, natural distur-
bances affect a significant proportion of Earth’s ecosys-
tems; disturbances such as fires, storms, droughts, and
insect outbreaks affect over 100 000 km
2
annually in
North America alone (Amiro et al.,2010).Climatechange
is generally increasing the incidence of natural distur-
bances (Dale et al.,2001),includingfires(Westerlinget al.,
Table 1 Typical trajectories of change in forest properties following stand-replacing disturbance
Forest property Typical trajectory References
Biomass
Biomass
accumulation rate
Rapid initial increase, peak at intermediate age followed
by slow decline to near zero in old-growth forests.
Lichstein et al., 2009; Yang et al., 2011;
Hember et al., 2012
Leaf biomass or area Rapid initial increase, relatively stable thereafter. Uhl & Jordan, 1984; Bormann & Likens,
1994; Law et al., 2003; Goulden et al.,
2011; Yang et al., 2011
Fine root biomass Rapid initial increase, relatively stable or modest
decline thereafter.
Vogt et al., 1983; Claus & George, 2005;
Yuan & Chen, 2010
Carbon cycle
Gross primary
productivity
Rapid initial increase, relatively stable or modest
decline thereafter.
Amiro et al., 2010; Goulden et al., 2011
Net primary
productivity
Rapid initial increase, modest decline thereafter. Gower et al., 1996; Law et al., 2003;
Pregitzer & Euskirchen, 2004; Goulden
et al., 2011
Heterotrophic
respiration
Relatively constant. Law et al., 2003; Pregitzer & Euskirchen,
2004; Goulden et al., 2011
Net ecosystem
C balance
Initially negative (C source), increasing to maximum
(C sink) at intermediate ages, declining thereafter.
Controversy remains as to whether it declines to zero
(C neutrality).
Law et al., 2003; Pregitzer & Euskirchen,
2004; Zhou et al., 2006; Baldocchi, 2008;
Luyssaert et al., 2008; Amiro et al., 2010;
Goulden et al., 2011
Biogeochemistry
Foliar [N] Relatively constant with age, although both decreases
(more common) and increases have been observed.
Davidson et al., 2007; Drake et al., 2010;
Yang et al., 2011
N mineralization Mixed responses; both increases and decreases have
been observed.
Vitousek et al., 1989; LeDuc & Rothstein,
2010
Hydrology
Canopy transpiration Rapid initial increase, modest decline thereafter. Roberts et al., 2001; Delzon & Loustau,
2005; Amiro et al., 2006; Drake
et al., 2011a
Hydraulic limitation Increases with age. Drake et al., 2010, 2011a
Sensitivity to variation
in water availability
Decreases with age. McMillan et al., 2008; Drake et al., 2010;
Voelker, 2011
Community dynamics
Species turnover Rapid initial turnover, decelerating decrease in
turnover rate as the forest ages.
Anderson, 2007b
Species richness Initial increase, sometimes peaking and declining
modestly in older forests.
Shafi & Yarranton, 1973; Finegan, 1996;
Anderson, 2007b
Competition Increasing competitive advantage to late-successional
species (e.g., shade tolerant, slow growing, higher
wood density, longer lived)
Bazzaz, 1979; Bazzaz & Pickett, 1980;
Finegan, 1984
Size structure Initially, relatively even aged; competitive thinning
and seedling recruitment drive convergence
toward inverse square relationship between
abundance and diameter (diverse age structure)
Enquist et al., 2009
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
2K. J. ANDERSON-TEIXEIRA et al.
2006) and biotic disturbances such as insect outbreaks
(Evangelista et al.,2011;Hickeet al.,2011).Theoryand
models predict that future climate change may cause
even more drastic changes (e.g., Westerling et al.,2011),
depending on the future course of greenhouse gas emis-
sions and the resultant shifts in climate (IPCC, 2007).
Because secondary forests are strong carbon sinks with
considerable value for greenhouse gas mitigation (Ander-
son-Teixeira & DeLucia, 2011) and also represent a poten-
tial bioenergy source (e.g., US DOE, 2011), secondary
forests are likely to play substantial roles in climate miti-
gation initiatives and bioenergy production (Kirilenko &
Sedjo, 2007).
Although there is strong and abundant evidence that
climate change will affect forests of all ages, we lack
synthetic understanding of how climate change will
interact with forest age to shape the dynamics of forest
recovery. Because forests undergo substantial reorgani-
zation of following major disturbance (Table 1), it is
likely that climate change will have different effects on
forests of different ages, thereby altering the trajectory
of succession relative to those observed for historical
climates. Climate change may alter one or more distinct
features of successional trajectories (Fig. 1). First, the
rate at which the forest moves along the successional
trajectory may be altered without necessarily implying
any changes to the successional pathway or the state of
mature forests; for example, increased productivity
may accelerate biomass accumulation without altering
the biomass of mature forests. Second, the state of
mature forests may be altered; for example, maximum
biomass may be altered if future climates place differ-
ent biophysical constraints on the number and size of
trees that can persist. Third, the successional pathway
may be altered; for example, tree establishment may be
delayed by altered climatic conditions such that pro-
portionally more time is spent in an early-successional
shrub phase. Distinguishing how climate change affects
forests of different ages and thereby how it alters suc-
cessional trajectories is critical in understanding how
climate change will impact both recently disturbed and
mature forests.
This review considers how altered atmospheric CO
2
and climate are likely to impact trajectories of forest
recovery, with a particular focus on how climate
change may alter the rate of succession, the state of
mature forests, and successional pathways (Fig. 1). We
consider five major lines of evidence relating forest
structure and function to directional variation in CO
2
and climate (i.e., average conditions, as opposed to
intra- or interannual variation), each of which yields
insight into how forest recovery may be altered under a
changing climate. First, we review how climatic influ-
ences the dynamics of forest recovery across broad
climatic gradients. Second, we summarize the results of
experimental studies quantifying the effects of elevated
CO
2
, elevated temperature, and altered precipitation
regimes on the dynamics of forest recovery. Third, we
review observations of altered forest recovery under
contemporary multivariate environmental change.
Fourth, we consider how altered community dynamics
may impact forest recovery. Fifth, we review model
predictions. Finally, we synthesize findings from these
separate lines of evidence, identify remaining uncer-
tainties, and discuss the implications for ecological
communities, biogeochemical processes, and the
climate system.
Dynamics of forest recovery across broad climatic
gradients
Although few studies have evaluated how climate
influences forest recovery across broad climatic gradi-
ents (Prach & Rehounkov!
a, 2006; Anderson, 2007a),
there is clear evidence that climate exerts a strong influ-
ence on the rate of succession, the state of mature for-
ests, and their successional pathways (Fig. 1). The rate
of forest regrowth following disturbance is strongly
influenced by climate (Brown & Lugo, 1982; Johnson
et al., 2000; Anderson et al., 2006). Globally, the rate of
living biomass accumulation increases with tempera-
ture, being on average three to four times faster in the
tropics than in high-latitude forests (Fig. 2a; Anderson
et al., 2006). Likewise, biomass accumulation rate
increases with precipitation at a global scale (Fig 2b).
Within the tropics, rates of biomass accumulation are
Fig. 1 Schematic diagram illustrating three ways in which cli-
mate change may impact the dynamics of forest recovery. Rela-
tive to the historical trajectory of change in a forest property
(here, biomass) with age, climate change may alter (1) the rate
of change, (2) the state to which the property converges as the
forest matures (‘mature state’), or (3) the successional pathway
(i.e., the sequence of states through which any given ecosystem
property passes and the relative amount of time spent in each).
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
FOREST RECOVERY UNDER CLIMATE CHANGE 3
dramatically higher in moist climates (precipitation
10002500 mm yr
!1
) than in dry climates (precipitation
<1000 mm yr
!1
); however, the positive influence of
precipitation appears to saturate, with rates in wet cli-
mates (precipitation >2500 mm yr
!1
) less than or equal
to those in moist climates (Brown & Lugo, 1982; Mar!
ın-
Spiotta et al., 2008). Although further research is
required to fully understand the mechanisms through
which temperature, water availability, and their sea-
sonal dynamics affect rates of biomass accumulation in
secondary forests, we can say conclusively that warmer
temperatures and higher moisture availability are asso-
ciated with higher rates of biomass accumulation.
Growth in secondary forests is strongly linked to ele-
mental cycling. Biogeochemical cycles of elements
including C, nitrogen (N), and phosphorous (P) are
coupled to biomass accumulation through stoichiome-
tric constraints on the elemental composition of vegeta-
tion, such that rates at which these elements are
sequestered in vegetation are grossly proportional to
rates of biomass accumulation (Yang et al., 2011).
Indeed, mirroring the climate dependence of rates of
biomass accumulation (Fig. 2ab; Anderson et al.,
2006), it has been observed that the rate of N uptake by
a regrowing tropical forest in Costa Rica is four times
that of a regrowing temperate forest at Hubbard Brook,
USA (Russell & Raich, 2012). However, the trajectory of
forest recovery is also shaped by biogeochemistry
climate interactions. For example, climate influences
temporal patterns of N availability during secondary
succession (Vitousek et al., 1989), rates of change in soil
C and N (Li et al., 2012), and plant tissue stoichiometry
(Wright et al., 2004). Thus, climate may indirectly influ-
ence forest recovery through its influence on biogeo-
chemistry, as occurs in the case of forests developing
on Hawaiian lava flows (Anderson-Teixeira et al., 2008;
Anderson-Teixeira & Vitousek, 2012).
A few studies have compared rates or pathways of
secondary succession across broad climatic gradients.
Following clear cutting in western Oregon, climate
shapes both the rate and pathway of forest succession;
in the western Cascades region, conifer regeneration is
slower and follows a longer establishment delay com-
pared with the more mesic Coastal Range region (Yang
et al., 2005). In subalpine forests of the Colorado Rock-
ies, the rate of succession is more than twice as rapid in
mesic sites as compared with xeric sites (Donnegan &
Rebertus, 1999). Likewise, in the Medicine Bow moun-
tains of Wyoming, succession to a mature sprucefir
forest is most rapid in a mesic drainage bottom, slower
on a less mesic north-facing slope, and rarely occurs at
more arid sites prior to stand-clearing fire (Romme &
Knight, 1981). In the Czech Republic, the rate of succes-
sion in vegetative communities (including forests and
nonforests) is strongly influenced by climate; mean
annual change in dominant species cover during the
first 12 years of succession decreases dramatically with
increasing elevation (increasing precipitation and
(a) (b)
(c) (d)
Fig. 2 Influence of climate on forest recovery rates (a, b) and on aboveground C stocks of mature forests (c, d). The rate of aboveground
biomass accumulation in forests recovering from stand-clearing disturbance varies globally with respect to (a) mean annual tempera-
ture (MAT) and (b) precipitation (MAP). Data, which are from Anderson et al. (2006), represent natural regeneration in 68 unmanaged
forests worldwide. Solid and dashed lines represent an exponential fit and its 95% confidence interval, respectively. Similarly, above-
ground C stocks (biomass +coarse woody debris; CWD) in mature forests vary globally with respect to (c) MAT and (d) MAP. Data
from Anderson-Teixeira et al. (2011). Dashed lines represent hypothesized bioclimatic limits.
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
4K. J. ANDERSON-TEIXEIRA et al.
decreasing temperature; Prach et al., 2007). These exam-
ples provide evidence that climate strongly influences
both the rate and pathway of succession.
In addition to its influence on the rate and trajectory
of forest recovery, climate also shapes the types of
steady-state conditions toward which secondary forests
can eventually converge. Globally, aboveground
biomass of forests is influenced by temperature and
precipitation (Fig. 2cd; Keith et al., 2009; Anderson-
Teixeira et al., 2011; Larjavaara & Muller-Landau,
2012), and climate strongly influences most other major
components of ecosystem C cycles, including gross and
net primary productivity (GPP and NPP, respectively;
Luyssaert et al., 2007), soil and whole-ecosystem respi-
ration, and soil organic carbon (Raich & Schlesinger,
1992; Jobb!
agy & Jackson, 2000). Similarly, species diver-
sity varies globally with respect to climate (Brown et al.,
1998). In sum, climate can determine the state to which
forests converge following disturbance both directly
through biophysical constraints and indirectly through
its influence on biogeochemistry and the surrounding
metacommunity.
The broad-scale patterns described above demon-
strate that climate strongly influences the rate of forest
recovery, successional pathways, and the structure and
function of mature forests. However, transient dynam-
ics under a rapidly changing climate may diverge from
expectations based on these contemporary patterns,
and increasing atmospheric CO
2
concentrations will
alter physiological constraints on forests. To under-
stand the more immediate responses of forest recovery
to elevated CO
2
and climate change, we turn to experi-
mental manipulations.
Forest responses to experimental manipulation of
CO
2
, temperature, and precipitation
Experiments manipulating CO
2
, temperature, and pre-
cipitation demonstrate that altered climatic conditions
will alter ecosystem and community dynamics in sec-
ondary forests. The responses of terrestrial ecosystems
in general to these experimental manipulations have
been previously reviewed (e.g., Pendall et al., 2004; De
Graaff et al., 2006; Norby & Zak, 2011; Wu et al., 2011;
Beier et al., 2012; Dieleman et al., 2012; Lu et al., 2012);
here, we focus specifically on the responses of forests
and any age dependency of their responses (Fig. 3).
Responses to CO
2
fertilization
Tree-dominated ecosystems all in temperate or boreal
regions have been exposed to elevated CO
2
through
Free-Air Carbon dioxide Enrichment (FACE), Open
Top Chamber (OTC), and Whole Tree Chamber (WTC)
experiments. Given the logistical difficulties of elevat-
ing CO
2
in forests with tall canopies, the majority of
these experiments have been performed on young
forests or trees, with only one FACE experiment in a
mature forest to date (Table S1).
Elevated CO
2
consistently enhances photosynthesis,
or GPP at the ecosystem level (Ceulemans & Mousseau,
1994; Curtis & Wang, 1998; Ainsworth & Long, 2005;
Hyv
onen et al., 2007). In young forests, this results in
increased NPP and biomass; at least at the onset of the
experiment (DeLucia et al., 1999; Norby et al., 2005).
However, whereas substantial NPP and biomass
increases have occurred at the onset of experiments,
this NPP stimulation has persisted in some but not all
forests (Oren et al., 2001; Seiler et al., 2009; McCarthy
et al., 2010; Norby et al., 2010). Moreover, this response
becomes less consistent as forests become older, and
NPP did not increase in the only mature forest exposed
to elevated CO
2
(Fig. 3; K
orner et al., 2005; Bader et al.,
2009). Similarly, leaf and fine root biomass are consis-
tently stimulated in young forests, but may decline in
old forests (Fig. 3; K
orner et al., 2005; Bader et al., 2009).
Thus, although there is strong evidence that CO
2
fertil-
ization increases the rate of biomass accrual in young
forests, a question remains as to whether elevated CO
2
increases the biomass and productivity of mature for-
ests (Fig. 1; K
orner et al., 2005; Hyv
onen et al., 2007;
Norby & Zak, 2011). In large part because of this uncer-
tainty, it remains unclear whether the net carbon
balance of mature forests will increase in response to
CO
2
fertilization (Fig. 3).
The ability of forests to sustain increased NPP under
elevated CO
2
as they age and, ultimately, the potential
for mature forests to increase C storage under elevated
CO
2
depends in large part upon biogeochemistry. One
potential explanation of observed declines in NPP stimu-
lation under elevated CO
2
as forests age is that increased
productivity immobilizes nutrients in woody tissue or soil
organic matter such that soil N and other nutrients
needed to sustain growth become depleted and may
eventually limit growth (Luo et al.,2004).ProgressiveN
limitation can be alleviated through a variety of mecha-
nisms: trees can increase their N use efficiency, invest
more C in belowground nutrient acquisition, or access
deep N pools (McKinley et al.,2009;Iversen,2010;Drake
et al.,2011b;Norby&Zak,2011).Nlimitationcanalsobe
mitigated if greater N mineralization occurs under high
CO
2
,orifN
2
fixation is stimulated by elevated CO
2
(Zanetti et al.,1996;Hungateet al.,2004;Luoet al.,2004;
Hoosbeek et al.,2011;Norby&Zak,2011).Earlywork
suggested that N mineralization declines under elevated
CO
2
(Hungate et al.,1999),butmorerecentstudiessug-
gest that there can be a priming effect through time from
increased atmospheric CO
2
that stimulates soil micro-
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
FOREST RECOVERY UNDER CLIMATE CHANGE 5
bial activity, which in turn degrades slowly cycling
organic matter pools and release mineral N (Carney
et al.,2007;Langleyet al.,2009;Drakeet al.,2011b).
Elevated CO
2
may also increase N availability by
increasing labile C to drive the energetics of N
2
fixation (Hungate et al.,1999).However,ina
scrub-oak system in Florida, N
2
fixation was negatively
impacted by 7 years exposure to elevated CO
2
(Hun-
gate et al., 2004), and N
2
-fixation rates have continued
to decline perhaps due to canopy closure and light
limitation (Duval, 2010). Thus, N deficiency may be
avoided and NPP stimulation sustained over time
through a variety of mechanisms; however, it remains
uncertain whether this can continue indefinitely or
whether NPP stimulation in all forests would eventu-
ally decline given sufficient time (Hyv
onen et al., 2007;
Norby & Zak, 2011).
The responses of tree growth to elevated CO
2
are
variable among species (Bazzaz, 1990; Saxe et al.,
1998; Pe~
nuelas et al., 2001; K
orner et al., 2005; Seiler
et al., 2009; Dawes et al., 2011), and differential spe-
cies responses have commonly been observed in
CO
2
-enrichment experiments (Table S1). For exam-
ple, of the three codominant canopy tree species
(Fagus sylvatica,Quercus petraea,Carpinus betulus) in
the mature deciduous forest exposed to elevated
Fig 3 Schematic diagram illustrating typical forest successional trajectories under ambient climate (solid lines; as reviewed in Table 1)
and how these are affected by experimental CO
2
fertilization, warming, and drought (increases in blue, decreases in red; color satura-
tion scales with certainty). Responses to CO
2
and climate change are based on a comprehensive review of experimental studies (Tables
S1S3). Responses are considered to have high certainty when observed in multiple sites and low certainty when observed in only one
study. *Indicates a response that is time dependent; it may change from negative to positive as increased N mineralization stimulates
biomass growth (Melillo et al., 2011).
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
6K. J. ANDERSON-TEIXEIRA et al.
CO
2
, shade-tolerant Fagus exhibited increased annual
basal area increments in response to CO
2
in two of
four treatment years, whereas growth of the other
species remained the same or declined (K
orner et al.,
2005). Similarly, proportional species’ contributions
to whole-ecosystem productivity shifted in a Florida
scruboak ecosystems exposed to elevated CO
2
:
dominant Quercus myrtifolia exhibited strong biomass
growth, Q. chapmanii exhibited less of an effect, and
subdominant Q. geminata showed no growth stimu-
lation (Dijkstra et al., 2002). Thus, differential species
growth responses consistently alter proportional spe-
cies’ contributions to whole-ecosystem productivity
and will likely change the composition of future
communities.
Understory vegetation can influence ecosystem func-
tioning and future community composition (Nilsson &
Wardle, 2005) and, therefore, impacts of global change
on juvenile trees and influential nontree species serve
as a window into the forests of the future. Moreover, as
the majority of forest biodiversity is in the understory
stratum, impacts on understory species as well as sym-
biotic mycorrhizal fungi bear consequences for tree
recruitment, carbon cycling, forest health and biodiver-
sity (Gilliam, 2007). Understory community responses
to CO
2
enrichment have been commonly observed
(Table S1). At ORNL-FACE, the woody understory
increased in importance relative to the total stand and
to herbaceous plants, indicating a potential acceleration
of succession under elevated CO
2
(Souza et al., 2010).
Consistent with earlier work using pots and growth
chambers (Bazzaz & Miao, 1993; Kubiske & Pregitzer,
1996; Kerstiens, 1998, 2001; H
attenschwiler & K
orner,
2000), CO
2
enrichment at DukeFACE tended to favor
slow-growing, shade-tolerant species with low rates of
productivity in understory conditions, again suggesting
that succession may be accelerated in temperate forests
under future conditions, with implications for bio-
sphereatmosphere carbon feedbacks (Mohan et al.,
2007). In addition, CO
2
enrichment may favor woody
vines (lianas; e.g., Sasek & Strain, 1990). This has been
observed in two FACE studies (Table S1); for example,
at DukeFACE, the woody vine poison ivy (Toxicoden-
dron radicans) growth was disproportionately enhanced
under elevated CO
2
(Mohan et al., 2006). Lianas have
been expanding in abundance in many regions of the
world often to the detriment of recruiting and mature
trees (Dillenburg et al., 1995; Ingwell et al., 2010; Schnit-
zer & Carson, 2010; Schnitzer & Bongers, 2011) and
the positive feedback of elevated CO
2
for vines may
hinder the establishment of secondary forests globally.
Thus, increasing atmospheric CO
2
may substantially
alter the rate and pathway of succession as well as the
composition of mature forest communities (Fig. 1).
Responses to warming
Over the last three decades, several tree-dominated eco-
systems of various ages almost all in temperate and
boreal regions have been exposed to experimental
warming (Table S2). These experiments have warmed
either aboveground vegetation or the soil (through use
of buried cables); there are few soil-and-air warming
experiments done at the scale of canopy trees (Slaney
et al., 2007; Bronson & Gower, 2010).
Soil warming in northern forests results in faster
decomposition and microbial processing of soil C and
N, which directly releases more CO
2
to the atmosphere
because of enhanced soil respiration (Table S2; Rustad
et al., 2001; Melillo et al., 2002, 2011). By increasing N
mineralization rates, soil warming can have an indirect
N fertilization effect, which generally increases above-
ground production and lowers C allocation to fine root
biomass (Fig. 3; Zhou et al., 2011). The net ecosystem C
balance in response to warming depends largely on the
counteracting effects of C release through increased soil
respiration and C sequestration through increased bio-
mass growth (Fig. 3); in a 60- to 70-year-old even-aged
oakmaple forest in central Massachusetts subjected to
7 years of soil warming (Harvard Forest), soil C losses
were increasingly offset by stimulated growth of can-
opy trees (after a lag of several years; Melillo et al.,
2011; Butler et al., 2012). Additional changes may be
driven by aboveground warming; over the first few
years of warming in a 12-year-old black spruce (Picea
mariana) plantation in Manitoba, soil respiration
increased under soil warming but decreased under
soil-and-air warming (Bronson et al., 2008). In this
study, elevated soil and air temperatures increased
spruce tree shoot growth (Bronson et al., 2009) but did
not change rates of photosynthesis or autotrophic respi-
ration (Bronson & Gower, 2010). Much remains to be
learned about how warming affects whole forested eco-
systems, particularly in subtropical and tropical forests,
where only one warming experiment has been con-
ducted to date (Cheesman & Winter, 2012). Moreover,
although we may posit that forest age modulates
warming responses based on the magnitude of struc-
tural and functional changes associated with forest
recovery (Table 1), there is of yet no clear evidence that
the direction of forest responses to warming varies by
age (Fig. 3).
Growth responses to warming vary among tree spe-
cies (Table S2), and this is likely to affect successional
dynamics and forest composition. For example,
although the large oaks at Harvard forest accounted for
the majority of C uptake and storage in woody tissue,
smaller maples exhibited a greater stimulation of
growth in response to soil warming stimulation (Mel-
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
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FOREST RECOVERY UNDER CLIMATE CHANGE 7
illo et al., 2011; Butler et al., 2012; Mohan et al., unpub-
lished results). Similarly, a warming experiment in a
recently timbered oakhickory forest in Pennsylvania
found altered phenology (with differential responses
among species) and community composition (Rollin-
son, 2010; Rollinson & Kaye, 2011). Thus, warming is
likely to alter species’ growth and phenology and,
thereby, the rate and pathway of succession and ulti-
mately the community composition of mature forests
(Fig. 1).
Responses to altered precipitation
There have been a number of precipitation manipula-
tion experiments in forests of a range of ages spanning
from boreal to tropical regions (Table S3; Beier et al.,
2012). Across this range of climates and forest ages,
tree growth and survival were generally increased by
water addition and reduced by water removal (Fig. 3;
e.g., Hanson et al., 2001; Nepstad et al., 2002; Plaut
et al., 2012; Vasconcelos et al. (2012), as was GPP or
NPP at the ecosystem level (Nepstad et al., 2002; Al-
berti et al., 2007). Soil respiration rates also tended to
increase under irrigation and decrease under drought
(Table S3; e.g., Conant et al., 2000; Sotta et al., 2007).
However, water addition only accelerated forest C
cycling up to a point; some more mesic forests did not
respond to precipitation manipulation (De Visser et al.,
1994; Bergh et al., 1999) or had accelerated C cycling
under reduced precipitation (Cleveland et al., 2010).
Sensitivity to precipitation manipulation often varied
by size class, but results were mixed as to whether
small or large trees were more sensitive (Hanson et al.,
2001; Nepstad et al., 2007). Whereas altered precipita-
tion had a strong effect on seedling emergence and
survival (Richter et al., 2012; Volder et al., 2012) and at
times had a stronger effect on small than on large trees
(Hanson et al., 2001), there were also instances where
exposed canopy trees suffered greater drought-related
stress (Nepstad et al., 2007; Schuldt et al., 2011). Thus,
within-stand relationships between tree age and
drought sensitivity do not necessarily mirror across-
stand relationships, where growth sensitivity to varia-
tion in water availability declines with stand age
(Table 1). As with experimental manipulation of CO
2
and temperature, differential species responses were
commonly observed under precipitation manipulation
experiments (Table S3; e.g., Yavitt & Wright, 2008),
portending future changes to community composition
under altered precipitation regimes. Thus, in sum-
mary, precipitation manipulation experiments have
demonstrated that water availability affects rates of
forest recovery, mature forest states, and probably suc-
cessional pathways (Figs 1 and 3).
Responses to multivariate environmental manipulation
Joint effects of altered CO
2
, temperature, and precipita-
tion are rarely purely additive (Dieleman et al., 2012),
and understanding the interactive effects produced by
combined manipulations remains an important chal-
lenge. Experimental manipulation of more than one of
these elements in a factorial design has occurred in sev-
eral intact forests or experimental mesocosms (Tables
S1S3). These studies demonstrate that tree growth and
carbon cycling in young forests are generally acceler-
ated under combined higher CO
2
, warmer, and wetter
conditions (Tables S1S3; e.g., Wan et al., 2004;
Comstedt et al., 2006; Slaney et al., 2007; Tingey et al.,
2007; Bauweraerts et al., 2013). In addition, different
species have responded differently to different ele-
ments of climate change; for example, at the alpine tree
line in Switzerland, growth of Larix decidual responded
positively to CO
2
but was unresponsive to soil warm-
ing, whereas Pinus cembra had a slight positive response
to warming but responded minimally to CO
2
(Dawes
et al., 2011). The limited number of studies and the
complexity of multifactor experiments make it prema-
ture to generalize about how forests of different ages
will respond to interactive elements of global change.
However, observed responses of forests to the environ-
mental change that has already occurred to which we
turn next reveal how secondary forests are respond-
ing to multivariate climate change to date.
Altered forest recovery under contemporary
multivariate environmental change
Historical reconstructions indicate that forests of all
ages have responded to the changes in CO
2
and climate
that have already occurred. By nature, these historical
records do not directly separate the effects of CO
2
, tem-
perature, and precipitation from one another and from
other potentially confounding environmental changes
(e.g., atmospheric deposition, ozone, management,
altered disturbance regimes). Rather, they provide a
picture of how the dynamics of forest recovery are
responding to contemporary multivariate environmen-
tal change.
Tree-ring and observational records extending back
decades to centuries have demonstrated the climate
dependence of forest productivity. Tree-ring records
have revealed increasing growth rates in numerous
forests including high-elevation forests in western
Washington (Graumlich et al., 1989), conifers in the
white mountains of California (Lamarche et al., 1984;
Salzer et al., 2009), Pinus ponderosa forests in the US
Pacific northwest (Soul!
e & Knapp, 2006), aspen (Popu-
lus tremuloides) secondary forests in Wisconsin (Cole
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
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8K. J. ANDERSON-TEIXEIRA et al.
et al., 2010), Abies and Quercus forests in France (Bec-
ker, 1989; Becker et al., 1994), and numerous other for-
ests throughout Europe (Spiecker, 1999; Babst et al.,
2013). These increased growth rates are generally
attributable to increased atmospheric CO
2
, tempera-
ture, or moisture (e.g., Graumlich et al., 1989; Soul!
e&
Knapp, 2006; Salzer et al., 2009; Cole et al., 2010). In
contrast, tree growth rates have decreased in response
to warming or drought stress in many other forests
around the world (Allen et al., 2010), including white
spruce (Picea glauca) in interior Alaska (Barber et al.,
2000), conifers in the southwest United States
(Williams et al., 2013), and tropical forests in Panama,
Malaysia, and Costa Rica (Feeley et al., 2007b; Clark
et al., 2010). Similarly, a review documenting evidence
of altered forest productivity over the last half century
indicates that the productivity of many forests is
increasing whereas that of others is declining (Boisve-
nue & Running, 2006). Although powerful for under-
standing the historical influence of climate on forest
productivity, these records are limited in that they do
not characterize responses across a range of forest
ages.
By comparing biomassage relationships (deter-
mined through a chronosequence approach) with cur-
rent biomass accumulation rates in forests of various
ages (determined through repeated sampling), a couple
of studies have identified accelerated biomass accumu-
lation in forests following stand-clearing disturbances.
Specifically, accelerated biomass accumulation has been
observed in temperate deciduous forests in the eastern
United States (McMahon et al., 2010a; see also Foster
et al., 2010; McMahon et al., 2010b) and in temperate-
maritime forests in the Pacific northwest (Fig. 4; Hem-
ber et al., 2012). Likely explanations of these increases
in secondary forest biomass accumulation rates include
increased atmospheric CO
2
, increased temperature,
increased moisture, and increased growing season
length (McMahon et al., 2010a; Hember et al., 2012).
Thus, climate change appears to be increasing the rate
of forest regrowth in some temperate forests; however,
parallel studies have yet to be conducted in other
regions.
The long time frame of forest recovery precludes
comparison of forests that have matured under differ-
ent climates, which would be necessary to determine
whether climate change is altering recovery trajectories
such that forests converge to an altered state as they
mature (Fig. 1). However, long-term monitoring of
mature forests can provide evidence as to whether
climate change is affecting the state of forests that
matured under past climates. Long-term monitoring of
old-growth forests provides mixed evidence as to
whether their total carbon storage capacity is changing;
many old-growth forests throughout the world appear
to be net C sinks (Baker et al., 2004; Luyssaert et al.,
2007; Chave et al., 2008; Lewis et al., 2009); however,
this effect is diminished at larger spatiotemporal scales
of measurement (Clark, 2002; Feeley et al., 2007a; Chave
et al., 2008). There is strong evidence of directional
change in community composition of forests through-
out the world; for example, long-term records from the
50 ha forest dynamics plot on Barro Colorado Island,
Panama, indicate increased dominance of drought-
tolerant species (Feeley et al., 2011). In addition, there
have been general increases in forest die-back globally
a phenomenon attributed to climate changetype
drought (Breshears et al., 2005; Allen et al., 2010;
Williams et al., 2013).
Thus, there is evidence of historical change in both
rates of forest regrowth and the state of forests that
matured under past climates. There is also some evi-
dence of changing successional trajectories driven by
altered community dynamics (reviewed below).
Although concurrent changes in multiple environmen-
tal factors including atmospheric CO
2
, climate, atmo-
spheric deposition, herbivore communities, disturbance
regimes, and management make it difficult to isolate
the cause of these changes, their global distribution and
directional correlation with trends in CO
2
and climate
provide strong evidence that they are at least partially
attributable to increasing atmospheric CO
2
and climate
change.
Fig. 4 Evidence of increasing rates of biomass accumulation in
coastal Douglas fir (Pseudotsuga menziesii) and western hemlock
(Tsuga heterophylla) forests in southwest British Columbia, Can-
ada. Plotted is the residual average biomass increment (B) from
1267 permanent inventory plots after correction for factors
including stand age, site quality, nitrogen availability, and
biomass (the five lines represent different correction methods,
as detailed in Hember et al., 2012). Linear regression represents
a significant positive trend. Reprinted from Hember et al. (2012).
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
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FOREST RECOVERY UNDER CLIMATE CHANGE 9
Community dynamics and the potential for state
changes
Successional pathways may be altered when elevated
CO
2
and climate change affect community dynamics,
either directly through differential effects on the perfor-
mance of various species and size classes or indirectly
through altered disturbance regimes and consequent
competitive outcomes.
Climate change will alter community dynamics by
altering the physical environment in which species of
varying physiological strategies are competing. Experi-
mental climate change manipulations (reviewed above;
Tables S1S3) and decades of forestry research on the
climate sensitivity of forest regeneration (Fowells &
Stark, 1965; Ferrell & Woodard, 1966; Thomas & Wein,
1985) have demonstrated that increased CO
2
and
altered climate will differentially affect growth rates of
trees by size and species, thereby altering population
dynamics, competitive interactions, and species compo-
sition of both young and mature forests. In addition,
climate change can differentially favor or inhibit com-
mon forest pathogens, providing another mechanism of
impact on community structure (reviewed by Sturrock
et al., 2011). Such community changes can affect ecosys-
tem function, altering production, C stocks, and biogeo-
chemistry. For example, model predictions of climate
change effects on forest productivity can be very differ-
ent if the community is allowed to develop dynami-
cally, compared with using parameters based on
average forest characteristics, which is a common prac-
tice in biogeochemical models examining the effects of
climate change (Bolker et al., 1995).
Beyond its direct effects on the dynamics of forest
recovery through physiological mechanisms, climate
change may also impact successional pathways indi-
rectly by altering the frequency, timing, severity, and
spatial extent of disturbances including fires, droughts,
storms, floods, and herbivore or pathogen outbreaks
(e.g., Dale et al., 2001; Westerling et al., 2006; Allen
et al., 2010; Sturrock et al., 2011). Frequency and inten-
sity of disturbance have been theoretically shown to
have very different effects on community diversity
(Miller et al., 2011; in determining microcosm diversity
(Hall et al.,2012).Thus,changesindisturbancefrequency
and intensity have the potential to shift community
composition, even when species are restricted to (and
are still viable in) their historic ranges. Moreover, large
changes to disturbance regimes are not required to
facilitate changes in community composition; in the
annual plant model of Miller et al. (2011), changing
disturbance mortality by just a few percentage points
can send a species to extinction. Changes in community
composition driven by altered disturbance regimes
may have dramatic consequences for ecosystem func-
tioning. For example, in Alaskan boreal forests, increas-
ing fire frequency and severity have shifted
competitive dominance from conifers to deciduous spe-
cies, affecting biomass and soil C accumulation, albedo,
and energy partitioning (Beck et al., 2011).
Disturbance can also provide niche opportunities for
invaders (Shea & Chesson, 2002), and the successful
invasion can dramatically alter successional trajectories
and also feedback to further modify disturbance
regimes (Mack & D’Antonio, 1998). Although distur-
bances are commonly believed to increase invader suc-
cess, recent work suggests that it is changes to
disturbance regimes, rather than disturbance events per
se that most strongly influence a communities’ suscepti-
bility to invasions (Moles et al., 2012). In this light,
climate change is likely to change the composition of
some communities by altering disturbance regimes to a
point where invader species can become dominant.
In some cases, climate change may push forests past
critical thresholds such that, upon perturbation, they
undergo drastic changes in community composition
and ecosystem properties (‘catastrophic shift’) and fail
to return to their previous state (Fig. 5). In many sys-
tems, the observed state of the community is not the
only possible stable state; a variety of empirical results
demonstrate the existence of alternative stable states in
nature (D’Antonio & Vitousek, 1992; Savage & Mast,
2005; Schr
oder et al., 2005; Odion et al., 2010; Scheffer
et al., 2012). Large changes in the environment can
bring about large changes in ecosystems, but smooth,
gradual changes in abiotic conditions also can cause
abrupt shifts in ecosystem properties and functioning
(Scheffer et al., 2001). Systems that are structured by
disturbance and are susceptible to abiotic forcing (such
as regenerating forests) may be more likely to display
alternative stable states (Didham et al., 2005). When dis-
turbance keeps systems in perpetual flux, as is the case
for many forests, no true stable equilibrium (in the clas-
sical, dynamical systems sense) is reached. Instead, for-
ests undergo periodic cycles of disturbance and
regeneration, and it is these cycles that constitute the
‘state’ of the system.
Many forests are resilient (sensu Grimm & Wissel,
1997) to commonly experienced disturbances, but
effects of climate change, such as changes to the distur-
bance and precipitation regimes, can change the
composition and productivity of forest communities
(Thompson et al., 2009), forcing the system into
different cyclical behaviors. Although different initial
trajectories can lead to different mature forest states,
there is also the possibility that different initial trajecto-
ries can lead to the same mature state, or that similar
initial trajectories can lead to distinct mature states
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
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10 K. J. ANDERSON-TEIXEIRA et al.
(Fig. 1, ‘alternative transient states’ sensu Fukami &
Nakajima, 2011).
In some forested regions, the existence of alternative
stable states implies that forests may not return to their
previous state following disturbance. A general mecha-
nism underlying such alternative stable states is that
seedlings and young forests are often more vulnerable
to disturbances such as drought, herbivory, and fire
than their mature counterparts (Table 1; Stromayer &
Warren, 1997; Thompson & Spies, 2010). As a result,
conditions that support the persistence of mature
forests may not be amenable to forest regeneration. For
example, following fire, conifer regeneration may be
delayed or prevented by drought or competitive inhibi-
tion by grasses or shrubs (Savage & Mast, 2005;
Roccaforte et al., 2012). There are also systems in which
postfire establishment of pyrogenic vegetation or
vulnerability of young stands to crown fire reduces the
probability of forest regeneration (D’Antonio & Vitousek,
1992; Savage & Mast, 2005; Thompson & Spies, 2010;
Staver et al., 2011). For example, in the Klamath region
of Oregon and California, high-intensity fire shifts the
community from a high-biomass mixed conifer forest
to a pyrogenic low-biomass shrubchaparralhard-
wood community, in which state it may be maintained
by subsequent fires of any intensity (Odion et al., 2010;
Thompson & Spies, 2010). Alternative stable states may
also be driven by hydrologic, microclimatic, or biogeo-
chemical mechanisms; for example, postfire forest
resilience may be impacted by changes to soil biogeo-
chemistry and hydrological functioning (Ffolliott et al.,
2011; Smithwick, 2011).
Climate change may gradually alter the landscape of
alternative states, having minimal impact on mature
forests, but shifting conditions such that forests will be
unlikely to reestablish following disturbance (Fig. 5).
The probability of forest regeneration may be reduced
by mechanisms such as reduced probabilities of seed-
ling establishment under more arid conditions, reduced
competitive advantage of seedlings relative to grasses
or shrubs, or increases in disturbance frequency or
severity. Although ecological theory points toward the
risk that some forests may unlikely to return to their
previous state following stand-clearing disturbance as a
result of global change (Fig. 5), empirical evidence
remains scant. In the southwestern United States, pon-
derosa pine forests meet the criteria for forests that may
be vulnerable to climate change-induced catastrophic
shifts and are often failing to reestablish following fire
(Dore et al., 2008; Roccaforte et al., 2012); however, a cli-
mate change mechanism has not been demonstrated.
Understanding the potential for climate change to dra-
matically alter or prevent postdisturbance recovery
remains an important challenge.
Thus, based on empirical findings and theoretical
concepts, community composition and ecosystem func-
tion of regenerating forests under climate change are
likely to change, both quantitatively, and in terms of
stability. Given that climate change, disturbance
regimes, and community dynamics interact in complex
ways to shape ecosystems, correctly predicting the
behavior of forests over the next century will require
greater understanding of the potential for altered com-
munity dynamics to dramatically impact carbon
cycling, biogeochemistry, and ecosystematmosphere
exchanges.
Ecosystem and earth system model projections
Ecosystem and earth system models (ESMs) provide a
means to project dynamically how ecosystems will be
impacted by multiple interacting environmental
changes over spatiotemporal scales that exceed the
limits of observation and experimentation. ESMs vary
in complexity from fully coupled global circulation
Fig. 5 Schematic diagram illustrating the potential for
disturbance to force ecosystems from one stable state to another
as the climate changes. Colored shapes represent the landscape
of stable ecosystem states under different climate regimes, and
balls represent states in which ecosystems can stably exist in
this case, the state to which the system converges at maturity
(which will be associated with a stable disturbancerecovery
regime). The plot below illustrates hysteresis, wherein alternate
stable states exist. As the climate changes, basins of attraction
shift such that the stable state at maturity eventually switches
from one state to the other. During the transition, however, dis-
turbance (indicated by black arrow) may hasten the shift from
one stable state to another. Modified from Scheffer et al. (2001).
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
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FOREST RECOVERY UNDER CLIMATE CHANGE 11
models (GCMs), which include two-way feedbacks
between the land, atmosphere, and oceans to make pre-
dictions about climate, to simpler models with less
interaction between the earth system components (e.g.,
one-way feedbacks to the atmosphere such as land-
cover changes to net terrestrial CO
2
uptake). ESMs
include land components embedded with physiological
and biogeochemical mechanistic representations of the
interactions between vegetation, the atmosphere, and
either prognostic disturbances (i.e., fire) or prescribed
disturbances (i.e., harvest). Vegetation is represented in
terms of broadly defined plant functional types (PFTs;
e.g., temperate conifers). When coupled with a specific
class of ecosystem models (dynamic global vegetation
models; DGVMs), processes are included that allow
vegetation type to change based on climate conditions
(e.g., forest to grassland or woodland). Recent advance-
ments to some ESMs (CESM/CLM4.0, ORCHIDEE,
TEM) now include dynamic response variables for the
long-term physiological changes related to CO
2
and/or
temperature (Krinner et al., 2005; Thornton et al., 2007;
Zaehle & Friend, 2010). The complexity of these models,
and the variety of factors upon which model predic-
tions and associated uncertainty depend, preclude the
possibility of any one model incorporating all of the
known complexity of forest regeneration. However, for
models to make predictions about forest recovery
following disturbance, they need to be able to capture
the interactive effects of changing environmental condi-
tions and disturbance on forest recovery dynamics.
No model pays detailed attention to the roles of for-
est age and successional changes in species composition
in shaping the dynamics of forest recovery. Rather,
regenerating forests are generally parameterized as
mature forests, although sometimes there are two age
classes (e.g., fire BGC; Smithwick et al., 2009), and car-
bon allocation to wood may vary dynamically with age
(e.g., CLM4; Hudiburg et al., 2013). We are aware of
only one model where C allocation to nonwoody
components or physiology changes dynamically with
age (and this improves performance in describing age
trajectories of woody productivity; Davi et al., 2009).
Changes in community composition (i.e., PFTs), physi-
ological differences between early- and late- succes-
sional species, and age structure within a forest
(Table 1) generally are not incorporated (exception is
ED2; Medvigy et al., 2009). As a result, models have
difficulty accurately reproducing trajectories of change
in biomass or other components of the C cycle associ-
ated with forest age (Table 1). Nevertheless, to the
extent that forest responses are consistent across age
classes (Fig. 3), models can predict productivity
responses of young forests to elevated CO
2
and climate
change. Simulated climate change effects on forest
growth vary by model, region, and climate change sce-
nario; the direction of change in forest growth is
expected to vary regionally and to depend on the
course of atmospheric CO
2
and climate change
(Kirilenko & Sedjo, 2007). For example, in lodgepole
pine (Pinus contorta) forests regenerating from fire in
the Yellowstone region, woody production, live
biomass, N mineralization, and total ecosystem C are
projected to increase under two different future climate
scenarios, with percent increase depending on the cli-
mate scenario (Smithwick et al., 2009). Thus, models
demonstrate likely changes in forest productivity under
future climates; however, without giving specific atten-
tion to changes in physiology and C allocation with for-
est age, they say little about the responses of
regenerating forests specifically.
Because disturbance type, severity, size, and fre-
quency affect postdisturbance C dynamics and biogeo-
chemical cycling (Amiro et al., 2010; Smithwick, 2011),
future trajectories of forest recovery are likely to be dri-
ven by climate changedisturbance type interactions. In
most models, disturbance events are generally imple-
mented by altering forest biomass pools through remo-
vals (harvest), combustion (fire), or transfer of live to
dead material (insect outbreaks), with the amount
transferred scaled to disturbance severity. For fire and
insect outbreaks, the timing of transfer of biomass to
litter and forest floor components varies because tree
death can occur slowly, and snag fall rates are depen-
dent on a variety of factors including forest type
(Campbell et al., 2007; Edburg et al., 2011). At this time,
we are unaware of any model capable of representing
the specific dynamics (e.g., recruitment, altered hydrol-
ogy, or biogeochemistry) associated with distinct dis-
turbance types, severities, and sizes. Therefore, models
currently say little about how changing disturbance
severity and size are likely to impact forests; however,
they do reveal how altered disturbance frequency is
likely to impact forests. For example, in the Yellow-
stone region, fire burn area and frequency are projected
to increase under a range of future climate scenarios,
quite possibly to the extent that current forest commu-
nities will have insufficient time to recover before the
next fire event, making the current suite of conifer spe-
cies unlikely to persist (Westerling et al., 2011). Thus,
models demonstrate that climate change is likely to
have significant impacts on forested landscapes
through its influence on disturbance regimes.
Despite their uncertainties, ESMs have demonstrated
that forest recovery will be substantially altered under
future climates. Rates of recovery will change, with
direction and magnitude varying regionally and
depending on future courses of atmospheric CO
2
and
climate change. Altered disturbance regimes will inter-
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
12 K. J. ANDERSON-TEIXEIRA et al.
act with altered recovery trajectories, at times driving
biome shifts (Westerling et al., 2011). In combination,
the direct and indirect effects of climate change are pre-
dicted to have substantial impacts on regional C bal-
ances and forestry operations; for example, harvestable
forest biomass in Canada is projected to be reduced
2662% for the 21st century, depending on the model
assumptions of predicted growth rate, soil carbon
decay rate, and area burned by fire (Metsaranta et al.,
2011). However, specific representation of physiological
and community changes associated with forest age
(Table 1) will be required to understand how forest
recovery trajectories will be altered by climate change
(Fig. 1).
Conclusions
As reviewed above, there is strong evidence that
increasing atmospheric CO
2
, warming, and altered
precipitation regimes will alter trajectories of forest
recovery. This conclusion is supported by global patterns
in both forest regrowth rates and biomass of mature
forests (Fig. 2); responses of forests of various ages to
CO
2
, temperature, and precipitation manipulation
(Fig. 3; Tables S1S3); observations of altered forest
recovery under contemporary multivariate environ-
mental change (Fig. 4); our understanding of succes-
sional community dynamics and alternative stable
states (Fig. 5); and models. Because forests undergo
major structural, physiological, biogeochemical, and
compositional changes as they age (Table 1), it is logical
that responses to climate change vary as a function of
forest age (Fig. 3). Depending on differential responses
of forests of different ages, climate change can impact
rates of forest recovery, states of mature forests, and/or
recovery pathways (Fig. 1, Table 2), and understanding
the impact of climate change on forests therefore
requires attention to the role of forest age (Fig. 1).
Through its influence on young forests, climate
change will impact rates of forest recovery (Fig. 1,
Table 2). Multiple lines of evidence point to accelerated
regrowth in mesic northern forests under future climates
(Figs 24; Tables S1S2); however, responses of tropical
forest regeneration rates to elevated CO
2
and increasing
temperature remain uncertain. For forests globally, there
is strong evidence that biomass accumulation rates will
decrease under more arid conditions (Figs 2b and 3;
Table S3) sometimes to the point where forests may
never recover (Fig. 5). Changes to rates of nutrient
accumulation in biomass, biogeochemical cycling, and
community change are likely to parallel responses of
biomass accumulation rate (Table 2).
Climate change will also impact the state toward
which forests converge as they age (Fig. 1; Table 2). A
challenge of central importance is in understanding
how climate change responses of young forests on
which the majority of manipulative experiments have
been performed (Tables S1S3) relate to the ultimate
state of these ecosystems once they reach ‘maturity’
(Fig. 1). For instance, we do not know whether
increased biomass accumulation in young forests will
translate to increased biomass of old forests or whether
these forests will simply attain maximum biomass fas-
ter. The effect of elevated CO
2
on mature forest biomass
and total ecosystem C remains uncertain, although
decreases in either are unlikely; meanwhile, elevated
CO
2
is very likely to result in increased nutrient limita-
tion (Fig. 3; Table S1). Likewise, it remains unclear how
warming will affect mature forest biomass and ecosys-
tem C stocks (Fig. 3); it is likely that aboveground C
stocks will increase in northern climates (Fig. 2c) while
soil C stocks decrease and N mineralization increases
(Table S2). In contrast, changes in water availability
have predictable effects; reduced water availability will
reduce productivity, live biomass, and total ecosystem
C stocks (Figs 2d and 3; Table S3). In all cases, altered
community composition is very likely (Table S3).
Responses of mature forest states to combined changes
in CO
2
, temperature, and precipitation will vary region-
ally, and understanding how the states toward which
future forests will converge as they recovery from dis-
turbance (Fig. 1) remains an important challenge.
Climate change is also likely to impact pathways of
forest recovery (Fig. 1; Table 2), which may occur
through a variety of mechanisms including altered bio-
geochemistry (e.g., decreased N limitation during early
stages due to increased N mineralization), changing
biophysical constraints (e.g., reduced frequency of
years with enough precipitation to support seedling
establishment), or altered community dynamics. As
reviewed above, different species within the same com-
munity commonly have substantially different
responses to altered CO
2
or climate (K
orner et al., 2005;
Mohan et al., 2006, 2007; Seiler et al., 2009; Dawes et al.,
2011), and consequent changes to community structure
may impact ecosystem functioning in ways that cannot
be predicted based solely on characteristic physiologi-
cal responses of dominant taxa (Bolker et al., 1995). For
example, increased liana biomass under future climates
could meaningfully reduce forest biomass (Phillips
et al., 2002; Mohan et al., 2006; Ingwell et al., 2010). Dif-
ferential responses are likely to be most influential early
in succession, when species turnover rate is highest and
trees are most sensitive to environmental variation
(Table 1), and may have an enduring influence on com-
munity composition and ecosystem function (D’Anto-
nio & Vitousek, 1992; Bunker et al., 2005; Beck et al.,
2011; Hooper et al., 2012).
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
FOREST RECOVERY UNDER CLIMATE CHANGE 13
Table 2 Probable climate change impacts on trajectories of several forest properties following disturbance (sensu Fig. 1)
Forest property
Recovery
trajectory
Expected response to climate change
Elevated CO
2
Elevated temperature* Altered water availability Multivariate change
Biomass Rate of
change
Very likely increase. Very likely increase in temperate
and boreal forests; Uncertain
response in tropics.
Very likely increase with water
availability/decrease with
drought stress.
Likely increase in temperate and
boreal forests (absent moisture
stress); Likely decrease under
drought stress; Uncertain response
in tropics.
Mature
state
Uncertain (likely
increase or no change)
Possible changes in some
regions (e.g., increase in cold
regions)
Very likely increase with water
availability/decrease with
drought stress.
Likely changes (region and time
frame specific).
Pathway Likely changes driven
by shifts in community
dynamics,
biogeochemistry, or
biophysics.
Likely changes driven by shifts
in community dynamics,
biogeochemistry, or biophysics.
Likely changes driven by shifts
in community dynamics,
biogeochemistry, or biophysics;
High potential for catastrophic
shift to low-biomass (nonforest)
state under severe drought
conditions.
Likely changes driven by shifts in
community dynamics,
biogeochemistry, or biophysics.
Total C stock Rate of
change
Very likely increases. Likely increase in temperate and
boreal forests; Uncertain
response in tropics.
Very likely increase with water
availability/decrease with
drought stress.
Likely increase in temperate and
boreal forests (absent moisture
stress); Likely decrease under
drought stress; Uncertain response
in tropics.
Mature
state
Uncertain (likely increase
or no change).
Very likely decrease in soil
organic matter, possible
increase in biomass carbon
(higher latitudes). Net balance
uncertain and likely region
specific.
Very likely increase with water
availability/decrease with
drought stress.
Likely changes (region and time
frame specific).
Pathway Likely changes driven by
shifts in community
dynamics,
biogeochemistry, or
biophysics.
Likely concurrent reductions in
soil organic C and increases in
biomass C.
Likely changes driven by shifts
in community dynamics,
biogeochemistry, or biophysics;
High potential for catastrophic
shift to low C (nonforest) state
under severe drought
conditions.
Likely changes driven by shifts in
community dynamics,
biogeochemistry, or biophysics
(region- and time frame specific).
Biogeochemistry Rate of
change
Likely acceleration of
nutrient accumulation in
vegetation; Likely
acceleration of C & N
Likely acceleration of nutrient
accumulation in vegetation in
northern forests; Likely
acceleration of C & N cycling in
temperate and boreal forests;
Likely acceleration of nutrient
accumulation in vegetation
with increased water
availability/rate decrease with
drought stress.
Likely acceleration of nutrient
accumulation in vegetation in
mesic northern forests; Likely rate
decrease under drought stress;
Uncertain response in tropics.
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
14 K. J. ANDERSON-TEIXEIRA et al.
Table 2 (continued)
Forest property
Recovery
trajectory
Expected response to climate change
Elevated CO
2
Elevated temperature* Altered water availability Multivariate change
cycling in temperate and
boreal forests.
Uncertain response in the
tropics.
Mature
state
Likely acceleration of C &
N cycling in temperate
and boreal forests; Likely
decrease in soil N pool;
Uncertainty changes
total nutrient storage in
vegetation.
Likely acceleration of C & N
cycling in temperate and boreal
forests; Likely decrease in soil N
pool; Uncertain response in the
tropics.
Likely decrease in nutrient
limitation under drought stress.
Likely acceleration of C & N cycling
in temperate and boreal forests;
Likely decrease in soil N pool;
Possible increase in total nutrient
storage in vegetation.
Pathway Likely increase in nutrient
limitation.
Likely concurrent reductions in
soil N and increases in biomass N.
Likely changes driven by shifts
in community dynamics.
Likely increase in nutrient
limitation in mesic forests.
Community
composition
Rate of
change
Likely acceleration of
community change.
Likely acceleration of
community change; Uncertain
response in the tropics.
Uncertain (drought may reduce
the rate of community change
through retarded plant growth
or enhance it by increasing
mortality).
Likely acceleration in temperate
and boreal forests (absent moisture
stress); Uncertain response in
tropics.
Mature
State
Very likely alteration of
mature community
composition driven by
differential species
responses; Likely
increase in liana
abundance.
Very likely alteration of mature
community composition driven
by differential species
responses.
Very likely alteration of mature
community composition driven
by differential species
responses.
Very likely alteration of mature
community composition driven by
differential species responses;
Likely increase in non-native
species.
Pathway Very likely alteration
driven by differential
size- and species
responses, sometimes
causing shift to
alternative state.
Very likely alteration driven by
differential size- and species
responses, sometimes causing
shift to alternative state.
Very likely alteration driven by
differential size- and species
responses, sometimes causing
shift to alternative state.
Very likely alteration driven by
differential size- and species
responses, sometimes causing shift
to alternative state.
*Elevated temperature responses assume no change in moisture stress; responses to changes in water availability are listed in ‘Altered water availability’ column.
‘Rate of change’ refers to the rate at which the forest approaches its mature state. ‘Mature state’ refers to the state to which forests converge as they age. ‘Pathway’ refers to the
sequence of states through which any given ecosystem property passes and the relative amount of time spent in each.
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
FOREST RECOVERY UNDER CLIMATE CHANGE 15
In the most dramatic cases, altered successional
pathways may result in catastrophic shifts to an
alternate stable state (e.g., a forest to grassland tran-
sition; Fig. 5). There are documented instances
where, following disturbance, young forests fail to
establish or persist under conditions that are amena-
ble to persistence of mature forests (Thompson &
Spies, 2010; Roccaforte et al., 2012). When these con-
ditions are linked to climate, as they often are (e.g.,
sufficient moisture for seedling establishment, fire
regime), climate change is likely to force a transition
to an alternate stable state (Fig. 5). As a result,
directional changes to forest ecosystems that would
happen gradually in the absence of disturbance may
be greatly accelerated by disturbance (Fig. 5).
There remain several important unanswered ques-
tions regarding the impact of climate change on the
dynamics of forest recovery:
(1) How does forest age modulate responses to climate
change? Forests of different ages have responded differ-
ently to climate manipulations (Fig. 3; Tables S1S3);
however, at this point climate manipulation experi-
ments provide only circumstantial evidence of age dif-
ferences in climate change response. Systematic
comparison of responses of forests of different ages to
experimental CO
2
or climate manipulation and to natu-
ral climate variability will be crucial to understanding
and modeling climate change impacts on forests of all
ages.
(2) How will successional trajectories differ under future
climates? Beyond understanding how age modulates
forest responses to climate change, we face the chal-
lenge of understanding how climate change will impact
entire trajectories of forest recovery (Fig. 1). It is impor-
tant to note that, because the climate history under
which a stand has developed affects its current state
and future trajectory, changes to entire trajectories can-
not be understood simply by integrating across
responses of forests different ages. Rather, it will be
important to understand how altered biogeochemical
dynamics and community composition shape succes-
sional pathways and the states toward which forests
converge as they mature.
(3) Where and when will state changes occur? Climate
change-driven regime shifts (Fig. 5) will have dramatic
consequences, yet they remain difficult to document
and predict. There is a need for experimental, observa-
tional, and modeling studies to identify the conditions
under which such shifts are likely and the mechanisms
through which they may occur.
(4) How will tropical forest regeneration respond to cli-
mate change? Although tropical forests are well repre-
sented in global-scale comparisons (Fig. 2),
precipitation manipulation experiments (Table S3), and
long-term monitoring of mature forests (e.g., Chave
et al., 2008), we are aware of only one study manipulat-
ing CO
2
or temperature at the whole-tree level in a field
setting in the tropics (Cheesman & Winter, 2012). This
constrains our ability to predict climate change
responses of tropical forests. Understanding how
climate change will affect tropical forest regeneration is
particularly important given the widespread use of
slash-and-burn agriculture in the tropics and the signif-
icant role of tropical forest regrowth in the global C
cycle (Pan et al., 2011).
An additional challenge lies in improved representa-
tion of forest recovery dynamics in ESMs, which are
currently simplistic in their treatment of forest recovery
dynamics. Although detailed representation of forest
recovery dynamics in global models is infeasible, we
believe that two advances will be important to improv-
ing the treatment of forest regeneration. First, the most
important stand age-dependent physiology and alloca-
tion strategies (driven by aging of dominant species
and changes in species composition) should be identi-
fied and incorporated. This will allow improved repre-
sentation of the dynamics of forest recovery in current
and future climates. Importantly, this will help to iden-
tify situations where young forests fail to establish
despite the persistence of their mature counterparts,
suggesting climate change-driven regime shifts (Fig. 5).
Second, although modeling individual species in ESMs
is infeasible, it will be necessary to represent the conse-
quences of demonstrated variability in species
responses to climate change and inevitable resultant
shifts in community composition and ecosystem pro-
cesses. With changing community composition, the net
ecosystem response may differ significantly from that
which would be predicted based on mean characteris-
tics of the original community (Bolker et al., 1995). In
the most dramatic cases, altered competitive interac-
tions may result in a regime shift from forest to a grass-
or shrub-dominated state (Fig. 5). Predicting regime
shifts in ESMs will be particularly important, as these
imply feedbacks to the climate system through altered
C storage, albedo, and hydrology.
Changes in the dynamics of forest recovery following
disturbance will result in potentially significant climate
feedbacks. Altered disturbancerecovery dynamics may
impact the C cycle enough to reverse the sign of a regio-
nal C cycle feedback (Kurz et al., 2008; Running, 2008;
Metsaranta et al., 2011). Moreover, albedo and evapo-
transpiration are important components of the climate
regulation services of ecosystems (Anderson-Teixeira
et al., 2012), change systematically over the course of for-
est recovery (Randerson et al., 2006; Kirschbaum et al.,
2011; Jin et al., 2012; O’Halloran et al., 2012), and may
shift substantially in response to climate change partic-
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
16 K. J. ANDERSON-TEIXEIRA et al.
ularly if the new community differs dramatically from
the old (Beck et al., 2011). Altered forest recovery
dynamics will result in particularly strong feedbacks to
climate change when a critical threshold is passed such
that forests fail to recover (Fig. 5), resulting in dramatic
reductions in C storage and altered biophysical proper-
ties. For example, in semiarid regions such as the US
southwest, current forest communities may not be sup-
ported under future more arid conditions and may not
re-establish following disturbance, resulting in a posi-
tive C cycle feedback (Breshears et al., 2005; Williams
et al., 2010, 2013; Anderson-Teixeira et al., 2011; Rocca-
forte et al., 2012). Thus, recently disturbed forests may
play a key role in shaping terrestrial feedbacks to climate
change.
This review has demonstrated that the dynamics of
forest recovery are likely to be significantly impacted
by rising atmospheric CO
2
and climate change. This
will have repercussions for biodiversity, climate, and
even economics, as the forestry industry and emerging
woody bioenergy industry stand to be affected by
altered forest regeneration rates (Kirilenko & Sedjo,
2007; Metsaranta et al., 2011; Hanewinkel et al., 2013).
Because the course of forest recovery shapes forest
structure and function for decades or centuries, climate
change impacts on secondary forests will have a lasting
legacy. Although the proportion of recently disturbed
forests is relatively small at any given time, disturbance
eventually affects all forests, and the proportion of for-
ests that have regenerated under altered climate condi-
tions will steadily grow. In these ways, climate change
will broadly impact forested regions through its influ-
ence on forest recovery dynamics.
Acknowledgements
Thanks to Jonathan Thompson and Sean McMahon for helpful
discussion and to three anonymous reviewers for helpful com-
ments. This research was supported by DOE grant
#DE-SC0008085 to KJAT, EHD, and BDD.
References
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air
CO
2
enrichment (FACE)? A meta-analytic review of the responses of photo-
synthesis, canopy properties and plant production to rising CO
2
.New Phytolo-
gist,165, 351.
Alberti G, Inglima I, Arriga N et al. (2007) Changes in rainfall patterns in Mediterra-
nean ecosystems: the MIND project. Forest@- Rivista di Selvicoltura ed Ecologia Fore-
stale,4, 460468.
Allen CD, Macalady AK, Chenchouni H et al. (2010) A global overview of drought
and heat-induced tree mortality reveals emerging climate change risks for forests.
Forest Ecology and Management,259, 660684.
Amiro BD, Orchansky AL, Barr AG et al. (2006) The effect of post-fire stand age on
the boreal forest energy balance. Agricultural and Forest Meteorology,140, 4150.
Amiro BD, Barr AG, Barr JG et al. (2010) Ecosystem carbon dioxide fluxes after distur-
bance in forests of North America. Journal of Geophysical Research,115, G00K02.
Anderson KJ (2007a) Rates of change in ecosystem and community properties during succes-
sion. PhD Dissertation; University of New Mexico, Albuquerque, NM.
Anderson KJ (2007b) Temporal patterns in rates of community change during succes-
sion. American Naturalist,169, 780793.
Anderson KJ, Allen AP, Gillooly JF,Brown JH (2006) Temperature-dependence of bio-
mass accumulation rates during secondary succession. Ecology Letters,9, 673682.
Anderson-Teixeira KJ, DeLucia EH (2011) The greenhouse gas value of ecosystems.
Global Change Biology,17, 425438.
Anderson-Teixeira KJ, Vitousek PM (2012) Ecosystems. In: Metabolic Ecology: a Scaling
Approach (eds. Sibley RM, Brown JH, Kodric-Brown A), pp. 99111. Wiley-Black-
well, Chichester.
Anderson-Teixeira KJ, Vitousek PM, Brown JH (2008) Amplified temperature depen-
dence in ecosystems developing on the lava flows of Mauna Loa, Hawai’i. PNAS,
105, 228233.
Anderson-Teixeira KJ, Delong JP, Fox AM, Brese DA, Litvak ME (2011) Differential
responses of production and respiration to temperature and moisture drive the car-
bon balance across a climatic gradient in New Mexico. Global Change Biology,17, 410.
Anderson-Teixeira KJ, Snyder PK, Twine TE, Cuadra SV, Costa MH, DeLucia EH
(2012) Climate-regulation services of natural and agricultural ecoregions of the
Americas. Nature Climate Change,2, 177181.
Babst F, Poulter B, Trouet V et al. (2013) Site- and species-specific responses of forest
growth to climate across the European continent. Global Ecology and Biogeography,
in press.
Bader M, Hiltbrunner E, K
orner C (2009) Fine root responses of mature deciduous
forest trees to free air carbon dioxide enrichment (FACE). Functional Ecology,23,
913921.
Baker TR, Phillips OL, Malhi Y et al. (2004) Increasing biomass in Amazonian forest
plots. Philosophical Transactions of the Royal Society of London Series B-Biological Sci-
ences,359, 353365.
Baldocchi D (2008) “Breathing” of the terrestrial biosphere: lessons learned from a
global network of carbon dioxide flux measurement systems. Australian Journal of
Botany,56,126.
Barber VA, Juday GP, Finney BP (2000) Reduced growth of Alaskan white spruce in
the twentieth century from temperature-induced drought stress. Nature,405,
668673.
Bauweraerts I, Wertin TM, Ameye M, McGuire MA, Teskey RO, Steppe K (2013) The
effect of heat waves, elevated [CO
2
] and low soil water availability on northern
red oak (Quercus rubra L.) seedlings. Global Change Biology,19, 517528.
Bazzaz F (1979) Physiological ecology of plant succession. Annual Review of Ecology
and Systematics,10, 351371.
Bazzaz F (1990) The response of natural ecosystems to the rising global CO
2
levels.
Annual Review of Ecology and Systematics,21, 167196.
Bazzaz FA, Miao SL (1993) Successional status, seed size, and responses of tree seed-
lings to CO
2
, light, and nutrients. Ecology,74, 104112.
Bazzaz FA, Pickett STA (1980) Physiological ecology of tropical succession: a compar-
ative review. Annual Review of Ecology and Systematics,11, 287310.
Beck PSA, Goetz SJ, Mack MC, Alexander HD, Jin Y, Randerson JT, Loranty MM
(2011) The impacts and implications of an intensifying fire regime on Alaskan bor-
eal forest composition and albedo. Global Change Biology,17, 28532866.
Becker M (1989) The role of climate on present and past vitality of silver fir forests in
the Vosges mountains of northeastern France. Canadian journal of forest research,19,
11101117.
Becker M, Nieminen T, G!
er!
emia F (1994) Short-term variations and long-term
changes in oak productivity in northeastern France. The role of climate and atmo-
spheric CO
2
.Annales des Sciences Foresti#
eres,51, 477492.
Beier C, Beierkuhnlein C, Wohlgemuth T et al. (2012) Precipitation manipulation
experiments challenges and recommendations for the future. Ecology Letters,15,
899911.
Bergh J, Linder S, Lundmark T, Elfving B (1999) The effect of water and nutrient
availability on the productivity of Norway spruce in northern and southern Swe-
den. Forest Ecology and Management,119, 5162.
Boisvenue C, Running SW (2006) Impacts of climate change on natural forest produc-
tivity evidence since the middle of the 20th century. Global Change Biology,12,
862882.
Bolker BM, Pacala SW, Bazzaz FA, Canham CD, Levin SA (1995) Species diversity
and ecosystem response to carbon dioxide fertilization: conclusions from a tem-
perate forest model. Global Change Biology,1, 373381.
Bormann FJ, Likens GE (1994) Pattern and Process in a Forested Ecosystem: disturbance,
Development, and the Steady State Based on the Hubbard Brook Ecosystem Study.
Springer-Verlag, Berlin.
Breshears DD, Cobb NS, Rich PM et al. (2005) Regional vegetation die-off in response
to global-change-type drought. Proceedings of the National Academy of Sciences of the
United States of America,102, 1514415148.
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
FOREST RECOVERY UNDER CLIMATE CHANGE 17
Bronson DR, Gower ST (2010) Ecosystem warming does not affect photosynthesis or
aboveground autotrophic respiration for boreal black spruce. Tree Physiology,30,
441449.
Bronson DR, Gower ST, Tanner M, Linder S, Van Herk I (2008) Response of soil sur-
face CO
2
flux in a boreal forest to ecosystem warming. Global Change Biology,14,
856867.
Bronson DR, Gower ST, Tanner M, Van Herk I (2009) Effect of ecosystem warming on
boreal black spruce bud burst and shoot growth. Global Change Biology,15,
15341543.
Brown S, Lugo A (1982) The storage and production of organic matter in tropical for-
ests and their role in the global carbon cycle. Biotropica,14, 161187.
Brown JH, Brown TE, Lomolino M (1998) Biogeography. 2 Sub. Sinauer Associates,
Sunderland, MA.
Bunker DE, DeClerck F, Bradford JC, Colwell RK, Perfecto I, Phillips OL et al. (2005)
Species loss and aboveground carbon storage in a tropical forest. Science,310,
10291031.
Butler S, Melillo J, Johnson J et al. (2012) Soil warming alters nitrogen cycling in a
New England forest: implications for ecosystem function and structure. Oecologia,
168, 819828.
Campbell J, Donato D, Azuma D, Law B (2007) Pyrogenic carbon emission from a
large wildfire in Oregon United States. Journal of Geophysical Research,112, G04014.
Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial com-
munity at elevated CO
2
leads to loss of soil carbon. PNAS,104, 49904995.
Ceulemans R, Mousseau M (1994) Tansley Review No. 71 Effects of elevated atmo-
spheric CO
2
on woody plants. New Phytologist,127, 425446.
Chave J, Condit R, Muller-Landau HC et al. (2008) Assessing evidence for a pervasive
alteration in tropical tree communities. PLoS Biology,6, e45.
Cheesman AW, Winter K (2013) Elevated night-time temperatures increase growth in
seedlings of two tropical pioneer tree species. New Phytologist,197, 11851192.
Clark DA (2002) Are tropical forests an important carbon sink? Reanalysis of the
long-term plot data. Ecological Applications,12,37.
Clark DB, Clark DA, Oberbauer SF (2010) Annual wood production in a tropical rain
forest in NE Costa Rica linked to climatic variation but not to increasing CO
2
.Glo-
bal Change Biology,16, 747759.
Claus A, George E (2005) Effect of stand age on fine-root biomass and biomass distri-
bution in three European forest chronosequences. Canadian Journal of Forest
Research,35, 16171625.
Cleveland CC, Wieder WR, Reed SC, Townsend AR (2010) Experimental drought in a
tropical rain forest increases soil carbon dioxide losses to the atmosphere. Ecology,
91, 23132323.
Cole CT, Anderson JE, Lindroth RL, Waller DM (2010) Rising concentrations of atmo-
spheric CO
2
have increased growth in natural stands of quaking aspen (Populus
tremuloides). Global Change Biology,16, 21862197.
Comstedt D, Bostr
om B, Marshall J, Holm A, Slaney M, Linder S, Ekblad A (2006)
Effects of elevated atmospheric carbon dioxide and temperature on soil respiration
in a boreal forest using
13
C as a labeling tool. Ecosystems,9, 12661277.
Conant RT, Klopatek JM, Klopatek CC (2000) Environmental factors controlling soil res-
piration in three semiarid ecosystems. Soil Science Society of America Journal,64, 383.
Curtis PS, Wang X (1998) A meta-analysis of elevated CO
2
; effects on woody plant
mass, form, and physiology. Oecologia,113, 299313.
Dale VH, Joyce LA, McNulty S et al. (2001) Climate change and forest disturbances.
BioScience,51, 723734.
D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the
grass/fire cycle, and global change. Annual Review of Ecology and Systematics,
23, 6387.
Davi H, Barbaroux C, Francois C, Dufr^
ene E (2009) The fundamental role of reserves
and hydraulic constraints in predicting LAI and carbon allocation in forests. Agri-
cultural and Forest Meteorology,149, 349361.
Davidson EA, de Carvalho CJR, Figueira AM et al. (2007) Recuperation of nitrogen
cycling in Amazonian forests following agricultural abandonment. Nature,447,
995998.
Dawes MA, H
attenschwiler S, Bebi P, Hagedorn F, Handa IT, K
orner C, Rixen C
(2011) Species-specific tree growth responses to 9 years of CO
2
enrichment at the
alpine treeline. Journal of Ecology,99, 383394.
De Graaff M-A, Van Groenigen K-J, Six J, Hungate B, Van Kessel C (2006) Interactions
between plant growth and soil nutrient cycling under elevated CO
2
: a meta-analy-
sis. Global Change Biology,12, 2077.
de Visser PHB, Beier C, Rasmussen L, Kreutzer K, Steinberg N, Bredemeier M et al.
(1994) Biological response of five forest ecosystems in the EXMAN project to input
changes of water, nutrients and atmospheric loads. Forest Ecology and Management,
68, 1529.
DeLucia EH, Hamilton JG, Naidu SL et al. (1999) Net primary production of a forest
ecosystem with experimental CO
2
enrichment. Science,284, 11771179.
Delzon S, Loustau D (2005) Age-related decline in stand water use: sap flow and tran-
spiration in a pine forest chronosequence. Agricultural and Forest Meteorology,129,
105119.
Didham RK, Watts CH, Norton DA (2005) Are systems with strong underlying abi-
otic regimes more likely to exhibit alternative stable states? Oikos,110, 409416.
Dieleman WIJ, Vicca S, Dijkstra FA et al. (2012) Simple additive effects are rare: a
quantitative review of plant biomass and soil process responses to combined
manipulations of CO
2
and temperature. Global Change Biology,18, 26812693.
Dijkstra P, Hymus G, Colavito D et al. (2002) Elevated atmospheric CO
2
stimulates
aboveground biomass in a fire-regenerated scrub-oak ecosystem. Global Change
Biology,8, 90103.
Dillenburg LR, Teramura AH, Forseth IN, Whigham DF (1995) Photosynthetic and
biomass allocation responses of Liquidambar styraciflua (Hamamelidaceae) to vine
competition. American journal of botany,82, 454461.
Donnegan JA, Rebertus AJ (1999) Rates and mechanisms of subalpine forest succes-
sion along an environmental gradient. Ecology,80, 13701384.
Dore S, Kolb TE, Montes-Helu M et al. (2008) Long-term impact of a stand-replacing
fire on ecosystem CO
2
exchange of a ponderosa pine forest. Global Change Biology,
14, 18011820.
Drake JE, Raetz LM, Davis SC, DeLucia EH (2010) Hydraulic limitation not declining
nitrogen availability causes the age-related photosynthetic decline in loblolly pine
(Pinus taeda L.). Plant, Cell and Environment,33, 17561766.
Drake JE, Davis SC, Raetz LM, DeLucia EH (2011a) Mechanisms of age-related
changes in forest production: the influence of physiological and successional
changes. Global Change Biology,17, 15221535.
Drake JE, Gallet-Budynek A, Hofmockel KS et al. (2011b) Increases in the flux of car-
bon belowground stimulate nitrogen uptake and sustain the long-term enhance-
ment of forest productivity under elevated CO
2
.Ecology Letters,14, 349.
Duval BD (2010) The Impact of Elevated CO
2
on N
2
Fixation and Ecosystem Level Element
Cycling. PhD; Northern Arizona University, Flagstaff, AZ.
Edburg SL, Hicke JA, Lawrence DM, Thornton PE (2011) Simulating coupled carbon
and nitrogen dynamics following mountain pine beetle outbreaks in the western
United States. Journal of Geophysical Research,116, G04033.
Enquist BJ, West GB, Brown JH (2009) Extensions and evaluations of a general quanti-
tative theory of forest structure and dynamics. Proceedings of the National Academy
of Sciences,106, 70467051.
Evangelista PH, KumarS, Stohlgren TJ, Young NE (2011) Assessing forest vulnerability
and the potential distribution of pine beetles under current and future climate sce-
narios in the Interior Westof the US. Forest Ecology and Management,262, 307316.
Feeley KJ, Davies SJ, Ashton PS, Bunyavejchewin S, Supardi MNN, Kassim AR et al.
(2007a) The role of gap phase processes in the biomass dynamics of tropical for-
ests. Proceedings of the Royal Society B,274, 28572864.
Feeley KJ, Joseph Wright S, Nur Supardi MN, Kassim AR, Davies SJ (2007b) Deceler-
ating growth in tropical forest trees. Ecology Letters,10, 461469.
Feeley KJ, Davies SJ, Perez R, Hubbell SP, Foster RB (2011) Directional changes in the
species composition of a tropical forest. Ecology,92, 871882.
Ferrell WK, Woodard ES (1966) Effects of Seed Origin on Drought Resistance of
Douglas-Fir (Pseudotsuga Menziesii) (Mirb.) Franco. Ecology,47, 499503.
Ffolliott PF, Stropki CL, Chen H, Neary DG (2011) The 2002 Rodeo-Chediski Wildfire’s
Impacts on Southwestern Ponderosa Pine Ecosystems, Hydrology, and Fuels. U.S.
Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort
Collins, CO.
Finegan B (1984) Forest succession. Nature, UK, 312, 109114.
Finegan B (1996) Pattern and process in neotropical secondary rain forests: the first
100 years of succession. Trends in Ecology and Evolution,11, 119124.
Foster JR, Burton JI, Forrester JA et al. (2010) Evidence for a recent increase in forest
growth is questionable. PNAS,107, E86E87.
Fowells HA, Stark NB (1965) . Natural regeneration in relation to environment in the
mixed conifer forest type of California. Pacific Southwest Forest and Range Experi-
ment Station, Forest Service, US Department of Agriculture, 1965.
Fukami T, Nakajima M (2011) Community assembly: alternative stable states or alter-
native transient states? Ecology Letters,14, 973984.
Gilliam FS (2007) The ecological significance of the herbaceous layer in temperate for-
est ecosystems. BioScience,57, 845858.
Goulden ML, McMillan AMS, Winston GC, Rocha AV, Manies KL, Harden JW,
Bond-Lamberty BP (2011) Patterns of NPP, GPP, respiration, and NEP during bor-
eal forest succession. Global Change Biology,17, 855871.
Gower ST, McMurtrie RE, Murty D (1996) Aboveground net primary production
decline with stand age: potential causes. Trends in Ecology and Evolution,11, 378.
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
18 K. J. ANDERSON-TEIXEIRA et al.
Graumlich LJ, Brubaker LB, Grier CC (1989) Long-term trends in forest net primary
productivity: cascade mountains, Washington. Ecology,70, 405410.
Grimm V, Wissel C (1997) Babel, or the ecological stability discussions: an inventory
and analysis of terminology and a guide for avoiding confusion. Oecologia,109,
323334.
Hall AR, MillerAD, Leggett HC, RoxburghSH, Buckling A, Shea K (2012)Diversitydis-
turbancerelationships: frequencyand intensity interact. BiologyLetters,8, 768771.
Hanewinkel M, Cullmann DA, Schelhaas M-J, Nabuurs G-J, Zimmermann NE (2013)
Climate change may cause severe loss in the economic value of European forest
land. Nature Climate Change,3, 203207.
Hanson PJ, Todd DE, Amthor JS (2001) A six-year study of sapling and large-tree
growth and mortality responses to natural and induced variability in precipitation
and throughfall. Tree Physiology,21, 345358.
H
attenschwiler ST, K
orner CH (2000) Tree seedling responses to in situ CO2-enrich-
ment differ among species and depend on understorey light availability. Global
Change Biology,6, 213226.
Hember RA, Kurz WA, Metsaranta JM, Black TA, Guy RD, Coops NC (2012) Acceler-
ating regrowth of temperate-maritime forests due to environmental change. Global
Change Biology,18, 20262040.
Hicke JA, Allen CD, Desai AR et al. (2011) Effects of biotic disturbances on forest car-
bon cycling in the United States and Canada. Global Change Biology,18,734.
Hooper DU, Adair EC, Cardinale BJ et al. (2012) A global synthesis reveals biodiver-
sity loss as a major driver of ecosystem change. Nature,486, 105108.
Hoosbeek MR, Lukac M, Velthorst E, Smith AR, Godbold DL (2011) Free atmospheric
CO2 enrichment increased above ground biomass but did not affect symbiotic
N2-fixation and soil carbon dynamics in a mixed deciduous stand in Wales. Bio-
geosciences,8, 353364.
Hudiburg TW, Law BE, Thornton PE (2013) Evaluation and improvement of the
Community Land Model (CLM 4.0) in Oregon forests. Biogeosciences,10, 453470.
Hungate BA, Dijkstra P, Johnson DW, Hinkle CR, Drake BG (1999) Elevated CO
2
increases nitrogen fixation and decreases soil nitrogen mineralization in Florida
scrub oak. Global Change Biology,5, 781789.
Hungate BA, Stiling PD, Dijkstra P et al. (2004) CO
2
elicits long-term decline in nitro-
gen fixation. Science,304, 12911291.
Hurtt G, Chini L, Frolking S et al. (2011) Harmonization of land-use scenarios for the
period 15002100: 600 years of global gridded annual land-use transitions, wood
harvest, and resulting secondary lands. Climatic Change,109, 117161.
Hyv
onen R,
$
Agren GI, Linder S et al. (2007) The likely impact of elevated [CO
2
], nitro-
gen deposition, increased temperature and management on carbon sequestration
in temperate and boreal forest ecosystems: a literature review. New Phytologist,
173, 463480.
Ingwell LL, Joseph Wright S, Becklund KK, Hubbell SP, Schnitzer SA (2010) The
impact of lianas on 10 years of tree growth and mortality on Barro Colorado
Island, Panama. Journal of Ecology,98, 879887.
IPCC (2007) Climate Change 2007: the Physical Science Basis. Contribution of working
group I to the fourth assessment report of the intergovernmental panel on climate
change. Cambridge University Press, Cambridge.
Iversen CM (2010) Digging deeper: fine-root responses to rising atmospheric CO
2
concentration in forested ecosystems. New Phytologist,186, 346357.
Jin Y, Randerson JT, Goulden ML, Goetz SJ (2012) Post-fire changes in net shortwave
radiation along a latitudinal gradient in boreal North America. Geophysical Research
Letters,39, L13403.
Jobb!
agy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its
relation to climate and vegetation. Ecological Applications,10, 423436.
Johnson C, Zarin D, Johnson A (2000) Post-disturbance aboveground biomass accu-
mulation in global secondary forests. Ecology,81, 13951401.
Keith H, Mackey BG, Lindenmayer DB (2009) Re-evaluation of forest biomass carbon
stocks and lessons from the world’s most carbon-dense forests. Proceedings of the
National Academy of Sciences,106, 1163511640.
Kerstiens G (1998) Shade-tolerance as a predictor of responses to elevated CO
2
in
trees. Physiologia Plantarum,102, 472480.
Kerstiens G (2001) Meta-analysis of the interaction between shade-tolerance, light
environment and growth response of woody species to elevated CO2. Acta Oeco-
logica,22, 6169.
Kirilenko AP, Sedjo RA (2007) Climate change impacts on forestry. PNAS,104,
1969719702.
Kirschbaum MUF, Whitehead D, Dean SM, Beets PN, Shepherd JD, Ausseil A-GE
(2011) Implications of albedo changes following afforestation on the benefits of for-
ests as carbon sinks. Biogeosciences,8, 36873696.
K
orner C, Asshoff R, Bignucolo O et al. (2005) Carbon flux and growth in mature
deciduous forest trees exposed to elevated CO
2
.Science,309, 13601362.
Krinner G, Viovy N, Noblet-Ducoudr!
eNet al. (2005) A dynamic global vegetation
model for studies of the coupled atmosphere-biosphere system. Global Biogeochemi-
cal Cycles,19, GB1015.
Kubiske ME, Pregitzer KS (1996) Effects of elevated CO
2
and light availability on the
photosynthetic light response of trees of contrasting shade tolerance. Tree Physiol-
ogy,16, 351358.
Kurz WA, Dymond CC, Stinson G et al. (2008) Mountain pine beetle and forest car-
bon feedback to climate change. Nature,452, 987.
Lamarche VC, Graybill DA, Fritts HC, Rose MR (1984) Increasing atmospheric carbon
dioxide: tree ring evidence for growth enhancement in natural vegetation. Science,
225, 10191021.
Langley JA, McKinley DC, Wolf AA, Hungate BA, Drake BG, Megonigal JP (2009)
Priming depletes soil carbon and releases nitrogen in a scrub-oak ecosystem
exposed to elevated CO
2
.Soil Biology and Biochemistry,41, 5460.
Larjavaara M, Muller-Landau HC (2012) Temperature explains global variation in
biomass among humid old-growth forests. Global Ecology and Biogeography,21,
9981006.
Law BE, Sun OJ, Campbell J, Tuyl SV, Thornton PE (2003) Changes in carbon storage
and fluxes in a chronosequence of ponderosa pine. Global Change Biology,9, 510524.
LeDuc SD, Rothstein DE (2010) Plant-available organic and mineral nitrogen shift in
dominance with forest stand age. Ecology,91, 708720.
Lewis SL, Lopez-Gonzalez G, Sonke B et al. (2009) Increasing carbon storage in intact
African tropical forests. Nature,457, 1003.
Li D, Niu S, Luo Y (2012) Global Patterns of the Dynamics of Soil Carbon and Nitrogen
Stocks Following Afforestation: a Meta-Analysis. New Phytologist.
Lichstein JW, Wirth C, Horn HS, Pacala SW (2009) Biomass chronosequences of Uni-
ted States forests: implications for carbon storage and forest management. In: Old-
Growth Forests, Ecological Studies (eds Wirth C, Gleixner G, Heimann M), pp.
301341. Springer, Berlin, Heidelberg.
Liu HP, Randerson JT, Lindfors J, Chapin FS (2005) Changes in the surface energy
budget after fire in boreal ecosystems of interior Alaska: an annual perspective.
Journal of Geophysical Research-Atmospheres,110, D13101.
Lu M, Zhou X, Yang Q et al. (2012) Responses of ecosystem carbon cycle to experi-
mental warming: a meta-analysis. Ecology, in press.
Luo Y, Su B, Currie WS et al. (2004) Progressive nitrogen limitation of ecosystem
responses to rising atmospheric carbon dioxide. BioScience,54, 731739.
Luyssaert S, Inglima I, Jung M et al. (2007) CO
2
balance of boreal, temperate, and
tropical forests derived from a global database. Global Change Biology,13,
25092537.
Luyssaert S, Schulze ED, Borner A et al. (2008) Old-growth forests as global carbon
sinks. Nature,455, 213.
Mack MC, D’Antonio CM (1998) Impacts of biological invasions on disturbance
regimes. Trends in Ecology and Evolution,13, 195198.
Maness H, Kushner PJ, Fung I (2012) Summertime climate response to mountain pine
beetle disturbance in British Columbia. Nature Geoscience,6, 6570.
Mar!
ın-Spiotta E, Cusack D, Ostertag R, Silver W(2008) Trends in above and below-
ground carbon with forest regrowth after agricultural abandonment in the neo-
tropics. In: Post-Agricultural Succession in the Neotropics (ed. Myster RW), pp 2272.
Springer, NewYork, NY.
McCarthy HR, Oren R, Johnsen KH et al. (2010) Re-assessment of plant carbon
dynamics at the Duke free-air CO
2
enrichment site: interactions of atmospheric
[CO
2
] with nitrogen and water availability over stand development. New Phytolo-
gist,185, 514528.
McKinley DC, Romero JC, Hungate BA, Drake BG, Megonigal JP (2009) Does deep
soil N availability sustain long-term ecosystem responses to elevated CO
2
?Global
Change Biology,15, 20352048.
McMahon SM, Parker GG, Miller DR (2010a) Evidence for a recent increase in forest
growth. Proceedings of the National Academy of Sciences,107, 36113615.
McMahon SM, Parker GG, Miller DR (2010b) Reply to Foster et al.: using a forest to
measure trees: determining which vital rates are responding to climate change.
PNAS,107, E88E89.
McMillan AMS, Winston GC, Goulden ML (2008) Age-dependent response of boreal
forest to temperature and rainfall variability. Global Change Biology,14, 19041916.
Medvigy D, Wofsy SC, Munger JW, Hollinger DY, Moorcroft PR (2009) Mechanistic
scaling of ecosystem function and dynamics in space and time: ecosystem demog-
raphy model version 2. Journal of Geophysical Research,114, G01002.
Melillo JM, Steudler PA, Aber JD et al. (2002) Soil warming and carbon-cycle feed-
backs to the climate system. Science,298, 21732176.
Melillo JM, Butler S, Johnson J et al. (2011) Soil warming, carbon-nitrogen interac-
tions, and forest carbon budgets. Proceedings of the National Academy of Sciences,
108, 95089512.
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
FOREST RECOVERY UNDER CLIMATE CHANGE 19
Metsaranta JM, Dymond CC, Kurz WA, Spittlehouse DL (2011) Uncertainty of 21st
century growing stocks and GHG balance of forests in British Columbia, Canada
resulting from potential climate change impacts on ecosystem processes. Forest
Ecology and Management,262, 827837.
Miller AD, Roxburgh SH, Shea K (2011) How frequency and intensity shape diver-
sitydisturbance relationships. PNAS,108, 56435648.
Mohan JE, Ziska LH, Schlesinger WH, Thomas RB, Sicher RC, George K, Clark JS
(2006) Biomass and toxicity responses of poison ivy (Toxicodendron radicans) to
elevated atmospheric CO
2
.PNAS,103, 90869089.
Mohan JE, Clark JS, Schlesinger WH (2007) Long-term CO
2
enrichment of a forest
ecosystem: implications for forest regeneration and succession. Ecological Applica-
tions,17, 11981212.
Moles AT, Flores-Moreno H, Bonser SP et al. (2012) Invasions: the trail behind, the
path ahead, and a test of a disturbing idea. Journal of Ecology,100, 116127.
Nepstad DC, Moutinho P, Dias-Filho MB et al. (2002) The effects of partial throughfall
exclusion on canopy processes, aboveground production, and biogeochemistry of
an Amazon forest. Journal of Geophysical Research,107, 8085.
Nepstad DC, Tohver IM, Ray D, Moutinho P, Cardinot G (2007) Mortality of large
trees and lianas following experimental drought in an amazon forest. Ecology,88,
22592269.
Nilsson M-C, Wardle DA (2005) Understory vegetation as a forest ecosystem driver:
evidence from the northern Swedish boreal forest. Frontiers in Ecology and the Envi-
ronment,3, 421428.
Norby RJ, Zak DR (2011) Ecological lessons from free-air CO
2
enrichment (face)
experiments. Annual Review of Ecology, Evolution, and Systematics,42, 181203.
Norby RJ, DeLucia EH, Gielen B et al. (2005) Forest response to elevated CO
2
is con-
served across a broad range of productivity. Proceedings of the National Academy of
Sciences of the United States of America,102, 1805218056.
Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtrie RE (2010) CO
2
enhance-
ment of forest productivity constrained by limited nitrogen availability. Proceed-
ings of the National Academy of Sciences,107, 1936819373.
Odion DC, Moritz MA, DellaSala DA (2010) Alternative community states main-
tained by fire in the Klamath Mountains, USA. Journal of Ecology,98, 96105.
O’Halloran TL, Law BE, Goulden ML et al. (2012) Radiative forcing of natural forest
disturbances. Global Change Biology,18, 555565.
Oren R, Ellsworth DS, Johnsen KH et al. (2001) Soil fertility limits carbon sequestra-
tion by forest ecosystems in a CO
2
-enriched atmosphere. Nature,411, 469472.
Pan Y, Birdsey RA, Fang J et al. (2011) A large and persistent carbon sink in the
world’s forests. Science,333, 988993.
Pendall E, Bridgham S, Hanson PJ et al. (2004) Below-ground process responses to
elevated CO
2
and temperature: a discussion of observations, measurement meth-
ods, and models. New Phytologist,162, 311322.
Pe~
nuelas J, Filella I, Tognetti R (2001) Leaf mineral concentrations of Erica arborea,
Juniperus communis and Myrtus communis growing in the proximity of a natural
CO
2
spring. Global Change Biology,7, 291301.
Phillips OL, V!
asquez Mart!
ınez R, Arroyo L et al. (2002) Increasing dominance of large
lianas in Amazonian forests. Nature,418, 770774.
Plaut JA, Yepez EA, Hill J, Pangle R, Sperry JS, Pockman WT, McDowell N(2012)
Hydraulic limits preceding mortality in a pi~
nonjuniper woodland under experi-
mental drought. Plant, Cell and Environment,35, 16011617.
Prach K, Rehounkov!
a K (2006) Vegetation succession over broad geographical scales:
which factors determine the patterns? Preslia,78, 469480.
Prach K, Pysek P, Jarosik V (2007) Climate and pH as determinants of vegetation suc-
cession in Central European man-made habitats. Journal of Vegetation Science,18,
701710.
Pregitzer KS, Euskirchen ES (2004) Carbon cycling and storage in world forests:
biome patterns related to forest age. Global Change Biology,10, 20522077.
Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration
and its relationship to vegetation and climate. Tellus B,44, 8199.
Randerson JT, Liu H, Flanner MG et al. (2006) The impact of boreal forest fire on cli-
mate warming. Science,314, 11301132.
Richter S, Kipfer T, Wohlgemuth T, Calder!
on Guerrero C, Ghazoul J, Moser B (2012)
Phenotypic plasticity facilitates resistance to climate change in a highly variable
environment. Oecologia,169, 269279.
Roberts S, Vertessy R, Grayson R (2001) Transpiration from Eucalyptus sieberi (L. John-
son) forests of different age. Forest Ecology and Management,143, 153161.
Roccaforte JP, Ful!
e PZ, Chancellor WW, Laughlin DC (2012) Woody debris and tree
regeneration dynamics following severe wildfires in Arizona ponderosa pine for-
ests. Canadian Journal of Forest Research,42, 593604.
Rollinson CR (2010) Simulated Climate Change Alters Post-Clear Cut Forest Vegetation
Communities. M.S.; Penn State University, State College, PA.
Rollinson CR, Kaye MW (2011) Experimental warming alters spring phenology of
certain plant functional groups in an early-successional forest community. Global
Change Biology,18, 11081116.
Romme WH, Knight DH (1981) Fire frequency and subalpine forest succession along
a topographic gradient in wyoming. Ecology,62, 319326.
Running SW (2008) Ecosystem disturbance, carbon, and climate. Science,321, 652653.
Russell AE, Raich JW (2012) Rapidly growing tropical trees mobilize remarkable
amounts of nitrogen, in ways that differ surprisingly among species. PNAS,109,
1039810402.
Rustad L, Campbell J, Marion G et al. (2001) A meta-analysis of the response of soil
respiration, net nitrogen mineralization, and aboveground plant growth to experi-
mental ecosystem warming. Oecologia,126, 543562.
Salzer MW, Hughes MK, Bunn AG, Kipfmueller KF (2009) Recent unprecedented
tree-ring growth in bristlecone pine at the highest elevations and possible causes.
PNAS,106, 2034820353.
Sasek TW, Strain BR (1990) Implications of atmospheric CO
2
enrichment and climatic
change for the geographical distribution of two introduced vines in the U.S.A. Cli-
matic Change,16, 3151.
Savage M, Mast JN (2005) How resilient are southwestern ponderosa pine forests
after crown fires? Canadian Journal of Forest Research,35, 967977.
Saxe H, Ellsworth DS, Heath J (1998) Tree and forest functioning in an enriched CO
2
atmosphere. New Phytologist,139, 395436.
Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in eco-
systems. Nature,413, 591596.
Scheffer M, Hirota M, Holmgren M, Nes EHV, Chapin FS (2012) Thresholds for bor-
eal biome transitions. PNAS,109, 2138421389.
Schnitzer SA, Bongers F (2011) Increasing liana abundance and biomass in tropical
forests: emerging patterns and putative mechanisms. Ecology Letters,14, 397406.
Schnitzer SA, Carson WP (2010) Lianas suppress tree regeneration and diversity in
treefall gaps. Ecology Letters,13, 849857.
Schr
oder A, Persson L, De Roos AM (2005) Direct experimental evidence for alterna-
tive stable states: a review. Oikos,110,319.
Schuldt B, Leuschner C, Horna V, Moser G, K
ohler M, van Straaten O, Barus H (2011)
Change in hydraulic properties and leaf traits in a tall rainforest tree species sub-
jected to long-term throughfall exclusion in the perhumid tropics. Biogeosciences,8,
21792194.
Seiler TJ, Rasse DP, Li J et al. (2009) Disturbance, rainfall and contrasting species
responses mediated aboveground biomass response to 11 years of CO
2
enrich-
ment in a Florida scrub-oak ecosystem. Global Change Biology,15, 356367.
Shafi MI, Yarranton GA (1973) Diversity, floristic richness, and species evenness dur-
ing a secondary (post-fire) succession. Ecology,54, 897902.
Shea K, Chesson P (2002) Community ecology theory as a framework for biological
invasions. Trends in Ecology and Evolution,17, 170176.
Slaney M, Wallin G, Medhurst J, Linder S (2007) Impact of elevated carbon dioxide
concentration and temperature on bud burst and shoot growth of boreal norway
spruce. Tree Physiology,27, 301312.
Smithwick EAH (2011) Pyrogeography and biogeochemical resilience. In: The Land-
scape Ecology of Fire, Ecological Studies (eds McKenzie D, Miller C, Falk DA, Cald-
well MM, Heldmaier G, Jackson RB et al.), pp. 143163. Springer, Netherlands.
Smithwick EAH, Ryan MG, Kashian DM, Romme WH, Tinker DB, Turner MG (2009)
Modeling the effects of fire and climate change on carbon and nitrogen storage in
lodgepole pine (Pinus contorta) stands. Global Change Biology,15, 535548.
Sotta ED, Veldkamp E, Schwendenmann L et al. (2007) Effects of an induced drought
on soil carbon dioxide (CO
2
) efflux and soil CO
2
production in an Eastern Amazo-
nian rainforest, Brazil. Global Change Biology,13, 22182229.
Soul!
e PT, Knapp PA (2006) Radial growth rate increases in naturally occurring pon-
derosa pine trees: a late-20th century CO
2
fertilization effect? New Phytologist,171,
379390.
Souza L, Belote RT, Kardol P, Weltzin JF, Norby RJ (2010) CO
2
enrichment accelerates
successional development of an understory plant community. Journal of Plant Ecol-
ogy,3, 3339.
Spiecker H (1999) Overview of recent growth trends in European forests. Water, Air,
and Soil Pollution,116, 3346.
Staver AC, Archibald S, Levin S (2011) Tree cover in sub-Saharan Africa: rainfall and
fire constrain forest and savanna as alternative stable states. Ecology,92,
10631072.
Stromayer KAK, Warren RJ (1997) Are overabundant deer herds in the eastern united
states creating alternate stable states in forest plant communities? Wildlife Society
Bulletin,25, 227234.
Sturrock RN, Frankel SJ, Brown AV et al. (2011) Climate change and forest diseases.
Plant Pathology,60, 133149.
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
20 K. J. ANDERSON-TEIXEIRA et al.
Thomas PA, Wein RW (1985) Water availability and the comparative emergence of
four conifer species. Canadian Journal of Botany,63, 17401746.
Thompson J, Spies T (2010) Factors associated with crown damage following recur-
ring mixed-severity wildfires and post-fire management in southwestern Oregon.
Landscape Ecology,25, 775789.
Thompson I, Mackey B, McNulty S, Mosseler A(2009) Forest Resilience, Biodiversity,
and Climate Change. Secretariat of the Convention on Biological Diversity, Mon-
treal. Technical Series. Vol. 43. 2009
Thornton PE, Lamarque J-F, Rosenbloom NA, Mahowald NM (2007) Influence of car-
bon-nitrogen cycle coupling on land model response to CO
2
fertilization and
climate variability. Global Biogeochemical Cycles,21, GB4018.
Tingey DT, Lee EH, Phillips DL, Rygiewicz PT, Waschmann RS, Johnson MG, Olszyk
DM (2007) Elevated CO
2
and temperature alter net ecosystem C exchange in a
young Douglas fir mesocosm experiment. Plant, Cell and Environment,30,
14001410.
Uhl C, Jordan CF (1984) Succession and nutrient dynamics following forest cutting
and burning in Amazonia. Ecology,65, 14761490.
US DOE (2011). US Billion-Ton Update. Biomass Supply for a Bioenergy and Bioproducts
Industry. Oak Ridge National Laboratory, Oak Ridge, TN.
Vasconcelos SS, Zarin DJ, Ara!
ujo MM, de Miranda I, S. (2012) Aboveground net pri-
mary productivity in tropical forest regrowth increases following wetter dry-
seasons. Forest Ecology and Management,276, 8287.
Vitousek P, Matson P, Cleve K (1989) Nitrogen availability and nitrification during
succession: primary, secondary, and old-field seres. Plant and Soil,115, 229239.
Voelker SL (2011) Age-dependent changes in environmental influences on tree
growth and their implications for forest responses to climate change. In: Size- and
Age-Related Changes in Tree Structure and Function, Tree Physiology (eds Meinzer
FCC, Lachenbruch B, Dawson TEE, Meinzer FC, Niinemets
U), pp. 455479.
Springer, Netherlands.
Vogt KA, Moore EE, Vogt DJ, Redlin MJ, Edmonds RL (1983) Conifer fine root and
mycorrhizal root biomass within the forest floors of Douglas-fir stands of different
ages and site productivities. Canadian Journal of Forest Research,13, 429437.
Volder A, Briske DD, Tjoelker MG (2012) Climate warming and precipitation redistri-
bution modify tree-grass interactions and tree species establishment in a warm-
temperate savanna. Global Change Biology,19, 843857.
Wan S, Norby RJ, Pregitzer KS, Ledford J, O’Neill EG (2004) CO
2
enrichment and
warming of the atmosphere enhance both productivity and mortality of maple tree
fine roots. New Phytologist,162, 437446.
Westerling AL, Hidalgo HG, Cayan DR, Swetnam TW (2006) Warming and earlier
spring increase western US forest wildfire activity. Science,313, 940943.
Westerling AL, Turner MG, Smithwick EAH, Romme WH, Ryan MG (2011) Continued
Warming Could Transform Greater Yellowstone Fire Regimes by Mid-21st Century. Pro-
ceedings of the National Academy of Sciences.
Williams AP, Allen CD, Millar CI, Swetnam TW, Michaelsen J, Still CJ, Leavitt SW
(2010) Forest responses to increasing aridity and warmth in the southwestern Uni-
ted States. PNAS,107, 2128921294.
Williams AP, Allen CD, Macalady AK et al. (2013) Temperature as a potent driver of
regional forest drought stress and tree mortality. Nature Climate Change,3,
292297.
Wright IJ, Reich PB, Westoby M et al. (2004) The worldwide leaf economics spectrum.
Nature,428, 821827.
Wu Z, Dijkstra P, Koch GW, Pe~
nuelas J, Hungate BA (2011) Responses of terrestrial
ecosystems to temperature and precipitation change: a meta-analysis of experi-
mental manipulation. Global Change Biology,17, 927942.
Yang Z, Cohen WB, Harmon ME (2005) Modeling early forest succession following
clear-cutting in western Oregon. Canadian Journal of Forest Research,35, 18891900.
Yang Y, Luo Y, Finzi AC (2011) Carbon and nitrogen dynamics during forest stand
development: a global synthesis. New Phytologist,190, 977989.
Yavitt JB, Wright SJ (2008) Seedling growth responses to water and nutrient augmen-
tation in the understorey of a lowland moist forest, Panama. Journal of Tropical
Ecology,24, 1926.
Yuan ZY, Chen HYH (2010) Fine root biomass, production, turnover rates, and nutri-
ent contents in boreal forest ecosystems in relation to species, climate, fertility, and
stand age: literature review and meta-analyses. Critical Reviews in Plant Sciences,
29, 204221.
Zaehle S, Friend AD (2010) Carbon and nitrogen cycle dynamics in the O-CN land
surface model: 1 Model description, site-scale evaluation, and sensitivity to param-
eter estimates. Global Biogeochemical Cycles,24, GB1005.
Zanetti S, Hartwig UA, Luscher A et al. (1996) Stimulation of Symbiotic N
2
Fixation
in Trifolium repens L. under Elevated Atmospheric pCO
2
in a Grassland Ecosystem.
Plant Physiology,112, 575583.
Zhou G, Liu S, Li Z et al. (2006) Old-growth forests can accumulate carbon in soils.
Science,314, 1417.
Zhou Y, Tang J, Melillo JM, Butler S, Mohan JE (2011) Root standing crop and chemis-
try after 6 years of soil warming in a temperate forest. Tree Physiology,31, 707717.
Supporting Information
Additional Supporting Information may be found in the
online version of this article:
Table S1. Summary of experimental manipulations of CO
2
in tree-dominated ecosystems through Free-Air Carbon
dioxide Enrichment (FACE), Open Top Chamber (OTC), or
Whole Tree Chamber (WTC; in situ only) methodology.
Table S2. Summary of experimental warming in tree-domi-
nated ecosystems (listed in order of forest age).
Table S3. Summary of experimental manipulations of pre-
cipitation (PPT) in tree-dominated ecosystems (listed in
order of forest age).
Published 2013. This article is a U.S. Government work and is in the public domain in the USA., Global Change Biology, doi: 10.1111/
gcb.12194
FOREST RECOVERY UNDER CLIMATE CHANGE 21
... Recovery is a key ecological process that influences forest stability, structure, and function in the face of extreme events (Anderson-Teixeira et al. 2013;Hodgson et al. 2015;Donohue et al. 2016). Tree recovery is defined as the capacity of a system to return to a stable state and function after a disturbance (Ingrisch & Bahn 2018;Gessler et al. 2020). ...
... low NDVI values). Such repetitive droughts can alter the recovery time and push the forest beyond the "tipping point"-associated with tree mortality -and lead to a deterioration of the forest ecosystem (Anderson-Teixeira et al. 2013;Schwalm et al. 2017). We showed that the NDVI in 2015 is slightly lower that in 2020, most likely due to the 2015 drought period and heatwave from Central Europe that had a lower intensity than in 2018. ...
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... For communities dominated by long-lived and slowgrowing organisms, the study of recruitment dynamics is particularly timely as mortality events linked to climate driven disturbances are becoming increasingly severe (Anderson-Teixeira et al. 2013;Hughes et al. 2019;Schweiger et al. 2020). Such systems typically possess an ensemble of strategies such as seed banks, clonality, and asexual propagation that allow rapid recovery following perturbation. ...
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